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Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum
Brain Research Reviews, 6 (1983) 247-297
247
Elsevier
Functional Anatomy of the Tectum Mesencephali of the Goldfish. An Explorative Analysis of the Functional Implications of the Laminar Structural Organization of the Tectum J. MEEK Department of Anatomy and Embryology,
University of Nijmegen, Faculty of Medicine, Geert Grooteplein Noord 21, Postbus 9101, 6500 HB Nijmegen (The Netherlands)
(Accepted August 8th, 1983) Key worak: tectum mesencephali -
goldfish - teleosts - laminar organization - functional anatomy - circuitry analysis connectivity matrix - multimodal integration
CONTENTS 1. Introduction
.............................................................................................................................................
248
2. Survey of the structural tectal organization ....................................................................................................... 2.1. Tectal afferents ................................................................................................................................... 2.1.1. Origin of tectal afferents ............................................................................................................... 2.1.2. Topographicorganizationof tectal afferents ...................................................................................... 2.1.3. Laminar organization of tectal afferents ............................................................................................ 2.1.4. Quantitative properties of tectal afferents ......................................................................................... 2.2. Intrinsic tectal strutture ........................................................................................................................ 2.2.1. Tectal neurons ........................................................................................................................... 2.2.2. Synaptic organization of the tectum ................................................................................................. 2.3. Tectal efferents ................................................................................................................................... 2.3.1. Tectal targets ............................................................................................................................. 2.3.2. Efferent tectal cell types ................................................................................................................
251 251 251 251 253 254 255 255 256 258 258 259
3. A conceptual framework of tectal circuitry ....................................................................................................... 3.1. Startineooints .................................................................................................................................... .............................................................................. 3.1.1. The lamination pattern of tectal neuronalelements 3.1 .l .l. Tectal afferents .............................................................................................................. 3.1.1.2. Tectal interneurons ......................................................................................................... 3.1.1.3. Efferent tectal neurons ..................................................................................................... 3.1.2. Presynaptic tectal zones ................................................................................................................ 3.1.3. Postsynaptic determinationof neuronal input ..................................................................................... 3.1.4. The hypothesisof laminar specificity ................................................................................................ 3.1.4.1, Generai considerations ..................................................................................................... 3.1.4.2. Laminar specificity in tectal circuitry .................................................................................... 3.1.4.3. Quantitative elaboration of laminar specificity in tectal circuitry ................................................. 3.1.4.4. Considerations regarding type XIV neurons .......................................................................... 3.2. Calculation of the connectivity index and the connettive importance ................................................................ 3.2.1. Connectivity index ...................................................................................................................... 3.2.2. Connettive importance ................................................................................................................ 3.3. Analysis of tectal circuitry ...................................................................................................................... 3.3.1. Tectal circuitry involved in toral input processing ................................................................................ 3.3.2. Tectal circuitry involved in visual input processing ............................................................................... 3.3.3. Tectal circuitry involved in telencephalic input processing ..................................................................... 3.3.4. Tectal circuitry involved in ‘deep’ tectal input processing ....................................................................... 3.35. The connettive importance of tectal afferents in the different tectal layers ................................................. 3.3.6. The connettive relations of the tectal ce11types ................................................................................... 3.4. Critica1 evaluation of the framework presented ...........................................................................................
260 260 261 261 262 263 263 263 264 264 264 265 266 266 267 261 268 268 270 272 274 275 276 27X
0165-0173/83/$03.00 0 1983 Elsevier Science Publishers B.V.
248 4. Survey of physiological data .......................................................................................................................... 4.1. Toral input processing .......................................................................................................................... 4.2. Visual input processing ......................................................................................................................... 4.2.1. Responses after electrical stimulation of the optic nerve ........................................................................ 4.2.2. Visual responses of retina1 fiber terminals ....... .................................................................................. 4.2.3. Visual responses of tectal neurons ................................................................................................... 4.3. Deep tectal input processing-multimodality .............................................................................................. 4.4. Tectal efferents ...................................................................................................................................
279 279 280 280 280 281 283 283
5. Comparison
284
6. Summary
of structural and Conclusion
and physiological
data
................................................................................................
.............................................................................................................................
7. Appendix .......................................................................... ..................................................................... 7.1. Alternative 1 ...................................................................................................................................... 7.2. Alternative 2 ., ,. _. ..... _, ..
_.
Acknowledgements Abbreviations
._.....
References
.... ___. ,.
.___
285 286 287 288 290
._.
290
_.
1. INTRODUCTION
The tectum mesencephali or optic tectum constitutes the most highly developed part of the brain of fish (Figs. 1 and 2). In most teleosts this strutture is differentiated into 7 layers which from deep to superficial are indicated as follows: layer 1 or stratum periventriculare (SPV); layer 2 or stratum centrale (SAC); layers 3 and 4, together named stratum griseum centrale (SGC), while layer 4 is also called the inner plexiform layer (IPL); layer 5 or stratum fibrosum et griseum superficiale (SFGS); layer 6 or straturn opticum (SO) and layer 7 or stratum marginale (SM). In goldfish, the thickness of the tectum is about 600pm. A second marked feature of the tectum is the precise topographic organization of the retinotectal projection. A large number of aspects concerning the structure and function of the teleostean tectum has been investigated in a variety of species (Table 1). Unti1 now. however, no attempt has been made to obtain an integrated concept from al1 these data. The main purpose of the present paper is to explore in which way and to which extent such a functional anatomica1 concept is possible at present, in particular with respect to the laminar organization. This exploration is primarily based on the goldfish, since for this species the most complete set of data is available (see Table 1). In addition, data on other teleosts will be used for comparison. The design of the present paper is as follows: at
290
first, the results available on the structural tectal organization will be reviewed briefly and summarized in a number of schemes. Secondly, tectal circuitry will be analyzed qualitatively and quantitatively on the basis of the structural data available and the concept of laminar specificity. The starting points and methodology of this analysis will be presented in substantia1 detail in order to enable extensive evaluation
c
MOuhw-~
Fig. 1. The brain of the goldfish. a, in situ: b, dorsal view; c, latera1 view. b.olf.. bulbus olfactorius; cereb., cerebellum; hypoth.. hypothalamus; med. spiri., medulla spinalis; rhomb.. rhombencephalon; telenc., telencephalon.
249
Fig. 2. Transverse sections through the tectum mesencephali of the goldfish. Top: the position of the tectum shown at low magnification (Lux01 fast blue-Cresyl fast violet staining). TL, torus longitudinalis; TS, torus semicircularis; ‘ITB, tractus tetto-bulbaris. Bottom: the tectal layers in a section stained with Hematoxilin-Eosin, SAC, stratum album centrale; SFGS, stratum fibrosum et griseum superficiale; SGC, stratum griseum centrale; SM, stratum marginale; SO, stratum opticum; SPV, stratum periventriculare. The numerical indication of these layers and their boundary regions ls*is presented at the right side.
of the specific tectal- as well as the more genera1 neurobiological-applicability of the analysis performed. Thirdly, the inferences of the structural circuitry analysis will be compared with physiological data in
order to explore to which extent the functional anatomy of the teleostean tectum is unravelled at present and in which way more definite insight may be obtained in the future.
TABLE 1 Literature dealing with tetta of teleosts Goldfish (Carassio
Connections Afferents Retino-tectal (topographical) Retino-tectal (laminar)
auratus) Other cyprinids’
Other teleo&*
115,116,154,156,230 79,130,167,168,219,231,240
135,230 184,197,198
2,83,84,177
107,108,109,137,144
Efferents Retina1 projections
83,84 63,201,231,240,241
137 184,197,198,201
Retinopetal fibers
163,219,240,253
163,184
Other afferents
Morphology Development Comparative gross morphology Golgi-studies Ultrastructure Optic nerve and tract Neurochemistry Chemoarchitectonics Neurotransmitters Acetylcholine
Glutamate GABA Monoamines RNA/Protein synthesis Electrophysiology E.E.G. Evoked potentials Visual stimulation Optic nerve stimulation Nou-retina1 afferent stimulation Saccade-related Multi-unit responses Retinotectal topography Single unit responses, extra cellular Visual units
4,12,13,22,127,229,230 7,49,51,57,59,89,130,132,136,157, 186,188,198,258,268 11,27,54,109,110,164,207,224,234. 259 27,54,111.112,207,214,224,234 7,24,26,49,51,53,57,59,63,89,157, 175,186,188,189,201,258,268, 52,76,157,158,162,163,208,253, 256
142,155
15,117,118,185,190,217,218 8***,119,120,222,232,235,242,277 13,17,40,41,120,133,186,192,193, 225,226,255.263 6,31,32,106.118,12S,131,132 56,223,250,251
133,148,152,200
103,133,192,193
3,149,150,166,246,248,267 16,48,95,145,165,204
31,103,144
129.140
272
272
35-37,39,66,68,69,70,72, 160,178,187,213,221,228, 266 67 187,267 38
160
34,35,39,160.266
126,196,233
180 195,196
1
183
60,93,247
1,101,124,189,199,211,212 125,219,249,252
183,189,227 146 265
10,93,124,247 18-21.23,125,161,257,260-262 264
96
115,116,154
22,127,229,230
42,75,90,91,113-115, 138,176,199,215,216,249, 269,270,271 25,64,90,176 70,202
90,146,171,173,174,194, 209,210
73,74,90,91,92,134,141,205,206. 254,257,261,262,280
171 147,172
12.64,73,205 202 275
Behavioral responses After tectal stimulation After tectal ablation
239,279
45,119
Plasticity and specificity
55,97,220$
Non-visual and multimodal units Single unit responses, intracellular Tectal targets
Including: the crucian carp (Carassiw IOX.IOY.133.137.146.194.1Y7.198.227.230.265;
Tinca
tinca
carassius)
5.29,30,43,44,61,159 14,45,119
IW.119.126.144.147~171.172.173.174.196.20.2ll~.233;
lM).183.184~lR9.198~272;
Alburnus
the
alburnusl84.198;
Barbus
carp
(Cyprinw
fluvia~il&lY2.l98;
~a~pio)3l,l~l3.~~~7, ,dus
~p,9~1.163.201;
Phoxinus s~.~“.l~8;Rutilis rutilti’~J97.‘98; and Scardinus erythrophthalmusl~J98.
Results obtained with about 50 different species (except for the comparative morphological studies). The most frequently used Icralurus sp, l1.l8.19.20.21.22.23.3S,39.63,l33.160.1. species are: Salmo sp. 4.5.13.15.3l.35.39.73.74.90.91.117.118.133.134.1M1.185.180.198; Eugerres I27.MO.230;
plumien ffo/ocen,rus
54,,31.132,2S0,251.254,255.256.257.258.259.260.261.262.263.264.275. sp,26.54.100,226.259.275;
a,,d
other teleost. Review, with omission of previous literature. Only some recent reviews have been indicated.
Navodo,,
Aslyanax modes~usl~9Jl”.lll.l~2,2~~7.2S3,
~p,6.56.oJ.Zl7.2IX.234.26U~ N o
Lepomis
~p,24.14.60.6~,
more than 4 references dea1 with any
251 2. SURVEY
OF THE STRUCTURAL
TECTAL
ORGANI-
ZATION
ally to the tectuml37. The projection alic area dorsalis been investigated
2.1. 2.1.1.
Tectal afferents
source
of tectal
afferents
is the
retina, not only in teleosts, but in al1 vertebrates. A massive contralateral retinotectal projection has been described
of the telenceph-
to the carp tectum
has
in detail by Ito and Kishidai07, who
also published an extensive study on the connections of the carp torus longitudinalislas. The torus longi-
Origin of tectal afferents
The best-known
centralis
by many authors for a variety of tele-
osts, including goldfish (Table 1). Springer and Gaffney*a’ and Prasada-Rao and Sharmaiss recently reported a small additional ipsilateral retinotectal projection in goldfish and catfish, respectively. Although by far most retina1 fibers project to the tecturn, severa1 other brain centers receive retina1 projection as well, either exclusively contralateral or bilateral (for references, see Table 1). These centers include (1) the preoptic hypothalamic region; (2) nuclei in the dorsolateral and ventrolateral thalamus; (3) pretectal nuclei and (4) so-called accessory optic nuclei in the rostral mesencephalon. Detailed discussions on the retina1 projections and possible speciesspecific andior technique dependent variations have recently been presented by Springer and Gaffney240 and Prasada-Rao and Sharmai8s. Apart from the retina, in goldfish a number of nuclei project to the tectum as well, as has been demonstrated by Grover and Sharmas4 with the aid of retrograde HRP-transport. These nuclei include one telencephalic area (area dorsalis centralis), 3 diencephalic nuclei (nucleus dorsolateralis, area pretectalis and nucleus pretectalis), 6 mesencephalic structures (torus longitudinalis, contralateral tectal half, nucleus of the rostral mesencephalic tegmentum, torus semicircularis, nucleus dorsolateralis tegmenti and nucleus isthmi) and one rhombencephalic nucleus (nucleus reticularis superior) (Fig. 3A). The telencephalo-tectal projection in the goldfish has also been described by Airhartl and Oka and Uedai77. Whereas Grover and Sharmas4 found an exclusively ipsilatera1 telencephalotectal projection, Airhart* and Oka and Uedai77 described a bilatera1 projection. In the carp, Luitent37 has obtained results closely resembling those of Grover and Sharmas4 in the related goldfish. In addition, in the carp the nucleus preopticus appears to project to the tectum, while the pretectum projects not only ipsi- but also contralater-
tudinalis appears to project exclusively to the ipsilatera1 tectum, whereas afferents to this torus originate almost exclusively vula cerebelli
in the valvula cerebelliio*. The val-
is a cerebellar
actinopterygians, longitudinalisi70.
just
strutture
as the
With respect to non-cyprinid
only present in
mesencephalic
torus
teleosts the following
results are available. Telencephalo-tectal projections have been described for Eugerres, Holocentru.9, Zctalurusl* and 5 other specie@. Commissural intertectal fibers have been demonstrated in Eugerres,
Holocentru64 and Astyanax234. The isthmotectal projection has been studied extensively in Navodonll0.207. The torus semicircularis is the largest
nucleus of the mesencephalic tegmentum and receives most of its input from auditory and lateral-line sensory systernslos.1*1.170~214.The tectal projection of the torus semicircularis has recently been described extensively by Carr et al.27 for gymnotiform teleosts. These are electric fish in which the torus semicircularis receives an important electrosensory inputt*,z’. In such teleosts, the tectum receives a well-developed ipsilateral projection from the torus semicircularis, just as has been described for the non-electrosensory goldfish and carp. In Xiphophorus, Miinz et al.164 have described a population of LH-RH (luteinizing hormone-releasing hormone) positive fibers in the tectum, which probably originate from LH-RH positive neurons in the midbrain. 2.1.2. Topographic organization of tectal afferents The topographic organization of the retino-tectal projection is a general, well-known principle for al1 vertebrates. For goldfish, the retinotopic organization of the retinotectal projection has been investigated electrophysiologically by Jacobson and Gazetis%ii6 and histologically by Meyerts6. It has been confirmed by many authors who used the goldfish retino-tectal system for experiments dealing with specificity and plasticity of nervous connections (for review see refs. 5.5 and 97) and has been described for a number of other teleosts as wel14~12.13.22.1*7.135.*30. Recently, it has been shown that the optic nerve and
252
;I
,homb
or M Tect
I
Te
FRI
TL
i
-c
NDL
f
-
Ret i
7,
Ret C
B Fig. 3. Schematic representation of present knowledge concerning the extrinsic connections of the goldfish tectum. A: afferent tectal connections (for details and references. see section 2.1.1). B: efferent tectal connections (for details and references, see section 2.3.1).
tract
also
rather
have
complex
a retinotopic
one
organization,
(Astronotus223
albeit
and
a
gold-
fiShl6.48.2ll4),
Topographic order has been described for 4 other tectal afferent systems, unti1 now, however, each in different teleosts. First, the commissural intertectal fibers appear to connect preferentially homotopic tectal regions in Eugerres and Holocentrus54 as well as in goldfishsJ.84. Secondly, the projection of the torus longitudinalis to the tectum, extensively studied by Ito and Kishidalos in the carp, has a rostrocaudal topographic organization. Thirdly, the reciproca1 isthmotectal connections in Nuvodon appear to have a rather refined topographic organizationlllJ)7. Finally, the projection from the torus semicircularis to the tectum in the electrosensory gymnotiform teleosts also has a refined topographic organization,
which
is in spatial
register
with
the
retinotopic
mapl2.27,
Some additional reports concerning the topographic tectal organization should be mentioned. Fish and Voneida64 have reported a kind of somatotopic map in the blind fish Astyanux hubbsi and in the goldfish. In the latter anima], this map was reported to be roughly in register with the visuotopic map. However, it is unknown by which afferent system these somatosensory responses are provided to the tectum. Grover and Sharmas4 reported that in the goldfish the pretectal nuclei project preferentially to the rostral tectum, whereas afferents from the torus semicircularis, the nucleus dorsolateralis tegmenti and the reticular formation preferentially terminate in more caudal tectal regions.
253
Ret
TL
Tel
cTect
AP NP NI NRMT
only DLT
TS NRS
been
demonstrated
experimentally
in
the
carptas, the typical characteristics of the margina1 axons in different teleostslo3,1~.131~149 as well as the close correlation
between
the degree of development
of the torus and the margina1 layer in a large number of teleost@
indicate
that the torus projects
same tectal layer in all teleosts, including The reports
about
ents are somewhat
%C%? Resuks of retrograde
confusing.
tectal affer-
The degeneration
ex-
periments of Vanegas and Ebbessonzss on Eugerres and Holocentrus as well as the telencephalic HRP-in-
ISPV
%%%Z?Results of anterograde
the telencephalic
to the
goldfish.
tracing experiments tracing experiments
Fig. 4. Summarizing scheme of the lamination pattern of tectal afferents iti the goldfish. For details and references, see section 2.1.3. The interrupted hatching in the fifth column is meant to indicate that the experiments performed do not allow for conclusions about terminals in this zone.
2.1.3. Laminar organization of tectal afferents The present knowledge concerning the laminar distribution of afferent terminals in the goldfish tecturn is summarized in Fig. 4. The most detailed results have been obtained by means of anterograde tracing techniques, which clearly visualize afferent termination patterns. Additional information, although less precise, has been inferred from retrograde labeling experiments in which HRP was injected in the tectum at different depths. The laminar distribution of retino-tectal terminals in the goldfish has been analyzed with a variety of techniques, including degeneratior9, autoradiographyi30J6s, cobaltchloride219, cobaltous lysinez40 and HRPt67. These studies show a massive projection to the contralateral SFGS (layer 5) and the SO (layer 6), in particular its superficial part, with some sparse termination in the SGC (layer 3/4) and the SAC (layer 2). The projection to layer 314 was not observed with degeneration techniques23i, most probably because of the relative insensitivity of this technique. A comparable lamination pattern of retino-tectal fibers has been reported for a large number of other tele~,tS7.49.Sl.57.59.89.l30.l36.l57.1R4.l86.l88.l97.l98,258.268~
Afferents from the torus longitudinalis terminate in one single tectal layer, viz. the superficial margina1 layer (layer 7). This layer is only present in actinopterygians, as is the torus longitudinalis. Although the toral origin of the unmyelinated margina1 fibers has
jections
of Ito et al.109 in severa1 other teleosts
(in-
cluding the carp and the crucian carp), clearly show termination of telencephalic efferents in the ipsilateral stratum griseum centrale, especially in layer 3/4. Some sparse additional termination may be found in layers 6 and 2259or layer 415109.A similar telencephalic tectal termination pattern can be inferred for carpia7.137, goldfishsd and catfishii on the basis of tectal HRP injections. In al1 these teleosts tectai HRP injections result in labeling of neurons in the ipsilatera1 telencephalic area dorsalis centralis, and such labeling is only obtained when the HRP injection includes the SGC. Termination of telencephalic efferents in the SGC, and especially in layer 314, was recently confirmed for goldfish by Oka and Uedai” by means of a degeneration study. However, these authors also describe a contralateral projection. The degeneration experiments of Marotte and Mark144 and Airhart2, using carp and goldfish, respectively, are even more confusing, since these authors not only describe bilatera1 projections, but also termination throughout layers 3, 4 and 5. Whereas the latter results might be due to aspecific degenerative reactions, which may occur under certain conditions (see e.g. ref. 143), the incompatibility of the results of Oka and Uedai77 and those of Grover artd Sharmas4 is more difficult to explain. Leaving the problem of ipsi-versus bilatera1 projections undecided, it may be concluded that telencephalic fibers seem to terminate for the major part in the SGC, with a special concentration in layer 3/411.84.107.109.137.177.2S9~ The layers of termination of intertectal fibers have only been determined clearly in the teleosts Eugerres and Holocentrus with the aid of light- and electronmicroscopical degeneration studies54.io6. In these species the intertectal fibers terminate predominantly in layer 3, and for a small portion in layer 2. In 3 othcr
254 reports,
dealing
with Astyanax hubbsW,
goldfishs-i
than the number
of ganglion
cells, indicating
that
and carpis7, the termination leve1 of intertectal fibers was not indicated explicitly, but judging from the
some ganglion cells might give rise to more than one fiber in the optic nervei67. A number of about 200,000
drawings
optic nerve fibers has also been estimated
published
in these papers,
in these teleost
for Eu-
intertectal fibers also terminate in deep tectal layers (layers 2 and 3). The massive degeneration found in
gerre9.
layer 7 after section of the intertectal
ing fine-structural criteria - has roughly been estimated at 30 millionis~. However, this is most proba-
Marotte
and Mark144 is probably
the torus longitudinalis
commissure
due to damage
by of
(cf. Ito and Kishidai(rs).
The number of synaptic contacts made by retina1 fibers in the goldfish tectum - identified us-
bly a serious underestimation, since HRP labeling of retina1 terminals shows that their number is substan-
The lamination pattern of the remaining tectal afferents in goldfish can be inferred from the study of Grover and Sharma@, who placed HRP injections at
tially larger than expected on the basis of the generally used fine structural criteriar66. Using HRP label-
different
ing, Murray
levels in the tectum. They conclude
that ef-
ferents from the area pretectalis, nucleus pretectalis, nucleus of the rostral mesencephalic tegmentum and nucleus isthmi predominantly in the SFGS (layer 5), and that the nucleus dorsolateralis thalami projects to the mid-tectal leve1 (SGC). Terminals from the torus semicircularis and nucleus reticularis superior could only be labeled with deep tectal HRP-injections, including the SAC (layer 2). It has already been mentioned that these results are less conclusive with respect to the laminar organization than those based on degeneration or autoradiographic experiments. Apart from the difficulty of the rather large size of HRP injections compared with the thickness of the tectal layers, variations in axon diameter, in the extension and density of the terminations of individua] axons and in the rostrocaudal position of the different projections also affect these resultsx4. Carr et al.27 found that in gymnotiform teleosts the torus semicircularis also projects predominantly to the SAC (layer 2), with some additional projections to the SPV (layer 1) and the SGC (layer 3 and 4). 2.1.4. Quantitative properties of tectal afferents From a quantitative point of view the retina1 fibers constitute by far the most important tectal afferent system in goldfish. The number of retina1 ganglion cells is approximately 130,000 in goldfish of about 10 cm lengthi67 and a similar number has been preof similar sizer23 carps sented for crucian (120,00&180,000; mean value 140,000). Larger crucian carps may reach an average number of 200,000 ganglion cellW. At least 90% of the ganglion cells project to the tectum 167.The number of optic nerve fibers in goldfish of about 10 cm length has been estimated at about 165,0004X or 2OO,OOOi6s.This is larger
et al.167 have calculated
a number
of
about 50 million retina1 terminals per tectal half, but their data do not allow an estimation of the number of resulting synaptic contacts. As far as the goldfish is concerned, afferents from the torus longitudinalis are quantitatively the second in importance. The tectum is the only known target of the torus longitudinaliWJ64, and the importance of the toro-tectal projection can be judged from the number of cells in the torus, the thickness of the marginal layer, and from the number of synapses in the margina1 layer. For goldfish of about 10 cm, the number of toral cells may be estimated at 100,000 (preliminary ce11 counts in Nissl preparations) and the number of synapses made by the margina1 axons may be estimated at about 25 million (derived from the total number of contacts of type 1 neurons, see Meekis”). Among different teleosts large differences may occur in the relative thickness of the optic (layers 5 and 6) and margina1 (layer 7) layer.+J. The margina1 layer attains its largest thickness in Holocentrus12”.226, whereas it is smallest in Trachinocephalusl2”. The optic layers have their largest relative thickness in Navodonl2’). The goldfish has a ‘standard’ tectum in this respecti?(J. Quantitative data concerning the number of axons and synaptic contacts of other tectal afferent systems are not available at present. Only the following can be noted. The telencephalic projection might well be the third in importance, considering the rather large dimensions of the area centralis dorsalis, the large number of cells labeled after tectal HRP injections*(‘7 and the quite dense degeneration in the SGC after telencephalic lesionszsy. In Navodon the nucleus isthmi has a rather heavy projection to the tectum as welW. In severa1 teleosts the intertectal projection
255 is reported
characteristic
to be very sparse54.83.*4,106,137.234 and in
location
and
extension
of dendritic
goldfish and carp also only a small percentage of cells in the torus semicircularis seems to project to the tec-
trees and with characteristic axonal properties. Four ce11types have myelinated axons which leave the tec-
tums4.137. In contrast, the torus semicircularis of gymnotids has a rather heavy projection to the tectum27.
turn (type VI, X, X11 and X111), whereas 8 ce11 types
The heaviness
and XIV). The axonal properties
teleosts
of other projections
is uncertain.
the nucleus pretectalis,
Judging
to the tectum
are interneurons
of
from the small size of
area pretectalis,
nucleus
XV are obscure. as
dor-
follows:
(type 1, 111, IV, V, VII, VIII, The number type
1,
1X
of type 11, X1 and
of neurons
is estimated
5000-20,000;
type
111,
solateralis and nucleus of the rostral mesencephalic tegmentum in goldfishisi these centers probably give
2500-10,000;
rise to only few tectal afferents.
that the cytoarchitecture of the goldfish tectum consists of a fairly strictly organized frame, formed by
2.2. Intrinsic tectal strutture
the rather
2.2.1. Tectal neurons The neurons of the goldfish tectum have been studied with Golgi techniques by Leghissaiss, Meek and Schellartisz and Romeskie and Sharmazm. The results of Meek and Schellart are summarized in Fig. 5. These authors distinguish 15 ce11 types, each with a
rons, intermingled with the numerous and variable type XIV neurons. A detailed comparison of these results and those of Leghissa has been presented by Meek and Schellartlsz, and similarities and differences with respect to the results of Romeskie and Sharmazm have been discussed by Meekisi. Tectal cytoarchitecture has also been analyzed
grmp
1 _1
I
l
Ila
Ilb
X\,,\,
,
-
type
I
group type Irr
,--
2 Ill
XI
l-2
million.
infrequently
and Schellartlsz
occurring
conclude
type I-X111 neu-
VI
5_--_
-II
XIII ,
Meek
II_
IVa/b V
4
,
XIV,
type IV-X111, each 500-2000 and type
XIII 2
I
XIV[‘largél-,
~
_
XIV~small’l _
I ,_._~
XV. I
71
Fig. 5. Schematic representation of the cell types in the goldfish tectum (after Meek and Schellartisz). The soma sizes and dendritic extensions of type I-X111, have been drawn to scale using average values, whereas for type XIV and XV some typical neurons have been drawn. Unmyelinated axons have been drawn thinly, whereas myelinated axons leaving the tectum end with an arrow. The cell types and groups have primarily been distinguished on the basis of dendritic properties. Group 1 includes neurons with dendrites in layer 7 (type 1 and 11); group 2 includes monostratified neurons (with dendrites at a single level; type 111, IV and V); group 3 includes bistratified neurons (with dendrites at two separate levels; type VI, VII, VIII, 1X and X); group 4 includes mulrisrrarifiedneurons (type X1. X11 and X111); and group 5 includes non-stratified neurons (type XIV and XV). The calibration bar is 100 Pm.
256 with the Golgi-technique
Barbus fzu-
in the teleosts
viatilis’g2, Salmo irideus13.186, Eugerres plumieri263, Bagrus sp. and Ictalurus punctatu9,
Hemichromis
Poecilia32 and Holocentrusl06. Whereas some studies predominantly dea1 with glia cells12*.246or glycogenmetabolism248, most studies dea1 with cytological
bimaculatu_+~, Holocentrus rufus and H. ascensio-
synaptic
nk226. Taking
regard to the synaptic organization be noted.
al1 Golgi-studies
together,
it may be
concluded that, except for quantitative differences, the tetta of the teleosts studied are basically similar. This conclusion is supported by the comparative study of Kishidalzo on a variety of teleosts. A detailed comparison of various Golgi-studies sented by Meek and Schellartis2. Whereas
severa1 Golgi-studies
tectum tend to stress the variability
has been pre-
on the teleostean of the individua1
neurons133,200.*26.263,others emphasize a strict classification of ce11types on the basis of relevant similaritie@Js2. The schematic presentation of ce11 types in Fig. 5 is the result of the latter approach, presenting a classification of ce11 types with averaged characteristics determined in a quantitative waylS2. Such a presentation, which like al1 classifications necessarily includes some simplications, neglects some variabilities and favours some characteristics at the expense of others, might seem to be simplistic in view of the capriciousness of the Golgi-methods and the large variability of individua1 neurons. It should, however, be realized that (1) when a large number of neurons is investigated using a variety of Golgi modification@ a rather complete description of neuronal types may be obtained; (2) The variability of tectal neurons is often more apparent than rea1 because of incomplete impregnation, oblique planes of sectioning, and difficulties in defining tectal layers in Golgimaterial; (3) The method employed for classification by Meek and Schellartls2 clearly shows monomodal distributions for the location of specific dendritic trees; and (4) EM investigation has revealed that at least 6 of the ce11types distinguished by means of this classification have characteristic synaptic properties as welll50. The major advantage of a strict classification on the basis of well-defined characteristics is that it allows for integration of neuronal morphology with synaptology*5(J, circuitry (see section 3), as well as physiology (see section 5). 2.2.2. Synaptic organization of the tectum Severa1 aspects of the ultrastructure of the tectum of normal, adult teleosts have been studied, in particular in g~~~f~~~l49.l50.246.248.267, carp31.103, Eugerresl31,
properties
of the neuronal
elements.
and With
the following can
In layer 7, the margina1 layer, the thin, unmyelinated fibers from the torus longitudinalis make many synaptic contacts with the spiny dendrites of type 1 or pyramidal neurons. These contacts are of the asymmetric type and the presynaptic elements contain small round vesicles31~1~3~*06~‘~~,~~4.~4Y. Comparison of the ultrastructure
of the margina1 layer in carp (Cy-
prinus carpio) and trout (Salmo gairdneri) revealed that in the carp more convergent synapses occur (one terminal contacting two or more spines of the same neuron), whereas in trout the tota1 number of synapses is substantially larger-ll. In Holocentrus, which has the largest margina1 layer of al1 teleosts investigated SO far!*” a second type of presynaptic element, containing flattened vesicles has been described in layer 7106. Unti1 now, these have not been found in other ~~~~~~~~31.103,131.14Y, Layer 5, the SFGS, is the main region of retina1 termination (see section 2.1.3). As has been shown with degeneration experiments3~tl)h~l”* retina1 terminals contain large round vesicles and pale mitochondria with delated cristae, and make asymmetrical synaptic contacts. These criteria can also be used in norma1 EM rnaterial”,lO6,1”‘.‘““. Their frequency of occurrence in the SFGS has been estimated at 16% in Holocentrus and 18% in goldfish, while Meekls” has calculated that they form 1&20% of the synaptic contacts in the SFGS of goldfish. However, Murray and Edwardsl66, using HRP labeling of retina1 terminals, recently have shown that at least 37% of the terminal population in the SFGS is of retina1 origin. This means that a large portion of sections through retina1 terminals is not recognizable by pure morphological features, and that the previously reported frequencies are serious underestimations’66. The most important postsynaptic elements for retina1 terminals are small dendritic profiles- 1.1~13,11~6,131.150,166~ In addi_ tion, other structures are postsynaptic to retina1 terminals, including large dendritic shaftsl3~~t4Y~l50,sornatal49.tsO and profiles containing synaptic vesic~es103.106,14Y,
A variety
of non-retina1
presynaptic
elements
in
257 the SFGS has been describedlo3,106,131.149.Unti1 now,
SAC. In contrast,
the origin of these elements partly represent afferent
ic shafts of type XIV neurons,
is unknown. terminals
They might of various
sourcesi49 (see Fig. 4) and partly axon terminals
of
interneurons. In particular the population of Ss terminals (small terminals with small round vesicles) reported in Nolocenrrust06
might well represent
axonal
the synaptic density on the dendritwhich pass through the
SAC and SGC to reach the SFGS, is relatively
low.
The SAC or layer 2 is dominated by the occurrence of myelinated fibers, which partly represent tectal efferentsta3.tst~t49. However, fibers
represent
tectal
another
afferents,
portion
of these
terminating
pre-
terminals of type XIV or SPV neuronst4s. Postsynaptic structures in the SFGS show a large variability as
dominantly on the dendrites and ce11bodies of the efferent type X111 neurons and the basa1 dendrites of
well, and integration of hght- and electron-microscopic results in this layer is rather difficultia3.t~.tst.
the efferent
Meekt49.150 could identify
Fig. 4). The SPV or layer 1 is characterized
a number
of postsynaptic
structures on the basis of a combined study, each with characteristic synaptic
Golgi-EM properties.
The frequently occurring type I neurons, e.g., receive only few synaptic contacts on their ce11body and dendritic shaft, whereas the relatively rare type VI neurons receive much more synaptic contacts. A low density of synapses on type 1 or pyramidal neurons has also been reported for Eugerresist. Villani et al.267 describe that some neurons in the SFGS of goldfish exhibit degenerative changes after kainicacid treatment, whereas others do not. Judging from their ultrastructural features, the kainic-acid sensitive neurons belong to type 1, whereas the insensitive neurons belong to type VI (cf. refs. 149 and 267). In the SGC (layers 4 and 3) a variety of pre- and postsynaptic elements constitute a complex neuropil3*.~03.~0~.131.144.149. Only a smali portion of ah these elements has been identified. Ito et al.iw showed by means of degeneration experiments that in Hoiocentrus some of the S4 terminals (medium-sized terminals with various-sized, round vesicles) belong to telencephalic afferents, whereas some of the S5 terminals (small terminals with small round vesicles) arise from intertectal commissural fibers. However, comparison of the Golgi-EM results of MeektQ and the results of Ito et al.106 suggests that most S, terminals, which form 65% of al1 terminals in the SGC of Holocenfrus, represent type XIV axon terminals, whereas the S4 terminals, in particular those in Iayer 314, may represent type 1 axon terminalst49. Severa1 types of postsynaptic elements in the SGC have been identified and described by Meekt49.tsa in the goldfish with Golgi-EM. The ce11bodies and dendrites of the efferent type X11 or fusiform neurons have a rather large density of synaptic contacts, just as the dendrites of the efferent type X111 or multipolar neurons from the
type X11 neuronsi49.
the SAC may originate
These afferents
from various
sources
in (see
by the closely
packed celi bodies of the pe~ventricular (type XIV and XV) neurons, which are traversed by various fiber bundles3*.10~.131,144.*49.*46.*67. Synaptic contacts only occur on the somata of the most superficially located ce11 bodies, whereas deeper positioned neuronal somata are devoid of such contacts131.149.l~o.*~. Some authors have described junction-like specializations between somata and/or proximal dendrites of these neuronstas.149. Whereas the majority of these neurons is resistant to kainic-acid treatment, some of them show kainic-acid induced degenerative reaction+. Present knowledge concerning the synaptic organization of the teleostean tectum may be summarized as follows: first, in most teleosts (goldfish, carp, Eugerres) tectal synaptology appears to be straight-forward, since almost exclusively axo-dendritic and axosomatic synapses have been found31.lo.7.131.149.*6:.The only known exception is constituted by the few contacts between retina1 terminals and vesicle-containing profilestOs~t49. However, in the highly developed tectum of Holucentr~l*O.22b synapto~ogy appears to be somewhat more complicated, since in this tectum presynaptic dendrites (F2 type) and glomerular arrangements (S3 type) have been encountered as wellt06. Secondly, each tectal layer contains its own, characteristic set of presynaptic terminals, as has qualitatively been described by severa1 authors3*.t03,tst,t44 and has been quantified by Ito et al.106 for Holocentrus. The most striking features of this presynaptic lamination pattern are (a) the exclusive occurrence of toral afferent terminals in the marginal Iayer (layer 7)31.1~3~~~.~3~.~4Y; (b) the occurrence of retina1 terminals in the SFGS (layer S), which, however, constitute only a minor portion of the pre-
258 layer (about synaptic elements in this 2WO%)3.1(~6.13*.132.‘66;(c) The abundant occurrence (65%) of S, terminals most probably
in the SGC (layer 4 and 3)1’)6,
representing
axon terminals
of the
periventricular type XIV neuronsi4Y; and (d) The occurrence of severa1 types of myelinated afferent ter-
The most important differente between the results of Grover and Sharmas-i and those of other authors mentioned”4.‘37,224,234 concerns the tetto-isthmic projection,
which has not been described
for the gold-
fishss but was demonstrated in al1 other teleosts investigateds4.1’7.224.2’4. Moreover. Ito et al.ii’).ili and et al.207 demonstrated in Navodon modprojection is highly or-
minals in the SAC and deep SGC (layers 2 and 3)i@.
Sakamoto
Thirdly, the postsynaptic structures in the tectum (the dendrites and ce11 bodies of the tectal neurons)
estus that the tetto-isthmic
appear to have a characteristic density and number of synaptic contactsi”“. The average density of contacts
trophysiological evidente for the existence of a tectoishtmic projection in Holocentrus and Eugerres. In fact, in al1 classes of vertebrates investigated, the nu-
per ce11 type ranges from about IOOprn? neuronal ber of contacts neuronlsO.
15-80 contacts
per
surface, whereas the average numranges from about 200 to 5000 per
2.3. Tectal efyerents 2.3.1.
Tectal targets
The efferents of the goldfish tectum have been investigated by Grover and Sharmass. Their results, combined with those of Schmidt”” concerning tectoretina1 efferents in the goldfish, are summarized in Fig. 3B. A projection to the nucleus isthmi, not identified as a tectal target in the goldfishs-i is included in Fig. 3B for reasons to be dicussed below. The overall pattern of tectal efferents has also been investigated in the teleosts Ictaluru.94, Eugerres and Holocentru+.
the blind fish Astyanax hubbsP, and the carp Cyprinus carpiol37. These studies agree with the results of Grover and Sharmas” in describing ascending, bilatera1 projections to the nucleus rotundus and other pretectal ce11groups, a media1 projection to the contralateral tectal half and descending projections to the ipsilateral torus semicircularis, other ipsilateral dorsolateral tegmental areas, the ipsilateral lateral reticular formation and the contralateral medial reticular formation (Fig. 3B). The descending efferents constitute the largest efferent tectal tract (tractus tetto-bulbaris). Ebbesson and Vanegas and Luiteni37 describe an additional media1 projection to the torus longitudinalis. However, the toral afferents labeled by these authors represent at least in part the cerebello-toral afferents, which traverse the tectum before reaching the torus 1ongitudinalisi~‘s. A projection from the tectum to the torus semicircularis has also been described for electric gymnotiform tele()sts?7.2’4
dered,
and Williams
and Vanegas
cleus isthmi or its homologue,
provided
the nucleus
elec-
parabige-
minaliss7Jn receives the bulk of its input from the tectum mesencephali (teleosts,ii2.207: amphibians 85.X7.203.274. , reptiles,h”: birds,YY,i”“; and mamrnalsY.s’~,‘+t,l~“) and is considered as a ‘satellite system’ of the tectum or colliculus superiorsz. SO, a nucleus isthmi without tectal input would be quite unlikely. Most probably. the deviating results of Grover and Sharmasj with respect to the tetto-isthmic projection will have a technical explanation and not reflect a species differente. Consequently, also in the goldfish the nucleus isthmi should be considered as a tectal target (Fig. 3B), just as in other teleosts. The existence of a tetto-retina1 projection is a point of controversy in the literature. Anatomica]163,245,253.278 electrophysiological and studiesJ(rxJiY~~shhave clearly demonstrated the existence of retinopetal, centrifuga1 fibers in teleosts. However, the origin of these fibers is not certain. Electrophysiological results strongly suggest a tectal origin of retinopetal fibers. Using electrical stimulation of the optic nerve, Vanegas et al.256 found in Eugerres a fast-conducting population of fibers in the SO (layer 6) that showed severa1 characteristics of antidromic activation. Moreover, these fibers remained intact after eye-enucleation, which excludes a retina1 origin and suggests a tectal origin. Similar electrophysiological results were obtained by Schmidt?iY in the goldfish. Electronmicroscopical studies corroborated the persistente of large caliber (= fast conducting) fibers in the SO after eye-enucleationl32. Sandeman and RosenthaP recorded the activity of retinopetal fibers in the trigger fish Hemibalistes chrysopterus, which could be activated by visual, vestibular, vibratory and tattile stimuli. Their responses were weakened by ablation of the ipsilateral tectum and abol-
259 However,
these represent
other ce11types than those
ished by ablation of the contralateral tectum, strongly suggesting a tectal origin. Anatomica1 studies, using HRP injections in the eye or optic nerve, have yielded less consistent re-
in the SFGS and SGC, while those in the SFGS are not bipolar. Furthermore, the number of neurons la-
sults. Schmidt*is has reported
beled by Meyer and Ebbessonis’
for the goldfish the bi-
lateral labeling of a large number vertically oriented bipolar tectal
(about 1500) of neurons in the
SFGS. However, this labeling could not be obtained in norma1 specimen, but only when the eye had been enucleated 2-6 weeks before, and Springer and Gaff-
labeled by SchmidW,
was considerably
because they are located both
and Meyer et al.158
smaller than the number
of neurons
labeled by Schmidt*i9. Apart from the tectal neurons, Meyer and Ebbessonis’, Meyer et al.158 and Ebbesson and Meyers* labeled severa1 tel- and di-encephal-
in
ic nuclei as well, which were not labeled by Schmidt*ig. Other studies in severa1 teleosts did not at al1 result in
demonstrating tetto-retina1 neurons in goldfish. The identity of the neurons shown by Schmidt*is is anoth-
labeling of tectal neurons, but only of various nontectal sources of retina1 afferents, including a telen-
er problem. Some of them probably represent type 1 neurons (see Fig. 5), because of the characteristic bi-
cephalic nucleusi62J63, a preoptic nucleu9, a nucleus in the optic tract76 and a pretectal nucleus’62. Peyrichoux et al.184, using cyprinid fishes, could not at al1 produce reproducible labeling of retinopetal cells. SO, with respect to tetto-retina1 projections severa1 uncertainties exist, which may partly reflect speciesdifferencess*, but partly also may be due to technical reasonsisi. Nevertheless, the results of Schmidt*iY have been tentatively incorporated in Fig. 3B, since at present the existence of recto-retina] fibers cannot be excluded.
ney*m and Uchiyama
et al.253 did not succeed
furcation of the apical dendritic shaft at the boundary of layer 6 and 7 or because of the presente of a basa1 dendritic shaft in layer 4. Type 1 neurons, however, are clearly interneurons, not projecting outside the tectumi@J5*. Other neurons labeled by SchmidW might represent type VI neurons, which indeed have efferent axons. However, these axons are not of a large caliber and do not course through the SOi@,is*, as could be expected for tetto-retina1 fibres from the electrophysiological results (see above). Meyer and Ebbessoni57, Meyer et al.158, and Ebbesson and MeyerQ also labeled tectal neurons after HRP injection in the eyes of Synodontis nigriventris, Tetraodon fiuviatilis, and Julidochromis regani, respectively.
VI
X
\
Fig. 6. Summary of the present erences, see section 2.3.2.
knowledge
-4
tractus
concerning
XIV
XIII
XII
7
retIna
2.3.2. Efferent tectal ce11types Although most Golgi-studies remained unable to determine the character and course of tectal axons, Meek and SchellartiQ could prove on the basis of a
the efferent
tetto-bulbarls
tectal neurons
xv
/ nucleus Isthmi
and their targets
pretectum +contralat tectum
contralateral tectum
in the goldfish.
For details and ref-
260 modified
Golgi-Cox
tal neurons
techniqueids
have myelinated
that 4 types of tec-
axons leaving
the tec-
turn (type VI, X, X11 and X111, see Figs. 5 and 6). Electron
microscopica1
observations
confirmed
this
finding for type VI, X11 and X111 neuronst49. The investigations of Grover and Sharmas4 corroborated the efferent character
of type X11 and type X111 neu-
rons, since both types of neurons were labeled after HRP injections in the torus semicircularis or in the tractus
tetto-bulbaris.
According
to the results
of
Schmidtzis, extensively discussed in the preceding paragraph (2.3.1), the axons of type VI neurons might possibly terminate
in the retina. HRP injection
in tectal targets have not yet labeled neurons that could belong to type X. Both light- and electronmicroscopic investigations revealed that in goldfish type XIV neurons have unmyelinated axons with abundant collateral terminations within the tectumt49.*52. Similar findings have been reported for Hemichromis”” and Holocentrus**6. However, recent investigations using HRP injection in tectal targets revealed at least 3 sites of termination of type XIV axons outside the tectum (viz. the nucleus isthmi, the pretectum and the contralateral tectal half), which means that severa1 typr XIV axons also have collaterals that leave the tecturn. Ito et al.112 labeled a peculiar subtype of type XIV neurons after HRP injection in the nucleus isthmi of Navodon modestus. This subtype, with a dendritic as well as an axonal arborization in iayer 6, has also been demonstrated in the goldfish (Meek and Schellartis?, p. 101; see also their Fig. 16, and Fig. 5 of the present paper). Conceivably, also in the goldfish, the basa1 axon collateral of this subtype projects to the nucleus isthmi (Fig. 6). Grover and Sharma84 demonstrated in the goldfish two other targets of type XIV axons, viz. the pretecturn and the contralateral tectal half. HRP injection in the pretectum, including the area pretectalis and nucleus rotundus, but not the nucleus pretectalis and nucleus geniculatus laterahs, labeled monopolar neurons in the tectal layers 1 or 2, with an apical process reaching layer 5, thus allowing for identification as type XIV neurons. Retrograde labeling in the contralateral tectum was difficult to obtain. but in one out of 15 attempts, Grover and Sharmasj clearly labeled neurons in the SPV. Although some of the labeled cells had a peculiar multipolar shape, most of
them might represent
type XIV or type XV neurons.
A projection of type XIV neurons to the contralateral tectal half is supported by two other findings. First. O’Benarl76
recorded
closely resembhng
in the SPV electrical
the activity of intertectal
activity commis-
sural fibers as recorded by Mark and Davidsoni41. Secondly, Ito et al.106 describe degeneration of some axon terminals
of the S, type in the tectum Hofocentectal half. As is
trus after lesions in the contralateral
discussed by MeektQ, SS terminals closely resemble the axon terminals of type XIV axons as identified in the goldfish (see also section 2.2.2). It is important to note that most targets
of type
XIV neurons project back upon the tectum (nucleus isthmi, area pretectalis and contralateral tectum; cf. Fig. 3A). This implies that most efferent axons of type XIV neurons form part of extratectal feedback loops. The present knowledge concerning the projections of efferent tectal neurons is summarized in Fig. 6. Thus far. the tectal neurons projecting to the nucleus pretectalis, nucleus geniculatus lateralis and nucleus dorsolateralis thalami have not been identified. 3. 4 CONCEPTUAL
FRAMEWORK
OF TECTAL
CIR-
CUITRY
3.1. Starting points Two types of starting points underhe the conceptua1 framework of tectal circuitry to be presented. On the one hand, severa1 structural results as surveyed in the preceding section have direct implications for tectal circuitry. These include (1) the straight-forward synaptic organization of the tectum, which implies that axon-terminals can be considered as exclusively presynaptic structures. whereas dendrites, celi bodies and initial parts of axons are exclusively postsynaptic structures; (2) the characteristic lamination pattern of presynaptic structures; and (3) the characteristic location, extension and synaptic densities of postsynaptic structures. On the other hand, some assumptions have to be adopted about the interrelations of different types of presynaptic structures which coexist at the same tectal leve]. In the next paragraphs both types of starting points will be discussed in detail. For references, the reader is referred to the preceding survey of the structural tectal organization.
261 3.1 .l.
The lamination pattern of tectal neuronal el-
ements 3.1.1.1.
because of the presente pretectalis,
Tectal afferents. On the basis of the lami-
of afferents from the nucleus
area pretectalis
and nucleus
isthmi.
The
nation patterns of tectal afferents as discussed in the preceding section (Fig. 4), 4 main afferent tectal
nucleus of the rostral mesencephalic tegmentum provides signals of unknown modality to this zone. (3) The bulk of telencephalic afferents terminates
zones can be distinguished
in the SGC, particularly
(see Fig. 7, left third).
(1) Afferents from the torus longitudinalis nate in layer 7, which thus can be characterized
be considered as the telencephalic afferent zone. However, also the axons of type 1 neurons, which are
termias the
the recipients
toral afferent layer. Since the torus longitudinalis receives its signals predominantly from the valvula cerebellilss, layer 7 may also be called the cerebellar ferent layer226.
in layer 3/4, which thus could
of toral signals, terminate
in layer 3/4.
Consequently, this zone should preferably be considered as the telencephalic-toral (cerebellar) afferent
af-
zone. In addition, tegmenti
(2) Layer 5 and its border zones (layer 5/6 and 4/5;
axons of the nucleus dorsolateralis
and a few retina1 fibers terminate
in this
zone. For the sake of simplicity, these will be left out of discussion. (4) Layers 2 and 3 can be considered as the ‘deep’ tectal afferent zone. Afferents from the contralateral tectal half, torus semicircularis and reticular formation specifically terminate in this region. In addition, some retina1 fibers terminate in layer 2, and it cannot be excluded that the area pretectalis, nucleus pretectalis, nucleus isthmi and nucleus of the rostral mesencephalic tegmentum have some additional projections to this region as well. The recent finding of LHRH containing afferents which terminate specifically in layers 2 and 3 in Xiphophorusl64 as well as the occurrence of severa1 types of myelinated afferents in
see Fig. 2) contains the bulk of retina1 afferents, and in addition afferents from the nucleus pretectalis, the area pretectalis, the nucleus isthmi and the nucleus of the rostral mesencephalic tegmentum. The nucleus pretectalis and area pretectalis can both be considered as ‘visual’ nuclei, since they have an important bilatera1 input from the retina (for goldfish, see refs. 231, 240, 241). The nucleus isthmi may also be considered as a ‘visual’ nucleus, since it receives its input from the ‘visual’ nucleus pretectalisll* and from a subtype of type XIV cellslt*, which also must be considered as ‘visual’ (see below). SO, layer 5 and its boundaries may be designated as the ‘visual’ afferent zone, not only because of their retina1 input, but also
cell types
TL
AP NP NI Ret NRMT
cTect Tel TS DLT NRS
Ill
IV VII
v
VIII IX
XIV
VI
1 2
SPV
1
0 -,
postsynaptic strutture presynaptlc strutture efferent axon
Fig. 7. Summarizing scheme of the laminar organization of the neuronal elements in the goldfish tectum. With respect to the tectal afferents, the main results as summarized in Fig. 4 have been indicated. With respect to the tectal ce11 types, the average position of the dendritic trees and axon terminals has been indicated (without indication of their extension) as summarized in Fig. 5. For details the reader is referred to section 3.1.1.
262 these layersi@ indicate
that the significante
of the
sively in the visual afferent
‘deep’ tectal afferent zone is not yet fully understood. The various kinds of non-visual responses that can be recorded
from the tectum are probably
‘deep’ tectal afferents. 3.1.1.2. Teda1 interneurons. pattern
of tectal neurons
provided
VI1 neurons). (c) Interneurons with their dendrites in layers 3 and 4 (type V neurons). (d) Interneurons with their dendrites both in the ‘visual’ and in the tel-
via
encephalic-toral The
stratification
in summarized
layer (type 111, IV and
(cerebellar)
afferent
layer 3/4 (type
VI11 and 1X). (e) The less strictly organized and very numerous type XIV neurons, which have their main dendritic tree in the visual afferent layer 5, and addi-
in Fig. 7
(middle and right thirds) which is derived from Fig. 5 by means of the following modifications. TO stress
tional dendrites
in other tectal layers.
the lamination pattern, only the average location of dendrites and axons is presented, without indicating
With respect to the axon terminations of tectal interneurons, Fig. 7 shows a rather refined stratifica-
their extension.
tion pattern in comparison with the pattern of tectal afferents. The axons of type 1 neurons specifically
Information
ce11bodies is omitted,
on the localization
of
since they do not seem to have
terminate in layer 3/4. The axons of the interneurons of group b, c and d terminate in layer 5, 415 or 4 in such a way that each of these layers contains the axon terminals of one monostratified or horizontal neuron and one bistratified neuron (layer 5: type 111 and
any specific significante in tectal circuitry deviating from that of dendrites. On the basis of the position of the dendrites of tectal interneurons in the 4 afferent zones described above, 5 groups of neurons can be distinguished (Fig. 7). (a) Interneurons with their dendrites mainly in the toral (cerebellar) rons). (b) Interneurons PRESYNAPTIC
type VII; layer 4/5: type IV and type VIII; layer 4: type V and type 1X). A portion of the axons of type V neurons terminates in layer 3. Apart from this, the
afferent layers (type 1 neuwith their dendrites exclu-
ZONES
POSTSYNAPTIC CHARACTERISTICS of some cell types type
7
:Tor
6
: Vis
+
516 j
: Vis + Ill
+ VII + XIV
4/5
: Vis+
+ VIII + XIV 9$_
I
type Ill
type
XIV
type VI
type XII
typexlll,
‘>g’
4 314
IV
: : Tel
213 ; : Deep
Fig. 8. Some organizational characteristics of pre- and postsynaptic structures in the goldfish tectum. A: laminar organization of the presynaptic tectal structures (afferents and axons of interneurons), which allows the distinction of eight presynaptic zones (see section 3.1.2). The presynaptic zones distinguished continue as gray bands in part B of this figure. B: characteristic position, extension, synaptic density and number of synaptic contacts of the postsynaptic structures of 6 important tectal cell types in the presynaptic zones distinguished (modified after Meektso). Both the dendritic lengths and the horizontal dendritic extensions have been drawn to scale, using average valuestsa. The diameters of the structures drawn indicate their mean circumference. Each dot represents 10 synaptic contacts.
263 ‘deep’ afferent layers 2 and 3 are very poor in axon terminations of interneurons as compared to the more superficial layers 4 and 5. The axons of type XIV neurons, which show many individua1 variations, terminate predominantly in layers 5, 4 and 3 with a preponderante in layer 4, the only tectal zone in which most probably no afferent terminals occur. In addition, some axons or collaterals of type XIV neurons project outside the tectum. 3.1.1.3. Efferent tectal neurons. Four types of neu-
shafts, ce11bodies and initial parts of axons are exclu-
rons project outside the tectum with myelinated axons and without recurrent collateralization in the tec-
consideration,
turn. Comparison of these efferent neurons (group f in Fig. 7) with the tectal interneurons reveals that type VI neurons show some correspondence with group b in having their dendrites in or near the visual afferent layer, and that type X neurons show a close correspondence to group d with dendrites in layer 415
posed to occur to some extent in layer 3.
as well as in layer 3/4. Type X11 and X111 constitute a separate group of multistratified efferent neurons. Three tectal ce11 types have obscure axonal properties (group g in Fig. 7). These will be left out of consideration in the next paragraphs.
sively postsynaptic or receptive structures. Combination of the 4 main afferent zones with the laminar distribution of the axons of tectal interneurons allows a distinction of 8 presynaptic zones or laminae, each of which contains a characteristic population of presynaptic structures; these zones are listed in Table 11 (cf. Figs. 7 and 8). It should be noted that the few axons of type XIV neurons
that might occur in layer 3/2+2 are left out of and that telencephalic
not strictly confined
afferents
are
to layer 314, but are also sup-
3.1.3. Postsynaptic determination of neuronal input The postsynaptic structures of the tectal ce11 types (dendrites, dendritic shafts, ce11 bodies and initial parts of axons) each have a characteristic average location in the different tectal layers (Figs. 5 and 7), and consequently also in the different presynaptic tectal zones distinguished. In addition, the dendritic trees have a characteristic
average extension
(Fig. 5)
and at least 6 tectal ce11types have characteristic aptic density
patterns
along their receptive
syn-
surface
3.1.2. Presynaptic tectal zones .4 conceptual framework of tectal circuitry implies a tentative description of the connectivity patterns
(Fig. 8). This characteristic location, extension and synaptic density together result in characteristic average numbers of synaptic contacts of the different
between the different types of pre- and postsynaptic structures. In the goldfish tectum this is greatly facilitated by the straight forward synaptic organization, i.e. the almost exclusive occurrence of axo-dendritic and axo-somatic synapses (section 2.2.2). This means that more peculiar contacts as e.g. triads, glo-
ce11 types in the different presynaptic tectal zones (Fig. 8), which may vary from zero (when no receptive surface is present in a presynaptic zone) or almost zero (e.g. the ce11 bodies of type 111 and XIV and the apical dendritic shaft of type 1) to thousand or more (e.g. type 1 in layer 7; type X11 in layer 4 and layer 2/3; type X111 in layer 2). It will be clear that the connectivity patterns of the tectal ce11 types are to a great extent determined by their characteristic average postsynaptic properties in the different presynap-
merular arrangements, dendro-dendritic and axo-axonal contacts can be left out of consideration, and that axon terminals can be considered as exclusively presynaptic structures, whereas dendrites, dendritic TABLE
11
Layer 7, with toral afferents
(tor)
Layer 6, with visual afferents
and axons of some type XIV neurons
Layer 516 and 5, with visual afferents Layer 4/5, with visual afferents Layer 4, without
afferents,
Layer 314, with telencephalic
and axons of type 111, VI1 and XIV
and axons of type IV, VI11 and XIV
but with axons of type V,, 1X and XIV afferents
Layer 3, with ‘deep’ and telencephalic Layer 312 + 2, with deep tectal afferents
(vis + XIV) (vis + 111 + VI1 + XIV) (vis + IV + VI11 + XIV) (V, + 1x + XIV)
and axons of type 1 and XIV
(tel + 1 + XIV)
afferents
(deep + tel+
and axons of type V,, and XIV
(dccp).
V, + XIV)
264 tic tectal zones
(Fig. 8). For a precise
evaluation,
however, the contribution of different types of presynaptic structures that occur in each presynaptic tec-
The absence of cellular specificity in the goldfish tectum is, apart from the general considerations presented above, supported by the following considera-
tal zone should be considered
tions. First, optic nerve terminals
as well. As will be out-
appear
to termi-
lined in the next section, these contributions may be approximated by presuming the presente of laminar
nate on al1 types of postsynaptic structures investigated in layer 5, which clearly indicates the absence
specificity.
of cellular specificity for this important
3.1.4.
afferent. Retina1 fibers even seem to occupy equa1 percentages of the postsynaptic sites present on the
The hypothesis of laminar specificity 3.1.4.1. General considerations. In a laminated brain strutture, the organization of synaptic connections may, in principle, reveal complete unspecifici-
ty. laminar specificity or cellular specificityr3’.
Lami-
nar specificity, as defined by Maler et a1.139, implies that presynaptic structures are specific with respect to their layer(s) of termination. but not with respect to the different types of postsynaptic structures present in that layer(s): they are presumed to terminate without preference on al1 types of postsynaptic structures within their layer of termination. In contrast, cellular specificity means that presynaptic structures only terminate on specific postsynaptic structures within a layer. Although a number of cellular specific connections have been described (e.g. the contacts between climbing fibers and Purkinje cells in the cerebellum (e.g. ref. 179) or the contacts between the axons of chandelier cells and the initial parts of pyramidal ce11 axons in he visual cortexsR.**2.?JX ), by far most types of synaptic contacts in the brain of vertebrates do not the cellular reveal specificity at leve1 ). This suggests that in (e.g. 78 88.98.139.lXl.1Yl.236.?37.273.276 laminated brain structures not SOmuch (chemo-) specific ce11to ce11interactions. but rather a refined lamination pattern of pre- and postsynaptic elements with competitive intralaminar interactions is used as a mechanism to realize specificity of synaptic connections, and renders the concept of laminar specificity rather plausible. The attractiveness of this concept of laminar specificity. even indicated as the ‘sine qua non’ of laminated structurest”. is that it may explain the formation of complex circuitry patterns in terms of relatively simple anatomica1 organizing principles. 3.1.4.2. Laminar specificity in tectal circuitr),. The concept of laminar specificity as defined in the preceding section implies both the existence of presynaptic zones and the absence of cellular specificity within these zones.
different
types of postsynaptic
type of tectal
structures
5150. Secondly, the similar, characteristic of contacts on al1 postsynaptic structures
in layer mean size in certain
layers, dendrites of type XIV excluded, might indicate that these structures are al1 contacted by the same population of presynaptic elementsts’). Thirdly, the concept of laminar specificity is closely associated with mechanisms of competition. Within the goldfish tectum, the different presynaptic structures that occur in each presynaptic zone might well compete for available postsynaptic sites, since the different types of postsynaptic structures each have a restricted, predetermined number of synaptic contactst”” (see section 2.2.2 and Fig. 8). The results of Murray et al.167, who found the same retina1 terminal density in tetta with a norma1 and with a ‘compressed’ retinotectal projection, are also in support of competitive mechanisms regulating synapse formation. Adoption of the hypothesis of laminar specificity for the goldfish tectum completes the set of structural organizing principles that are necessary as starting points for a tectal circuitry diagram. In summary, these organizing principles are (cf. Fig. 8): (a) the occurrence of presynaptic tectal zones or laminae. each with a characteristic population of presynaptic structures; (b) determination of interlaminar interrelations (i.e. interrelations between presynaptic structures in different presynaptic zones) by the characteristic location, dimensions and synaptic density of the postsynaptic tectal structures; and (c) determination of intralaminar interrelations (i.e. interrelations between presynaptic structures within a single presynaptic zone) by rules of laminar specificity. The resuhing tectal circuitry diagram which emerges from these principles is drawn in Fig. 9. This figure is derived from Fig. 7 by introduction of the following modifications: (a) axons have been drawn as lines; (b) information on the dendritic extensions and frequency of occurrence of tectal ce11 types is in-
265
TL
lLTLl
7.
NP VIS AP Ret NI NRMT
TEL (NDL) cTect TS NRS (Ret) dendrltk 0 1
r
-
I
dendrltc
~75 ,.uum (7 75-199ANn 200-3C0pm cl >300,um
norma1 1arge
number
of
0 fy
5c!o- 2cw 2500-10000 5000-20000
B
1-2 milhon
Fig. 9. Circuitry diagram of the goldfish tectum. Dendritic shafts are indicated by vertical bars and dendritic trees by horizontal bars. The latter are located as indicated in Fig. 7. Type XIV neurons have been drawn in a deviating way because of their peculiar properties (see section 3.1.4.4). Axons have been drawn as lines and are also located as indicated in Fig 7. In addition. the possibly efferent collaterals of some type XIV axons (see Fig. 6 and section 2.3.1) have been indicated. Neurons with obscure axonal properties (type 11, X1 and XV) have been omitted. (Supposed) synaptic connections are indicated by arrows. The dendritic extension, the dendritic density and the number of neurons per tectal half (according to Meek and SchellartiQ) are encoded as indicated left below in this figure. The cell groups indicated (a-f) have been discussed in sections 3.1.1.2 and 3.1.1.3 (see also Fig. 7).
cluded;
(c) (presumed)
synaptic
contacts
are indi-
cated by arrows; and (d) type XIV neurons have been drawn in a special way because of their peculiar role in tectal circuitry, which will be outlined below. 3.1.4.3.
Quantitative elaboration
ficity in tectaf circuitry.
of laminar speci-
The tectal circuitry diagram depicted in Fig. 9 reveals a complex pattern of intratectal connections. For an evaluation of the relative importance of these connections, a quantitative analysis is necessary. Such a quantitative circuitry analysis needs additional assumptions in the field of the laminar specificity hypothesis. For. interlaminar interrelations may be quantified on the basis of the characteristic numbers of synaptic contacts of the postsynaptic structures in the different presynaptic zones (Fig. 8). However, for precise quantification of intralaminar interrelations too few data are available. For example, in layer 5 the axons of about 200,000 retina1 ganglion cells terminate, but only 2500-10,000 type 111 axons and 500-2000 type VI1
axonsts*. The number of other types of presynaptic structures in this layer is unknown. The number of synaptic contacts made by each type of presynaptic strutture is also unknown, except for the number of retina1 fiber synapses, which has been estimated at about 30 milliont50 or more than 50 millionl@ (see section 2.1.4). For other layers a similar lack of quantitative data is encountered. In the absence of more precise data, the most simple ‘quantitative laminar specificity hypothesis’ has been adopted for a first approximation. This reads: Within a certain presynaptic
zone al1 types of presyn-
aptic elements distinguished
(as indicated
are presumed
in Fig. 8),
to make equa1 tota1 numbers of synaptic
contacts, the axons of type XZV excepted.
Assumptions regarding type XIV axons will be presented in the next section, and severa1 implications of the remaining part of this quantitative laminar specificity hypothesis will be discussed in more detail in section 3.4.
266 3.1.4.4.
Considerations
regarding
type XIV
rons. Type XIV neurons
constitute
ulation
from the remaining
of cells, deviating
ce11 types by their
large
frequency
a peculiar
neu-
based on the morphological
pop-
XIV axonsis2 as well as on the distribution of SS terminals in the tectum of Holocentrusl”6, which most
tectal
of occurrence
(about 1000 times more than other tectal ce11 types), their heterogeneity and their less strict dendritic and axonal lamination pattern (Fig. 5). These properties of type XIV neurons require separate quantitative assumptions
for their synaptic connections,
since the
quantitative laminar specificity hypothesis formulated above does not seem to be useful for these numerous cells. Fora quantitative analyses of tectal circuitry, two alternatives will be considered with respect to type XIV neurons. Both alternatives only apply to the average intratectal connectivity pattern of the tota1 population of type XIV neurons. For a more detailed analysis of possible subtypes too few data are available at present (see also section 3.4). First, the axons of type XIV neurons will be presumed to make exclusively synaptic contacts with type XIV dendrites, and not at al1 with other types of neurons. In other words, their axonal synaptic contacts are considered to be completely cellular specific. Although this assumption is probably too extreme, a certain degree of preference for mutua1 synaptic contacts is not unlikely for type XIV neurons, since both their dendrites and axons have smaller synaptic contacts than the remaining structures in the same layersis”. The major advantage of this presumed alternative is that it allows the analysis of the rather strictly organized circuitry of type I-X111 neurons. The results of this analysis, in turn, can be used as a basis for evaluation of the influente of type XIV cells in tectal circuitry. It should be noticed that this alternative does not imply that other axons would not contact type XIV dendrites. These contacts are presumed to follow the rules of the quantitative laminar specificity hypothesis formulated above. The second alternative that will be considered implies complete absence of cellular specificity for type XIV axons. Their synaptic contacts are now presumed to be laminar specific with the following quantitative elaboration: axons of type XIV cells are supposed to constitute 50% of al1 contacts in layer 5 and 516; 25% of al1 contacts in layer 415; 75% of al1 contacts in layer 4; 33% of al1 contacts in layer 314 and 50% of al1 contacts in layer 3. As is outlined in detail in the appendix (section 7.2), this distribution is
probably
characteristics
of type
are for the major part constituted
by type
XIV axons (section 2.2.2). Thus, with respect to the distribution of type XIV axon terminals, this condition represents
the most plausible
ent. However,
it is extreme
estimation
in presuming
at pres-
no cellular
specificity at al1 for type XIV axon terminals (see above). Consequently, the two alternatives to be considered for type XIV represent two extremes, somewhere in between of which the reality may be expected. Details with respect to both of these conditions are presented in the Appendix (section 7). 3.2. Calculation
of the connectivity
index
and the
connettive importance
On the basis of the starting points outlined above both a qualitative and quantitative structural analysis of tectal circuitry is possible. The quantitative part of this analysis will be performed in terms of connectivity index and connettive importance, which will be defined and explained in the next paragraphs.
Connectivity diagram and numbers of contacts
-
b
____J
r
c
-15orz=!=l
c
I y(l)~O50(b)+0.20(1)+0.3O(c) y (2)=040(a)+0.25(b)+O
Connectivity index
Connectlve
~ r(l)=0.63(B)+O37(Cl
‘mportance
i
r(2)=040
a
35 (1
)
CA)+ 0.47(B)+O.f3(C)
b
c
-100%
1
A
B
C
4100%
Fig. 10. Some quantitative connectivity parameters, iliustrated by a simple (hypothetical) circuit. For definitions, calculations and details, the reader is referred to sections 3.2.1 and 3.2.2.
267 3.2.1, Connectivity index Connectivity indices are meant to indicate the relative contribution of different types of presynaptic elements to the tota1 population of receptive synaptic contacts of a ce11type, They represent the ratio between the number of contacts of each type of presynaptic element with a particular ce11type and the tota1 number of receptive contacts of that ce11 type. TO take an example (see Fig. 10): if neurons of ce11type 1 have on average 250 contacts with afferents of type b, 150 contacts with afferents of type c and 100 synaptic contacts with axons of neighboring type 1 neurons, the connectivity index (y) of ce11type 1 with respect to type b equals 250/500 = 0.5 or 50%. In formula: y(l,b) = 0.5 The formulae with respect to type b and type 1 axons are: v(l,c) = 0.3 $,l)
= 0.2
a summarizing formula is: y(1) = 0.5(b) + 0.3(c) + 0.2(l). The values calculated can also be presented in a matrix (Fig. 10). The connectivity indices of the tectal ce11types, as calculated in the appendix, are presented in Table 111, which represents a matrix of tectal circuitry. The procedure followed may be summarized as follows (for details the reader is referred to the appendix): For type 1,111, VI, X11, X111 and XIV, the relative contribution of presynaptic structures occurring in different presynaptic zones is estimated on the basis of the number of contacts on the ce11types in these different presynaptic zones (see Fig. 8). For type IV, V, VII, VIII, 1X and X, where these numbers of contacts are not available, the relative contribution of presynaptic structures occurring in different presynaptic zones is estimated on the basis of the extension of their different receptive components in the different presynaptic zones (see Fig. 5), which supposes a homogeneous synaptic density along these components, The relative contribution of presynaptic structures occurring in the same presynaptic zone is approximated on the basis of the quantitative laminar specificity hy-
pothesis formulated in section 3.1.4.3. This implies an equa1 ~ont~bution of al1 pres~aptic structures in a single presynaptic zone, except for axons of type XIV. The connectivity indices of the tectal ce11types are calculated for both altematives considered with respect to type XIV axons, which means at first without taking account of the influente of type XIV axons, and secondly by assuming an extremely large influente of type XIV axons (see section 3.1.4.4). 3.2.2. Connettive importance Each tectal neuron can be considered as a relay station in the multiple pathways between tectal afferents and efferents (see Fig. 9). TO be able to evaluate the significante of the tectal ce11types in this respect, a parameter has been calculated which quantifies the tota1 set of mono-, bi-, and multi-synaptic connections between afferents and ce11types, This parameter has provisionally been termed ‘connettive importante’ since it indicates the importance of afferents exclusively on the basis of quantified connettive relations and should be distinguished from conceptions like electrophysiological, neurochemical, or functional importance. Mathematically, eonnective importances are calculated by algebraic solution of the connectivity indices-formulae in terms of afferent input. This solution is possible on the basis of the principle that, because of the integrative properties of neurons, the connectivity index of a certain ce11type represents, in fact, the connectivity index of each axonal synaptic contact of that ce11type. TO take an example (Fig. 10). If y(l) = 0.5(b) + 0.3(c) + 0.2(l), substitution of y(l) for (1) leads to the following result: y(l) = 0.5(b) + 0.3(c) + 0.2 y(l), or y(l) - 0.2 y(1) = 0.5(b) + 0.3(l), or I’-(l) = 0.63(B) f 0.37(C). TO distinguish them from ~onne~tivity indices, connective importances are indicated by capitals (IY, B and C instead of y, b and c). The formula just calculated means that the connettive importance of afferents of type b for ce11 type 1 is 63% (I(l,B) = 0.63) whereas the connettive importance of afferents of type c for ce11type 1 is 37% (I(l,C) = 0.37). TO
268 take ce11type 2 of Fig. 10 as another example: If y(2) = 0.40(a) + 0.25(b) + 0.35(l), substitution of I( 1) for (1) yields the following result:
type XIV neurons
Together y(2) = 0.40(a) + 0.25(b) + 0.35 I(l), y(2) = 0.40(a) 0.37(C)}, or
+
0.25(b)
+
3.1.4.4).
The calculation
with Fig. 9, these matrices provide the ba-
sis for the analysis of tectal circuitry to be presented
or
0.35
(section
of tectal connectivity indices and connettive importances is outlined in detail in the appendix (section 7).
(0.63(B)
+
in the next section. 3.3 Anafysis of tectal circuitry
y(2) = 0.40(a) + 0.25(b) + 0.22(B) + 0.13(C), or In this section
I(2) = 0.40(A) + 0.47(B) + 0.13(C).
The
connettive
importance
just
defined
the tectal circuits
involved
in the
processing of the 4 main streams of tectal input are analyzed on the basis of the starting points, diagram may
be
called overall connettive importance since it is related to mono-, bi-, and multi-synaptic connections. This overall connettive importance may be split up into direct and indirect connettive importance. The direct connettive importance indicates the relative contribution of direct, monosynaptic afferent contacts to the contacts of each ce11 type, and equals the connectivity index of the ce11types with respect to the afferents. The indirect connettive importance indicates the importance of bi- and multi-synaptic connections between afferents and ce11types, and equals the differente between the overall and direct connettive importance. A suitable way to present quantitative aspects of circuitry is a matrix with both connectivity indices and connettive importances. From such a matrix the numerica1 importance of the different types of connections of a ce11 type can be seen as well as that of the direct and indirect connections of the afferents. TO take ce11 1 of Fig. 10 as an example: the direct connettive importance of afferents of type b is 50% (= connectivity index); the overall connettive importante is 63%, and consequently the indirect importante is 13%. Furthermore, it can be seen whether the connettive relations between afferents and ce11 types are exclusively monosynaptic (OCy=I; e.g. connections between a and 2 in Fig.10). exclusively bi- or multisynaptic (O=y
(Fig. 9) and matrices (Table 111) presented. First, tectal circuitry will be described without consideration of the axons of celi type XIV (i.e. the first alternative for type XIV, see section 3.1.4.4 and the Appendix). This part of the analysis is illustrated by Figs. 11-14. The design of these figures is basically similar to that of Fig. 9, with the following modifications: (1) the cells have been placed in a rough sequence of importante with respect to their significante for the type of input under discussion; (2) cells which are not involved in a particular circuit have been omitted; and (3) the connettive importance of the type of input discussed is presented. Secondly, the results of this analysis will be compared with the second alternative type XIV (see section 3.1.4.4 and the appendix), which imphes an extremely large influente of this cell type. The comparison of both alternatives for type XIV is illustrated by Figs. 15 and 16. 3.3.1.
Tectal circuitry involved
in toral input proc-
essing
(i.e. afferents of the torus fongito layer 7 and terminate exclusively on the apical dendrites of type 1 neurons (Fig. 11). Although type 11 neurons have processes in layer 7 as well, there is good evidente for Eugerres and Holocentrus that these processes are presynapticr”6.22Q64. Their small number in the tectum of cyprinids might explain why these structures have not been observed in the goldfishI@ and the carp31,1”3. Judging from the distribution of synapses on type 1 neurons, the direct connettive importance of toral input for these neurons is as large as 90%. The axons of type 1 neurons terminate specifically in layer 3/4. where severa1 types of postsynaptic structures occur, including the basa1 dendritic tree of type VIII. type Tora1 afferents
tudinalis), are confined
269 TABLE 111 Two connectivity matrices of the goldfish tectum, based on the starti@ points and methods outlined in section 3.1 and 3.2, respectively
Matrix A holds for the first alternative assumed for type XIV axons, matrix B for the second alternative (see section 3.1.4.4.). The procedures and calculations applied are detailed in the appendix (section 7). A Ce11
Type of axon
tvpe
vis
tor
3 42 33 33 17 13
90
1
111 IV
VII VIII 1X V‘t V, XIV VI X X11 X111
Type of input te1
deeo
Os
1
III
IV
VI1
VIII
0,
0, 29
2
0, 29
2
7 13 20
22a
33 5a
30 13 6 6
20 7 13
13 20 33 9a
7
33 27 17 13
v,
XIV
v,
0,
0,
13 10 50
13 10 50
VIS
TOR
TEL
DEEP
7 91 74 77 47 39 39
92 4 12 11 25 29 29
61
13
2 5 14 12 28 32 32 50 17
50 10
64 39 26 17
17 29 13 8
19 32 20 21
33 4a
15a
7 39 50
33 27 17 13
IX
20 3 4
4 3
7a
3 13 2 3
15n
7 4 3
7a
3 13 2 3
8a
25 10 15 4
Sa
25 10 15 4
2a
100 (l-a)
4 8 + 100%
connectivity index t
t
41 54 + 100%
‘L annective importance f
B Ce11
Vi.?
1
111 IV VI1 VI11 1X V, V,
Type of input
Type of axon
2 28 25 23 13
10
tor
te1
90
0,
1 03
IV
III 03
14 3
8
8 13
13 17
17 8
XIV
13
3
VI X x11 X111
26 10 3 3
13 4 7
t
deep
37 46
3 13 2 3
1
VII
03
1x
v,
V3
XN
VIS
TOR
TEL
DEEP
17
3 43 25 30 40 38 75 50
6 73 70 70 54 48 55 34
91 6 8 8 15 19 10 5
1 8 10 10 18 22 14 27
1 13 12 12 13 12 21 33 22
1
14 25 20 13 10
3
25 20 13
10
8
5
8
3
3 10 1 2
3
2 1
VIII
2 1
connectivity index t
1X and type X neurons, ce11 bodies of type 1X and type X neurons, and dendritic shafts of type X11, type X111 and type XIV neurons (Fig. 11). Some of the type XIV neurons may have considerable dendritic trees in this layer as well. Thus, the most important candidates for further processing of toral input are type VIII, type 1X and type X neurons. Type VI11
3
3
3 13
3 13
5
2
2
1
44
57
9
12
3
10 1
6 3 4
6 3 4
2
1
1
50 38 37 2 28 4 -+ 100%
68 48 34 26
7 19 7 6
10 22 11 13
15 12 48 54 + 100%
?- connettive importance f
and type 1X neurons are interneurons, which may bring about an upward transport of information from layer 314 to layer 4/5 and 4, respectively. From layer 41.5,a further upward transport to layers 5 and 516 can be effected by the axons of type VII neurons. At this tectal level, however, the connettive importance of toral information is rather low (about lo%, Fig. 11).
270
tor 6
--
The i
_ -
connectlve
Importance toral
XIV
of
Input
Fig. Il, Tectal circuitry involved in the processing of input from the torus longitudinalis. The tectal neurons and their dendrites, axons
and (presumed) synaptic contacts are visualized as explained for Fig. 9. The neurons have been placed in a rough sequence of importante with respect to the type of input presented. The connettive importance of this input for the tectal cell types is indicated by the interrupted or black lines drawn as continuations of the tectal axons. These lines encode the connettive importance as calculated in the appendix for the first alternative (see Table MA). Completely black lines indicate a connettive importance of 100%; white lines would indicate a connettive importance of 0%. For further details, the reader is referred to section 3.3.1.
A great number of synaptic contacts between the axons of type XIV neurons and the other ce11types (the second alternative for type XIV, see section 3.1.4.4) would decrease the connettive importance of toral signals in tectal circuitry. since type XIV neurons are in general no important targets for type 1 axon terminals (Fig. 15 and 16). The most direct route from the toral input in layer 7 to tectal output is a two-synaptic pathway via type 1 and type X neurons. The connettive importance of toral input for type X neurons, however, is not very large (about 30% in the first alternative). The other tectal efferent neurons seem to be influenced to a still lower extent by toral signals, while this influente is provided mainly by pathways involving 3 or more synapses (Fig. 11). SO. the circuitry involved in the processing of toral information in the tectum has a number of peculiar
characteristics. No tectal efferent neuron is directly contacted by toral afferents. Al1 toral input is received by one specific type of interneuron, which conducts toral information downwards to one specific layer (layer 314). In this layer, again interneurons constitute most of the postsynaptic structures, which, in turn, effect an upward transport of toral information. Only one efferent neuron (type X) has dendrites specifically in layer 314, but the connettive importance of toral input for this efferent ce11type is not larger than 30%. Consequently, there seems to be a remarkable discrepancy between the large amount of toral input to the tectum and the low degree of representation of this input in the tectal outflow. 3.3.2.
Tectal circuitry involved in visual input proc-
essing
As described
in section
3.1.1.1,
the layers 5/6, 5
271 d
b --AA. Ill
IV
VII
VIII
IX
C
a
e
v
I
XIV
f VI
x
XII
XIII
_-----Il1
NP AP vis Ret
-___--
i
V,, vis
_---------_----_ ------
NRMT 4
-
3
1
Il"'
I
I
I
’
:>
’
’
;
:
0
I i
Ii
-
-
XIV
-
-
XIV
-
-
XIV lV
-
-
-
-
-
VIII ,X v4 I
XIV
The connettive importance of visual Input
I,
Fig. 12. Tectal circuitry involved in the processing of visual input. For explanation and details, the reader is referred to the legends of Figs. 9 and 11 and to section 3.3.2.
and 4/5 receive visual input by way of the retina1 fibers as well as by afferents from the nucleus pretectalis, the area pretectalis and the nucleus isthmi. Although these layers may also contain a small number of non-visual afferents (section 3.1.1. l), for the sake of simplicity the input of layers 415, 5 and 516 (the SGFS) will be considered as 100% visual in the following discussion. The visual afferents most probably make synaptic contacts with al1 tectal ce11 types except for types V and XV, the only ce11 types without dendrites in the visual afferent layers (Fig. 12). Type 111, IV and VI1 neurons may be considered as specific visual interneurons, since they have their postsynaptic structures exclusively in the visual afferent layers. They may also process some non-visual information by way of contacts with the axons of type VI11 neurons (type IV and VII) or of type VI1 neurons (type III), but this is probably only a low percentage (Fig. 12). The axons of type 111 and of type VI1 neurons terminate in layer 5 or 5/6, where no other interneurons have axon terminals, except type XIV, which will be discussed below. This stresses the importance of this layer for visual information proc-
essing, since not only the visual afferents appear to terminate in layer 5, but also the axons of the visual interneurons type 111 and type VII. Type IV neurons have their axon terminals in layer 4/5. Apart from the visual afferents, layer 4/5 also contains the axons of type VI11 neurons, which may provide some non-visual information from deeper tectal levels (Fig. 12). This suggests that layer 4/5 is somewhat less ‘visual’ than the remaining part of layer 5. Layers 4 and 314 may only receive ‘indirect’ visual input via the axons of type 1X and type 1 respectively, which bring about a downward transport of visual information. The connettive importance of visual input for type 1 cells is only about 5%, whereas this value for type 1X neurons is about 40% (Table 111). The connettive importance of visual input for type XIV neurons is about 60% under both alternatives assumed (Table 111). The main effect of a large number of contacts between axons of type XIV neurons and dendrites of other cell types would be a strong downward flow of visual information from SFGS to SGC, where type XIV axons have many terminals (Figs. 7 and 12). This, in turn, would in particular en-
272 large the influente of visual information on the tectal efferent neurons (Table 111and Fig. 16). Most likely,
al1 types of efferent
tectal
neurons
have direct synaptic contacts with visual afferents (Fig. 12). For type VI and type X11 this has been confirmed in the electron-microscopei49.
According
to
the present analysis type VI neurons represent the most ‘visual’ efferent neurons, since they are located in the visual afferent layers (Table 111 and Fig. 12). The position
of the dendritic
trees of type VI cells
raises some questions, however. Ultrastructural studies revealed that their apical dendritic tree, preferentially
located in the superficial
part of layer 6, is
not contacted by retina1 fiberst@J50. Since interneurons equally have no axon terminals in this region, except for some type XIV neurons, it is not clear which presynaptic structures make contacts with the apical dendritic tree of type VI neurons. Possible candidates are the retina1 terminals that constitute the thin superficial band of the retino-tectal projection (Fig. 4), which then should have ultrastructural characteristics deviating from the bulk of the retinotectal fibers (section 2.2.2). Other candidates are fibers from the nucleus pretectalis, area pretectalis, nucleus isthmi or nucleus or the rostral mesencephalic tegmentum, which, then, should terminate specifically in the superficial part of layer 6. It is important to notice that Laufer and VanegaG have described large axons at this tectal leve1 which do not degenerate after eye-enucleation. Although Laufer and Vanegasi considered these fibers as tectal efferents, it is equally conceivable that they constitute non-retina1 afferentslsl. Disregarding these uncertainties, the apical dendrites of type VI neurons are assumed to receive 100% visual input (Fig. 8). The basa1 dendritic tree of type VI neurons, preferentially located in layer 4 just below layer 4/.5, also makes no synaptic contacts with terminals identified as retina1 fibersi@J50. Although it might be possible that the axons of type IV, type VI1 and type 1X neurons make some synaptic contacts with the basa1 dendritic tree of type VI, most probably type XIV axons make most of the synaptic contacts on this dendritic tree. This would be in line with the high frequency of occurrence of type XIV axons in this layer and with the small size of the synaptic contacts of the basa1 dendrites of type VI cellst50. This implies that, at least for layer 4, the second alternative assumed for
type XIV seems to be more realistic than the first one (see section 3.1.4.4). The connettive efferent
importance
of visual input for the
ce11 types X, X11 and X111 is at least 40%,
25% and 15%, respectively (Table 111). Most of the visual information reaches these neurons via bi- or multi-synaptic pathways (Table 111 and Fig. 12) although al1 these tectal efferent neurons constitute monosynaptic pathways between visual input and tectal output as well. The percentages enumerated increase with increasing type XIV neurons
involvement
in tectal circuitry
of the axons of (Table 111 and
Fig. 16). Summarizing, the characteristics of the circuitry involved in visual input processing in the tectum are about the contrary of those of the circuitry involved in toral input processing. Whereas toral input is received by a single type of neuron, visual input is directly provided to almost al1 tectal neurons, and whereas toral afferents do not contact efferent neurons directly, al1 efferent neurons have direct contacts with visual afferents. A further contrast between toral and visual input processing is the simplicity of the toral afferent layer 7 (only one type of presynaptic element and one type of postsynaptic element) and the complexity of the visual afferent layer (layer 5 and its boundaries), where at least 9 types of presynaptic elements and 13 types of postsynaptic elements are involved in tectal circuitry. A further characteristic of visual input processing is the occurrence of severa1 types of visual interneurons which make synaptic contacts close to the contacts made by the visual afferents, an arrangement not realized for the toral input. Visual input seems to have a relatively high influente on the tectal outflow, whereas the toral influente on this outflow seems to be low (Fig. 16). 3.3.3.
Tectal circuitry involved in telencephalic
input
processing
Tectal circuitry involved in the processing of telencephalic input resembles to some extent the circuitry involved in toral input processing, since telencephalic afferents terminate at the same tectal leve1 (layer 3/4) to which type 1 axons convey their toral information (cf. Figs. 11 and 13). Accordingly, just as has been discussed for toral input (section 3.3.1), some part of the telencephalic input to layer 314 is trans-
273
&A, IX
~_
VIII
v
IV
VII
f
a
b
c
d
Ill
I
x
XIII
e XII
VI
XIV
7
6
-
Tel
.
.
:eI
_------
v3 -
-
XIV
2
1
The connectlve importance of telencephalic input
Fig. 13. Tectal circuitry involved in the processing of telencephalic input. For explanation and details, the reader is referred to the legends of Figs. 9 and 11 and to section 3.3.3.
ferred upward via the axons of type VIII, 1X and VI1 (Fig. 13), and the most important type of efferent neuron for telencephalic information is probably type X. A large influente of type XIV neurons would likewise decrease the influente of telencephalic input on the tectal outflow (Fig. 16). The main differences between the circuitry for toral input processing and that for telencephalic input processing concern the involvement of type 1 neurons and layer 7 in toral information processing, and the fact that telencephalic afferents are probably less strictly concentrated in layer 3/4 than the axons of type 1 neurons. Consequently, in contrast to the situation for toral input, there does exist a monosynaptic pathway from the telencephalic input to the tectal output via type X neurons and probably also via type X11 and type X111 neurons. Of the latter two, type X111 neurons might be the most important ones in this respect, since their dendrites in layer 3, preferentially located just below layer 3/4, might well have synaptic contacts with telencephalic afferents
(Fig. 13). Type X11 neurons receive most of their telencephalic input via contacts of their dendrites in layer 4 with axons of type 1X. However, for the same reasons as discussed above for the dendrites of type VI neurons in layer 4, type XIV axons probably constitute most of the presynaptic elements of the dendrites of type X11 neurons in layer 4. This would reduce the telencephalic influente on type X11 neurons substantially (Fig. 16). The ratio between telencephalic and toral input in layer 3/4 is not clear, since the number of telencephalic afferents, as well as the number of contacts made by these afferents is unknown. Under the conditions assumed by adopting the quantitative laminar specificity hypothesis (section 3.1.4.3), telencephalic input seems somewhat more important than toral input because of the involvement of type 1 neurons, but this is merely hypothetical. A striking point, however, is the competing character of the telencephalic and toral (i.e. cerebellar) afferent systems in tectal circuitry. The larger the influente of either one, the smaller
274 C
,,--\ V
.._
, cXIII
f
~_L_ XIV
~\ Xll
e
~.
_
XIV (‘large’)
,
9 -J\_., xv
7
6
5 XIV
XIV XIV (‘large’) XIV
----
v3
3
XIV
NRS c. iecr.y (RetI
‘deep’
2
1
The connettive of ‘deep’ tectal Input
’ 1
’ ’
! importance
’ ’
:
I
’ ’
I i
1
]
I
I
i l
!
_j
Fig. 14. Tectal circuitry involved in the processing of ‘deep’tectal input. For explanation and details, the reader is referred to the legen& of Figs. 9 and 11 and to section 3.314. -
the influente of the other will be, since both have to be integrated to a large extent by the same postsynaptic structures. It should be mentioned that afferents from the mesencephalic nucleus dorsolateralis also terminate in the SGC. For the sake of simplicity, however, these have been left out of discussion. The importante of this afferent system is obscure at this moment. The same holds for the few retina1 fibers terminating at this tectal level. 3.3.4. Tectal circuitry involved in deep tectal input proces~ing The so-called ‘deep’ tectal afferents, including fibers from the contralateral tectum, the torus semicircularis, the reticular formation, the retina and presumably severa1 other systems (see section 3.1.1.1), terminate almost exclusively directly on the large tectal efferent neurons, type X11 and type X111, which
have large dendritic trees in the deep afferent layers 2 and 3 (Fig. 14). Interneurons hardly occur in these layers, except for some type V neurons in layer 3, and the dendritic shafts of type XIV neurons. SO, in this respect the circuitry involved in deep tectal input processing seems to be the opposite of the circuitry involved in toral input processing, since deep tectal afferents terminate predominantly on efferent neurons, whereas toral afferents terminate exclusively on interneurons. Visual and telencephalic input processing take an intermediate position in this respect, since visual and telencephalic afferents terminate on both intemeurons and efferent neurons. A large number of contacts of type XIV axons with al1 tectal ce11 types would result in a substantial upward transport of deep tectal input to layers 4 and 5 (Fig. 15) and would increase the influente of deep tectal input on tectal interneurons as well as on efferent tectal neurons (Fig. 16).
275 without
1
tor
influente
fi
of type XIV
/-%
vis
......................** .... ~.?.%:::>:.Y.-* :.:~.:.:.:.:.:~.:.:.:.:.~ ...........I.. %%%z%%-::. ............................
tel
deep
influente
tor
’
vis
A
of
type
--~ tel
XIV I deep
7
*:z::::::.V.V:. m............. .~~\:;%:%~~~%~* ..zCzxx.~~~~~ %%%%V~.f’.‘.‘.‘.: 6
.::: : :
1..
:.
..:.
5
::
..’
:
.’
_:
:
:.::..
:
::..:
...:::. 4 .,
:.:
El
50% -_OY_
. . .:
:. :...
.,.,
..
nndirect connectlve Importance
; .:
3
2
Fig. 15. The direct and indirect connettive importance of the main types of tectal input in the different tectal layers. Part A holds for the first alternative and is based on formulae 14a-21a and 14b21b (see appendix, section 7); part B holds for the second alternative and is based on formulae 14c-21c and 14d-21d. For further details and discussion, the reader is referred to the text (section 3.3.5).
The circuitry involved in deep input processing in the tectum may, however, be more complex than suggested above for two reasons. Firstly, type XV neurons, a population of neurons with dendrites predominantly in layer 2 and 3, are not included in the preceding discussion because their axonal properties are obscure. Nevertheless, they will be involved in the deep input processing because of their dendritic properties. A portion of type XV neurons might well be interneurons with axons terminating in the tecturn, but others give rise to tectal efferents, as indicated by Romeskie and Sharmazm. Secondly, in particular the so-called ‘large’ subtype of type XIV neuronsls* may have considerable dendrites in layer 2 and/or 3. Consequently, these cells might have a still more important function in the integration of visual and ‘deep’ tectal input than the bulk of type XIV neurons (Fig. 15). Both Meek and Schellartl52 and Romeskie and Sharma*m consider these large type XIV
neurons cells . 3.3.5.
as interneurons,
just as the other type XIV
The connettive importance of tectal afferents in
the different tectal layers In the previous sections of this chapter the circuitry involved in the processing of the 4 main streams of tectal input has been analyzed. From this analysis the following stratification pattern emerges with respect to the connettive importance of the different types of tectal input (Fig. 15; for calculations, see the appendix, section 7). The 4 levels of distinct tectal input (see section 3.1.1.1) remain clearly distinguishable. However, in the interjacent layers a considerable mixing of the different modalities may be brought about by tectal interneurons, in particular in layer 3 and in layer 4 (Fig. 15). Only the boundary between layer 7, the toral input layer, and layer 6, the visual input layer is very sharp. Consequently, layer 7 can
276 be considered exclusively as a relay station for toral (i.e. cerebellar) input to the tectum, with no other re-
drites in layer 314).
lations with the deeper tectal layers than via the api-
Type 111, IV and VII neurons may be considered as visual interneurons, since the direct as well as the in-
tal dendrites of type 1 neurons. In this respect, type 1 neurons could equally well be considered to be tectal
direct connettive importance of visual input for these neurons is relatively large. Type IV and VII have
afferent
very extensive dendrites which make them suitable fora function in spatial interaction and integration of
elements
as to be tectal interneurons.
other sharp boundary 2 and layer
can be observed
1, the stratum
contains exclusively tic contacts.
between
periventriculare,
celi-bodies
Anlayer which
with very few synap-
The remaining part of the tectum, layers 2-6. is constituted by closely interrelated layers with only gradua1 transitions
from one layer to another.
The
superficial part, layers 6 and 5. is predominantly involved in visual information processing (Fig. 15), whereas the deep layer 2 is almost exclusively involved in ‘deep’ information processing. In layer 3 a considerable mixing of visual and ‘deep’ input might occur by means of the action of type XIV neurons (cf. Fig. 15A, B). In layer 314, just in between the deep. predominantly non-visual and the superficial, visual layers, the telencephalon and the cerebellum exert their influente, the latter after interposition of the torus longitudinalis. In layer 4 some degree of mixing between visual, telencephalic and toral information is realized. The connettive importance of visual input in this layer strongly depends on the involvement of type XIV cells (cf. Fig. 15A, B). Layer 41.5is remarkable because of the large extension of severa1 dendritic trees, suggesting an important function in spatial integration of visual input. The overall pitture of the connettive importance of the 4 main types of tectal input in the different tectal layers as presented in Fig. 15 clearly suggests that the laminar organization of the tectum is primarily relevant for multimodal integration. 3.3.6. The connettive relations of the tectal ce11types The connettive relations between the 4 main types of tectal afferents and the tectal ce11types, as numerically presented in Table IH, are visualized in Fig. 16 and have been analyzed in detail in section 3.3.1.-3.3.4. In summary, the following may be noticed. Type 1 neurons may be considered as the tectal afferents for toral (cerebellar) input. In addition, they may process some amount of visual input (via dendrites in layer 5) and telencephalic input (via den-
visual signals. The location of their dendrites in layer 4/5 may also indicate a function in integrating visual input with some amount of telencephalic and toral input, which reaches layer 415 by means of the axons of type VI11 neurons.
The bistratified
character
of type
VII may suggest that this type of neuron integrates more aspects of visual information than type IV and type 111 neurons. Type 111 neurons seem to be the most visual interneurons (Fig. 16) which is also suggested by their relative high percentage of direct contacts with retina1 fibersis”. Since their dendrites are not SO extensive, they are more likely involved in tempora1 aspects of visual Signa1 processing than in spatial aspects. The bulk of type XIV neurons can also be considered as visual interneurons (Fig. 16), although for some subtypes other modalities may be important as well. Their large number with respect to the number of retina1 and other afferents and their large variability make this ce11 type suitable for a number of specialized functions in Signa1 processing. Type V neurons, indicated as non-visual interneurons in Fig. 7, constitute a heterogeneous population, receiving different types of input depending on their position in layer 3 or 4 (Fig. 16). Their morphology suggests a function in spatial interaction between different tectal regions. Type XV might represent a second type of non-visual interneuron, involved in the processing of deep tectal input. Type VI11 and 1X probably integrate 3 different types of input: visual, telencephalic and toral input. Visual input seems the most important modality for type VIII, which has substantially larger dendrites in layer 415 than in layer 3/4, whereas for type 1X the toral/telencephalic input may be more important. This tendency is stressed when the position of the ce11 body and the origin of the axon is taken into consideration (see section 3.4). Among the efferent neurons, type VI neurons are probably specialized to transmit visual information beyond the tectum. Their receptive surface may integrate al1 aspects of visual information processing
277 “without” TOR VIS
type XIV TEL DEEP
VIS
with type XIV TOR TEL DEEP
B
Fig. 16. The connettive importance of the main types of tectal input for the tectal cell types, visualized by means of surface areas. Black parts indicate the direct connettive importance, grey parts the indirect connettive importance, and the total surface of the squares indicates the overall connettive importance. The size of the surface areas encodes the values calculated in the appendix and presented in Table 111as arranged in 10 classes: l-2,3-6,7-12, 13-20,21-30,31-42,43-56,57-72,73-90 and 91-100% connettive importance. Part A holds for the first alternative, part B for the second one. For further details the reader is referred to the text (section 3.3.6).
from layer 6,5 and 4. Type X neurons seem to be important for transport of toral and telencephalic information out of the tectum, integrated with visual information. The large efferent neurons of type X11 and type X111 may integrate information from al1 tectal input systems. For type X111 neurons, however, the deep tectal input seems to be dominant (Fig. 16). The importance of deep afferents is stressed by the
location of the ce11body and axon origin of type X111 neurons in layer 2. For type X11 neurons visual input is relatively more important than for type X111 neurons. The ratio between the influente of the distinct types of tectal input on type X, X11 and X111 depends to a large extent on the influente of type XIV neurons (see Fig. 16). The large degree of connettive differentiation as
278 shown in Fig. 16 suggests that the tectal ce11types can be considered as elements which each receive a characteristic sample out of the multimodal information available in the different presynaptic tectal zones.
proximation, it is clear that insight in tectal circuitry will be greatly improved when more becomes known with respect to their degree of cellular specificity, their number of axon terminals, the qualitative and quantitative characteristics of various subtypes, their
3.4. Critica1 evaluation of the framework presented
importance volvement
The analysis presented is not meant as a definite description of tectal circuitry - for this too little in-
(section 2.3.2).
formation
is available
at present -
but as a concep-
as origin of tectal efferents and their inin various extratectal feed back loops
The framework presented may be refined in several ways. The first one is to consider not only the num-
tua1 framework. This framework is constituted by a connectivity diagram (Fig. 9) and two matrices of
ber of synaptic contacts, but also their degree of symmetry, size and position. Incorporation of these addi-
connectivity indices and connettive ble III), and is primarily designed
tional synaptic characteristics in the connectivity matrices may be expected to have the following conse-
importances (Tato summarize the
structural data available in such a way that optimal comparison and integration with physiological data may be established. In particular Figs. 11-16 subserve this purpose. The framework constructed. however, is also useful to define precisely where and how it should be reinforced, refined and filled in to arrive at a more precise and definite description of tectal circuitry. In this respect the following may be noticed. Reinforcement of the frame should primarily be achieved in the field of the intralaminar interactions between presynaptic elements. These have been approximated by the rather plausible concept of laminar specificity, but the validity of this concept should be tested further. Only when the intralaminar distributions of presynaptic elements on the receptive surfaces of the different ce11 types have been analyzed qualitatively as well as quantitatively, a more definite mode1 of tectal circuitry comes into prospect. It should be noticed however, that adoption of the concept of laminar specificity is of rather low importance for the conclusions presented with respect to the multimodal integrative capacity of the tectum. This type of integration mainly depends on inter- (and not intra-) laminar interrelations, and it has been discussed that interlaminar interrelations are determined by the characteristic postsynaptic properties of the tectal ce11types. A second field of reinforcement of the frame to be mentioned concerns type XIV neurons. The function of this large population of neurons has been approximated by assuming two extreme alternatives for the intratectal connections of the ‘average’ type XIV neurons. Although this appears useful for a first ap-
quences. With respect to the degree of symmetry of synaptic contacts, it may readily be assumed that symmetrical synapses (with pleomorphic vesicles) are inhibitory, and consequently must get a negative sign in the connectivity matrices, whereas asymmetrical synapses (with round vesicles) are excitatory. Further, synapses with large contact zones most likely have a larger influente than synapses with small ones. This tends to enhance the direct connettive importance of afferents (see Meekis”, Table 2), whereas the connettive importance of type XIV neurons in tectal circuitry would be reduced, since their axons have relatively small contact zonesis(J. With respect to the position of synapses, it may be expected that contacts close to the axon hillock have a larger influente than more dista1 contacts. In general, this tends to enhance the functional differentiation between the tectal neurons as suggested by Fig. 16. Comparison of type X11 and X111, e.g., reveals that the axon hillock of type X111 is located in layer 2, which tends to enhance the connettive importance of deep tectal input for type X111. In contrast, the axon hillock of type X11 is situated more close to the visual layers 5 and 6. Equally. comparison of the position of the axon hillock of the related ce11 types VI11 and 1X in layer 415 and 314 respectively enhances the importance of toral and telencephalic input for type 1X. However. the position of synapses may also oppose their numerica1 properties. For example, the few retina1 fibers that contact type 1 neurons are close to the axon hillock. which tends to enhance their connettive importance for type 1 at the expense of that of the numerous toral afferents. Likewise, the relatively few retina1 fibers that terminate
279 in layers 3/4 and 2 are situated
close to the axon hill-
ock of the efferent type X11 and X111 neurons, might enlarge
the importance
tectal outflow. In spite of their relevance, characteristics mentioned rated in the connectivity reasons.
Firstly,
of visual input for the the additional
synaptic
have not been incorpomatrices for the following
the size and degree
might only incidentally
which
be incorporated,
of symmetry since for
most types of connections in this respect no data are available at present. Secondly, it is still obscure which parameters should be exactly considered: is it the diameter, the circumference or the surface of the contact zones, or should one consider the complete apposition zone? Should one consider the distante to the axon hillock, its root, its square or something else and how should one incorporate the diameter of dendrites and the occurrence of spines? How should the large number of contacts be taken into account which are intermediate between clearly asymmetrical and symmetrical contacts, and what is the relation between these parameters and types of neurotransmitters? These are al1 questions pertaining to the interface of histology and physiology, and incorporation of some rather arbitrary structural factors would not facilitate, but rather obscure an integration of structura1 and functional data. Consequently, it seems at this moment most useful to base a first approximation of tectal circuitry exclusively on the number of synaptic contacts, and to postpone the incorporation of additional factors unti1 more structural and physiological data have become available. A large number of additional refinements of the framework may be mentioned. TO arrive at a more precise description of tectal circuitry, not only the 4 main types of tectal input, but each type of afferent should be considered separately; equally not only average characteristics of tectal neurons should be considered, but also variations and deviations. Further, more data should be obtained with respect to the axonal arborization pattern of severa1 interneurons, the synaptic properties of severa1 ce11 types, topographical variations, etc. Considering the tota1 set of refinements as well as reinforcements enumerated, it may be concluded that the framework constructed represents the most simple concept of tectal circuitry possible at present, since it considers only average structura1 characteristics and the most simple quantitative
laminar specificity concept, whereas it neglects possible variations, diviations, complications and specializations.
It is, consequently,
not a fina1 result,
starting point for further research. A definite filling in of the framework
but a
has to be
achieved by electrophysiological studies. Morphologica1 research, however, precise it may be, only demarcates
the potentialities
of circuitry.
tent and in which way these potentialities under
different
conditions
TO what exare utilized
may only be understood
by physiological research. In the next sections it will be explored to which degree such an integration of physiological
and structural
present for the teleostean
data may be achieved
at
tectum.
4. SURVEY OF PHYSIOLOGICAL
DATA
In order to facilitate comparison of the circuitry framework presented and tectal physiology, in the present section the relevant physiological data are briefly surveyed. This survey is predominantly devoted to single unit studies, with special attention to the localization and identification of the units recorded. An extensive list of physiological studies is presented in Table 1. 4.1. Tora1 inputprocessing Some electrophysiological aspects of the processing of toral input in the tectum have been investigated by Vanegas et al.264 in Eugerres and Holocentrus by means of electrical stimulation of the margina1 tectal axons and subsequent extracellular recording of the electrical events throughout the depth of the tectum. The results can be easily interpreted on the basis of the morphology of type 1 or pyramidal neurons, which are the only targets of margina1 axons31.103.106.131,149.150. According to Vanegas et al.264 the most important electrical events after stimulation of the margina1 fibers are: (1) spike propagation along these fibers with a conduction velocity of 0.20 or 0.16 m/s; (2) monosynaptic depolarization of the apical dendrites of type 1 or pyramidal neurons; (3) an attive current sink at the leve1 where the apical dendrites of type 1 neurons converge to the dendritic shaft; and (4) an activation of the axon terminals of type 1 neurons in layer 314. It is remarkable that this tectal afferent system, which receives its principal in-
280 put from the cerebellum,
has many
group terminates
physiological
more superficially
than the more
characteristics strongly reminiscent of that part of the brain, particularly of the parallel fiber-Purkinje ce11
slowly conducting group. Histological verification of the recording site showed that their regions of termi-
system*@. Sajovic
nation roughly correspond respectively*W62. Current
and LevinthaPos
showed
that in
the zebrafish severa1 periventricular or type XIV neurons also respond to electrical stimulation of the torus longitudinalis.
These responses
may interact
in
various ways with responses elicited by electrical stimulation of the optic nerve (see section 4.2.3). The functional significante of the toral afferents to the tectum is obscure, since no further electrophysiologica1 data are available.
However,
lations on the basis of comparative
some specuanatomica1
and
behavioral data have been made. The presente of a valvula cerebelli, projecting to a torus longitudinalis which projects, in its turn, to type 1 tectal neurons via a peculiar margina1 layer, is unique for actinopterygians. The valvula cerebelli seems to some extent linked with the lateral line system, which may be mechanoreceptive as well as electroreceptive in teleosts. Both mechanoreceptorsss and electroreceptor.9 may have topographically organized projections to the valvula cerebelli. Conceivably, the valvular-toral-tectal system might allow for correlation of the visually perceived environment and the environment as perceived by means of the lateral line system. Another, related function ascribed to the torus longitudinalis is opto-static correlations,lo4. Both functions are especially important for maintaining posture in watert*O. It is noteworthy in this context that the torus longitudinalis and the stratum marginale of the tectum reach their highest degree of development in fishes that actively move, either from shallow to deep water or in turbulent water. In contrast, these structures are only poorly developed in epipelagic or bottom-dwelling fishesm). 4.2. Visual inputprocessing 4.2.1.
Responses after electrical stimulation of the op-
tic nerve
Electrical stimulation of the optic nerve has revealed that two retina1 fiber populations with different conduction velocities terminate in the SFGS. This has been demonstrated for Eugerres plumierPJ6*, goldfish*isJs* and carpl46. A laminar profile analysis of postsynaptic potentials occurring after electrical stimulation of the optic nerve showed that the fastest
to layer 5 and layer 415, theories indicate that the
electrical potentials which can be recorded extracellularly in a laminated strutture after massive electrical stimulation of a horizontally entering fiber system, exclusively represent the activity of long, vertically oriented dendrites or dendritic shafts7iJW19. The activity of horizontally are abundant
oriented
dendrites,
which
in layer 415 and 5, is not represented
in
these potentials. Consequently, especially type 1, X11 and XIV neurons have been considered to be responsible for the postsynaptic phenomena recordedzisJs7. Al1 3 of these types of neurons indeed have been shown to make contacts with optic nerve fibersl49~lso. Type 1 neurons are most probably contacted by the slow conducting fibers in layer 415, as could be concluded from the depth of recordings of postsynaptic action potential@ or the distribution of electrical sources and sinks through the tectal layerW. Type X11 and type XIV neurons may be contacted by both ‘slow’ and ‘fast’ conducting retina1 fibers. A tentative scheme correlating the electrical events recorded with the morphology of type X11 and/ or type XIV neurons has been proposed by Vanegas*s4. The retina1 fibers that terminate in layer 2 have a slower conduction velocity than both populations of fibers terminating in layer 5 and 4/5219. The results of Schmidt*lg did not allow for conclusions about ce11 types that are postsynaptic to this third population of retina1 efferents. Recently, Matsumoto et al.147 succeeded in intracellular recording of tectal neurons after electrical optic nerve stimulation, using in vitro preparations of the carp tectum. They could distinguish severa1 response types. and found that monosynaptically activated neurons exclusively occur in SFGS and SGC (layers 5, 4 and 3), whereas bisynaptically driven neurons occur in SFGS, SGC as well as SAC (layers 5-2). 4.2.2. Visual responses of retina1 fiber terminals A number of papers deal with responses of single tectal units after visual stimulation of the contralateral eye. For a correct interpretation of the results obtained it is necessary to know whether the responses
281 271). However,
these types of responses
represent the activity of retina1 fiber terminals or the activity of intrinsic tectal neurons. A definite elucida-
do not show any specific stratification
tion was recently
one type
achieved
by Rowezoz and Niida et
al.172 by means of intracellular
recording
and subse-
quent dye injection. Most investigations, however, used extracellular recording, for which more indirect ways of discrimination have to be applied. Reliable cellularly
criteria to distinguish recorded
between
the extra-
activity of retina1 fiber terminals
and tectal neurons were established by Sutterlin and Prosserz49 and O’Benari76, using electrical stimulation of the optic nerve and subsequent measurement of the latency of the spike response. Units firing after a latency period smaller than 2 ms are in general retinal fibers, whereas tectal neurons mostly fire after a latency of 3 to IO msl72,176.199.205.249.257.262, In addi_ tion, the spike responses of tectal neurons and retina1 fibers upon electrical stimulation of the optic nerve differ with respect to (1) the number of spikes elicited, (2) habituation, (3) maximal frequency of firing and (4) the shape, amplitude and time course of the action potentials. In particular the last aspect was used by Guthrie and Bank@-92 for identifying the responses of intrinsic tectal units. Galand and Liège73 used the depth of recording as a criterion. Units in layers 3 and 4 were considered as tectal neurons, since no retina1 fibers occur in this layer. However, units in layer 5 may be both retina1 fibers and tectal when no further criteria are availneurons, able73.1~,2is~*16. Jacobson and Gazetis, Cronly-Dillon42, Zenkin and Pigarevzso, Niida and Sato173.174, Ramstad and Hughesi94, Warzok and Mark@, Waterman and Hashimoto2” and Waterman and Aoki270 al1 made recordings of tectal units without identifying these units. However, judging from the location of the recording site in the SFGS and the use of meta1 electrodes, their results most likely represent optic fiber responses. Meta1 electrodes appear to be very selective in recording the activity of retina1 fiber activityi76.249 whereas micropipettes, filled with a salinesolution, may record the activity of both fiber terminals and neurons, with preference for the latteri76.249. Retina1 fibers that terminate in the tectum show a number of different types of responses after visual stimulation of the contralateral eye (e.g. sustained as well as transient on, off and on-off responses; movement and direction selectivity; E-vector sensitivity; refs. 42, 73, 115, 174, 176, 194, 249, 269, 270,
of stratification
pattern
in general
pattern.
Only
has been
men-
tioned, viz. by Jacobson and Gazeiis, who noticed that in layer 415 of the goldfish tectum only sustained responses
occur. This was confirmed
by Cronly-Dil-
lo@, Warzok and Marks*@ and O’Benari76, and was also reported for the zebrafishzos, but not for carpi74,is4. It is obscure whether these sustained responses may be ascribed to the slowly conducting population
of fibers which also occurs in layer 4/5*19.
There are presently no data about the functional significance of the retina1 fibers which terminate in layers 314 and 2. 4.2.3. Visual responses of tectal neurons Extracellular recordings of tectal units allow for a distinction of 3 populations of visual tectal neurons. One population is located in layer 5 and 415, the SFGS, a second one in layer 4 and 3 and a third one in layer 1. Sutterlin and Prosser249 and O’Benari76 found in the SFGS a particular population of neurons showing spontaneous firing in the dark, inhibited by light as well as by electrical stimulation of the optic nerve (type 1 of Sutterlin and Prosserz49 and the simple non-habituating cells of O’Benari76). The tectal neurons recorded by Schellart et al.215 also occur in the SFGS, but these showed partly different characteristics. The neuronal population described by Guthrie and Banksso~si.s* was not localized in any specific layer, but includes neurons in the SFGS as well. Apart from tectal neurons, terminals from the nucleus pretectalis, area pretectalis and nucleus isthmi which terminate in the SFGS might also be responsible for the responses observed. Their visual responses would at least have long latencies and other characteristics related to transsynaptic stimulation. Neuronal responses in layers 4 and 3 (the SGC) and layer 2 (the SAC) distinguish themselves by a number of peculiar characteristics. These may include the occurrence of rhythmic spontaneous activity90.249, habituation (newness-neurons)73.9*+176; large receptive fields and binocularity73,90 and a rather large ‘plasticity’ in responsei76. In addition, multimodality is encountered in the SGC and SAC (see below). There are no indications regarding specific ce11 types which would be responsible for these responses. Guthrie and Banks92 distinguished 8 types of re-
282 sponses,
based on specific visual stimulation
condi-
spike recordings
in layer 1 is unclear.
In the frog, the
tions. These could be recorded from layer 1 up to layer 5, with a slight preference for layer 4/5, 314 and 1.
same problem is encountered. In this animal, Gruberg and Lettvinss showed that the ce11bodies of peri-
This might be correlated with the larger density of ce11 bodies in these layers, but does not allow for
ventricular neurons revealed no or very erratic electrical activity. However, in the nucleus isthmi, a celi
identification
mass getting
of specific ce11 types.
might even suggest that the response
In contrast,
it
types distin-
guished are randomly distributed over the different morphologically distinguishable ce11types. Electrical responses tivity of periventricular
in layer 1, representing the acneurons, have been recorded
in the goldfish by O’Benarl76 and in the zebrafish by Sajovic and Levinthal~“s.2”6. The recordings of O’Benari76 revealed multi-unit burst-like activity of simultaneous firing neurons suggesting electric coupling. This might be correlated with the gap-like junctions between these cells (section 2.2.2). In most recordings, the activity could be changed by visual stimuh, which is in keeping with the occurrence of synapses with retinai fibers on the dendrites of these neuronst4sJso. According to O’Bena9, visual stimulation elicits a large variety of response-types in layer 1. which are sometimes rather irreproducible or ‘piasti?. Sajovic and Levinthalzos classified units in layer 1 of the zebrafish tectum on the basis of their responses on a fhckering spot. Most of them could be classified as type 1 (silent in the dark; phasic response at ON and OFF), type T (tonically firing in the dark; phasic response at ON and OFF), type S (silent in the dark; tonic response at ON) or type B (spontaneously firing in bursts). These 4 types also show characteristic responses to other visual stimmi, as e.g. moving spots, spots of different size, bars of varying orientation and surround stimulation~~~. Aithough most of these units were encountered in layer 1. thus representing type XIV neurons, severa1 were observed in more superficial layers as wellz~s. According to Sajovic and LevinthaW. these superficial recordings should be ascribed to dendrites or axons of the periventricular neurons, since they are physiologically indistinguishable from recordings in layer 1. Guthrie investigat~ng tectal neurons in the and Bank+, perch, also included SPV cells in their results, and equally could not distinguish the activity of SPV neurons from that of other tectal neurons. Because the axon hillock of the periventricular or type XIV neurons is situated far away from the cell body. viz. in layer 415, the functional significante of
its input
in the frog exclusively
from
periventricular tectal ceIWs7, good and well-defined responses could be recorded. Gruberg and Lettvir@ conclude that the somata of periventricular cells have no essential function in the electrical activity of these neurons. A similar situation present in teleosts. Also in teleosts,
might well be SPV- or type
XIV neurons are the most important afferent elements for the nucleus isthmiliz and in the nucleus isthmi well defined electrical activity can be recorded after stimulation of the tectum27s. SO, severa1 types of responses recorded in layer 1 might represent only residua1 electrical activity coming from the more superficially located axon hillock, rather than the full electrical activity of these neurons. The intracelluiar recordings of Rowezoz in Ambloplites rupestris revealed a type of visual tectal neuron with a cell body in the boundary region between layer 7 and 6 and dendrites in layer 5 or below. These neurons might well correspond to type 111neurons in the goldfish. since these neurons have some more deeply located branches in teleosts with a highly developed visual system, to which Ambloplites belong@. Type 111 neurons indeed receive monosynaptic retina1 [email protected]” and represent a visual type of tectal interneuron (see Fig. 16). The neurons identified by Rowe*@ showed a quite characteristic type of response, (on-off burst cells), but were not selettive for specific stimulus conditions. The intracellular recordings and subsequent dye injections of Niida et al. 172in Carassius carassius, a species closely related to Carassius auratus, identified visual neurons in layer 1 (type XIV), in layer 314 (which might be type 1X or type X neurons), in layer 4i5 (which might be type IV or type VI1 neurons) and in layer 5 (type 1 neurons), as is in accordante with previous extracellular recordings. By far most recordings were obtained from type I neurons, which is probabiy caused by the large frequency of occurrence of these neuronsis? and by their good endurance to electrode penetration, due to their large dimensions in the direction of electrode penetration. Type 1 neurons showed a number of different types of
283 responses,
corresponding
to the responses
recorded
extracellularly in layer 59OJ76JisJ49. The most remarkable result of Niida et al.172 is the complete absente of any correlation between the type of response recorded and the ce11 type identified. Type 1
from the contralateral tectum, the torus semicircularis and the reticular formation have been demonstrated. There are no physiological indications about the tectal ce11types which may be responsible multimodal
for the
responses.
Only a single recent paper fully deals with multi-
neurons showed a number of different types of responses, whereas other types of neurons showed the
modality
same type of response as some type 1 neurons. Recently, Sajovic and Levinthapas have investi-
tiani*. This author studied tectal single unit responses in Apteronotus albifrons, a weakly electric fish in
gated some interactions
which the torus semicircularis
between
visual and toral in-
put processing in the tectum of the zebrafish. applying simultaneous electrical stimulation
When of the
optic nerve and the torus longitudinalis, a substantial number of tectal neurons shows severa1 kinds of synergistic as well as antagonistic effects. These effects were recorded in layer 1 as well as more superficially and did not show any correlation with the type of visual response recorded nor with the laminar position of the recording site*os. Consequently, it is unknown which of the intratectal pathways present (Fig. 9) are involved in the different types of visuo-toral interactions recorded. 4.3. Deep tectal inputprocessing-multimodality With respect to non-visual responses in the tectum of teleosts, most reports are rather fragmentary. Sutterlin and Prosser*@ and Guthrie and Bank@ have reported spontaneously firing neurons in deep tectal layers that do not respond to visual stimulation. Galand and Liège73 described 3 types of multimodal units for deep tectal layers: visuotactile units; visuolateral line units and visuo-acoustic units. Visuotactile units in deep tectal layers have also been described by O’Benari76. Visuo-lateral line responses and visuo-acoustic units have also been described by Callens et al.25 and Niidai71, respectively, however, without referente to a particular tectal layer. Guthrie and Bank@ recorded the activity of deep tectal neurons during electrical stimulation of the fasciculus longitudinalis lateralis in the rhombencephalon. This type of stimulation could have both excitatory and inhibitory effects on deep tectal neurons. Fish and Voneida reported somatosensory responses, predominantly recorded in layer 1. SO, severa1 types of multimoda1 responses have been demonstrated in the tecturn, and these predominantly or perhaps even exclusively occur in deep tectal layers, where afferents
in the teleostean
ry information
tectum,
viz. that of Bas-
provides
electrosenso-
to the deep tectal layersn.
Bastiarri
describes that the visuo-topic and elettro-topic tectal maps are in spatial register, and that visual and electrosensory stimuli exert strongly interactive influences on many tectal neurons, most of which are located in layers 2 or 3. It should be mentioned that multimodality has frequently been demonstrated in the tectum of other vertebrates, including the salamander Ambystomas6, the lizard Zguana243, the 0~1122, the mouse46.47, the golden hamster*s, the rabbitsi and the cat77J44. In al1 these animals superficial tectal layers are exclusively involved in visual information processing, whereas deep tectal layers contain auditory, somatosensory and/or multimodal units as well. The visuotopic, acusticotopic, and somatotopic maps constituted by these units appear to be in spatial register with each other29.47,86.122.243,244
TO my knowledge, there are no data available concerning the electrophysiological properties of telencephalic afferents to the tectum. 4.4. Tectal efferents Apart from the studies on possible retinopetal tectal efferents, discussed in section 2.3.1, only two electrophysiological studies dea1 with other tectal efferents. Mark and Davidsoni41 recorded single unit activity in the intertectal commissure of Astronotus ocellatus. These units showed rhythmic spontaneous activity in the dark, which was mostly inhibited by increasing levels of background illumination, but could not be changed by patterned visual input, such as light or dark objects or moving stimuli. Wilhams and Vanega+ recorded electrical activity in the nucleus isthmi, nucleus rotundus, nucleus dorsolateralis tegmenti and corpus glomerulosum after electrical stimulation of the tectum in Eugerres and Holocentrus.
284
Their results confirm the anatomica1 demonstrations of tectal projections to the nucleus isthmi, nucleus ro-
might be well possible that visual input would appear
tundus
that according to Ebbessonjo the type 1 neurons of the visually well developed teleost Holocentrus re-
and nucleus
of the dorsolateral
tegmentum,
whereas the possible projection to the corpus glomerulosum is new. Neurons in the nucleus isthmi showed a characteristic burst of spikes after tectal stimulation. The responses in the nucleus rotundus (or nucleus prethalamicus)
showed two distinct excit-
atory components. Electrical stimulation
of the tectum of teleosts elic-
its severa1 types of movernents5.28,3”,44,‘59.
conjugate eye The direction
and of
body these
movements depends on the tectal site which is stimulated, suggesting a kind of motor-map within the tecturn5,‘59. These behavioral responses should be effectuated via tectal efferents. Eye movements elicited by tectal stimulation may be mediated by the nucleus pretectalis, which receives bilatera1 tectal input (see Fig. 3) and projects to the oculomotor nuclei63. Body movements may be mediated by the reticular formation, which is an important target of tectal efferents and projects to the spinai cord. The nucleus pretectalis, area pretectalis and the nucleus isthmi may be involved as well, since these tectal targets project to the cerebellum63J4.137. 5. COMPARISON LOGICAL
OF
STRUCTURAL
AND
PHYSIO-
DATA
Out of the physiological results surveyed, only few aspects can be correlated with the conceptual framework of tectal circuitry presented in section 3. The first aspect concerns the functional properties of type 1 neurons as reported by Vanegas et al.264 and Niida et al.172. Their large involvement in toral input processing264 is in good agreement with tectal circuitry. However, their pronounced responses upon visual stimulationl72 are at first sight somewhat surprising, because they have only few contacts with retina1 fibers. On the one hand this might indicate that the position of the retina1 terminals close to the axon hillock of type 1 neurons indeed increases the efficacy of their synaptic contacts substantially. On the other hand, purely visual stimuli are rather unphysiological, and the experiments of Niida et al.172 do not indicate the balance between toral and visual stimulation. When both toral and visual input would be provided to type 1 neurons in a physiological ratio, it
to be of relatively
low importance.
It is noteworthy
ceive no retina1 input at all, which would be a remarkable species differente with goldfish149 and Eugerresl31. However, the statement of Ebbessons” can only be evaluated after publication of more experimental detail.
A second aspect to be discussed is the lack of correlation between the type of response recorded and the ce11type identified, as reported by Niida et al. 172and also indicated by the results of Guthrie and Bank@. When neurons with a similar morphology and synaptology indeed would appear to subserve completely different functions, elucidation of functional anatomy becomes without prospect. However, it seems presently more plausible to postulate that the criteria used for electrophysiological characterization (on andlor off responses; transient andlor sustained responses) were not the most relevant ones for the neurons studied, and that the use of other visual as well as multimodal stimuli might well uncover common functional aspects of distinct ce11 types. The tectum mesencephali of teleosts probably is no analyzer of on-off or transient-sustained responses, but primarily of other aspects of visual as well as non-visual information. Apart from the aspects discussed above, comparison of structural and physiological data concerning the teleostean tectum reveals in general a great cleft between both types of data. This cleft is on the one hand caused by factors specific for tectal research, on the other hand also by more general neurobiological obscurities. In addition to the gaps in our anatomica1 knowledge, discussed in section 3.4, two main specific problems may be mentioned. At first, the physiologically investigated units have only rarely been identified morphologically, which greatly hampers integration of morphology and physiology. However, recent intracellular tectal recordings7”,‘47,172.~“~ indicate that in this respect substantial improvement may be expected in the near future. Secondly, by far most physiological studies on the teleostean tectum exclusively investigated visual responses of tectal neurons, whereas the important multimodal integrative capacity of these elements, as suggested by tectal cytoarchitecture and demonstrated in severa1 other
285 vertebrate classes, has escaped physiological attention. However, Bastiarri has recently studied multimoda1 (electrosensory and visual) integrative aspects more systematically, and his experimental design seems promising to obtain in the future a more complete pitture
of multimodal
information
processing
in
the teleostean tectum. In addition to the specific tectal problems mentioned, severa1 general neurobiological uncertainties prevent
integration
of structural
and functional
data.
tectal connectivity electrophysiological
in the goldfish is proposed, data conceming
(3) the
the teleostean
tectum are surveyed and (4) the degree of correlation between the structural and physiological data available is discussed. Apart from the retina, from at least 10 other these projections
tectal afferents
brain centers.
originate
At least 5 of
appear to be topographically
nized. Tectal afferents, neurons reveal a characteristic intratectal
orga-
as well as synapses lamination pattern.
Essentially, neuroanatomical research leads to a description of the synaptic connections of neurons (see
Tectal efferents
section 3), whereas neurophysiological research leads to a description of the electrical (spike) responses of neurons for various stimuli under various conditions. SO, integration of anatomy and physiology (functional anatomy) implies determination of the relations between synaptology and spike-responses. In this respect, a number of uncertainties exist. For example, what is the basic differente between neurons receiving few synaptic contacts (e.g. type XIV, receiving f 200 contacts) and neurons receiving many synaptic contacts (e.g. type XIII with + 5000 contacts)? How is the relation between the number of synaptic contacts activated and the frequency of the spike response? How many synapses should be excited to drive a neuron into saturation? When do synaptic contacts (excitatory or inhibitory) integrate linearly or non-linearly. What is the relation between the size or topographic position of a synaptic contact and its effect on the axonal spike responses? etc. etc. Al1 these aspects probably depend on general neurobiologica1 rules with respect to the integrative properties of the neuronal surface, but these are at present to a large extent unknown. Only when more knowledge of these basica1 neurobiological processes becomes available, a more detailed insight in the functional anatomy and circuitry of brain centers, including the teleostean tectum, comes into prospect.
types. The structural data surveyed allow the construction of a conceptual framework of tectal circuitry on the basis of 3 starting points. (1) The existence of at least 8 presynaptic zones or laminae, each containing a characteristic set of presynaptic structures (afferents and axons of interneurons). (2) The fact that the tectal postsynaptic structures (somata and dendrites of tectal neurons) each have a characteristic location, extension and synaptic density, which determines the relative importance of the different presynaptic zones for each ce11 type. (3) The laminar specificity hypothesis, which implies that presynaptic structures that coexist in a particular presynaptic zone terminate without preference on al1 types of postsynaptic structures within that zone. The conceptual framework of tectal circuitry is quantified in terms of connectivity index and connective importance. Analysis of the framework constructed Ieads to a detailed description of the intratectal pathways in-
6. SUMMARY AND CONCLUSION
The present paper is aimed at an exploration of the possible functional significante of the laminar organization of the goldfish tectum at both the cellular and the synaptic level. For this purpose (1) the data concerning the strutture of the teleostean tectum are surveyed, (2) a conceptual framework of the intra-
project
to at least 10 brain centers,
and have unti1 now been shown to arise from 6 ce11
volved in the processing of the 4 main streams of tectal input (i.e. visual, toral, telencephalic and ‘deep’ input). It was concluded that the laminar organization of the tectum is primarily relevant for multimodal integration and that the tectal ce11 types each receive a characteristic sample out of the multimodal information available in the different tectal layers. The physiological data available do not yet allow testing of the tentative conclusion formulated for two main reasons: (1) the tectal units which have been electrophysiologically investigated have only rarely been identified morphologically; and (2) by far most physiological studies exclusively used visual stimulation or electrical stimulation of the optic nerve, whereas other modalities or tectal afferents have
286 only incidentally The combined
received physiological topographical
zation of the teleostean
attention.
and laminar
from selected
organi-
tectum is in particular
suita-
ble for the localization and selection of objects in the environment on the basis of integrated multimodal information
(including
visual, acoustical,
and tattile information)
lateral line
and the subsequent
tion of the eyes, head andlor
body toward
orienta-
objects.
appears to be constant tebratesun. However, mechanisms
This general
throughout al1 classes of verthe underlying intratectal
are far from understood.
the present paper provides framework which facilitates these mechanisms
tectal function
It is hoped that
a functional anatomica1 a further elucidation of
in the tectum of teleosts.
or away
7. APPENDIX The connectivity indexes and connettive importances presented in Table 111and Figs. 11-16 have been calculated as follows. (Starting points, definitions and main outlines have been given in sections 3.1 and 3.2). Firstly, 8 presynaptic zones are distinguished. These are (see also section 3.1.2. and Fig. 8): Layer 7
zone a (za)
Layer 6
zone b (zb)
Layer 516and 5
zone c (zc)
Layer 415
zone d (zd)
Layer 4
zone e (ze)
Layer 314
zone f (zf)
Layer 3
zone g (zg) zone h (zh).
Layer 213and 2
Secondly, the connettive relevance of the different presynaptic zones for the ce11types distinguished is estimated either on the basis of the number of synaptic contacts as presented by Meek 150(see Fig. 8) or on the basis of the dendritic extensions as presented by Meek and Schellartis* (see Fig. 5). This yields the following formulae:
Tw 1
Judging from the numbers of synaptic contacts in the different presynaptic zones, the relevance of za:zb:zc:zd:ze:zf 1900:10:40:120:20:20, from which the following connectivity index (y) can be formulated: y(I) = 0.90za + 0.01 zb + 0.02 zc + 0.06zd + 0.01 ze + 0.01 zf.
Type 111
Ga)
This cell type confines its dendrites to layer 415. Consequently y(IV) = l.OOzd.
Type V
(la)
Judging from the numbers of synapses, zb:zc = 60:390 or ~(111)= 0.13zb + 0.87~~.
Type IV
=
(3a)
The neurons which are confined to layer 4 (type V,) give y( V,) = 1.00 ze
(4a)
The neurons which are confined to layer 3 (type V,) give y(V,) = l.OOzg. Type VI1
Judging from the dendritic extensions, zc:zd = 1:4, or y(VI1) = 0.20~~ + 0.80zd.
Type VI11
(6a)
Judging from the dendritic extensions, zd:ze:zf = 2:1:1, or y(VII1) = 0.50zd + 0.25 ze + 0.25 zf.
Type 1X
(sa)
(7a)
Judging from the dendritic extensions, zd:ze:zf = 2:1:2, or 7(1X) = 0.40zd + 0.20ze + 0.40zf.
(Sa)
287 Judging from the numbers of synapses, zc:zd:ze:zf:zg:zh
Type XIV
= 90:40:30:15:10:15, or
Y(XIV) = 0.45~~ + 0.20zd + 0.15ze + 0.08zf + O.OSzg + 0.08zh.
(9a)
Judging from the numbers of synapses, zb:zc:zd:ze = 2:2:1:5, or
Type VI
Y(V1) = 0.2 zb + 0.2~~ + 0.1 zd + 0.5 ze.
(IOa)
Judging from the dendritic extensions, zd:ze:zf = 2:1:2, or
Type X
Y(X) = 0.40zd + 0.20ze + 0.40zf.
(lla)
Judging from the numbers of synapses, zc:zd:ze:zf:zg:zh
Type X11
= 2:1:5:1:2:6, or
Y(XI1) = 0.12~~ + 0.06zd + 0.29ze + 0.06zf + 0.12zg + 0.35zh. Judging from the numbers of synapses, zc:zd:ze:zf:zg:zh
Type X111
Y(XIII)=0.08zc+0.08zd+0.08ze+0.08zf
(l2a)
= 1:1:1:1:3:5, or
+0.25zg+0.42zh.
(l3a)
Thirdly, the contributions of different presynaptic structures in each presynaptic zone are estimated on basis of the ‘quantitative laminar specificity hypothesis’ formulated in section 3.1.4.3. and the considerations regarding type XIV neurons made in section 3.1.4.4. This leads to different formulae for both alternatives to be considered, which now will be dealt with separately. 7.1. Alternative 1 As pointed out in section 3.1.4.4, this alternative implies that type XIV axons are assumed to make exclusively synaptic contacts with type XIV dendrites, and not with other cell types. Other axons are presumed to follow the rules of the ‘quantitative laminar specific hypothesis’ formulated in section 3.1.4.3. This yields the following formulae with respect to the presynaptic zones (cf. Fig. 8): za =
l.OOtor
(l4a)
zb =
l.OOvis
(l5a)
zc = 0.33vis + 0.33 (111)+ 0.33 (VII)
(l6a)
zd = 0.33 vis + 0.33 (IV) + 0.33 (VIII)
(l7a)
ze = 0.5O(V,) +0.50(1X)
(l8a)
zf = 0.50tel+O.50(1)
(l9a)
zg = 0.33 tel+ 0.33deep + 0.33 (V,) zh = l.OOdeep
(20a) (2la)
Substitution of formulae 14a-21a in formulae la-13a yields the connectivity index (Y) of each cell type in this first alternative: Y(I)
= 0.03 vis + 0.90 tor + 0.005 te1 + 0.005 (1) + 0.007 (111)+ o.02 (IV) + 0.005 (V,) + 0.007 (VII) + 0.02 (VIII) + 0.005 (1X)
(lb)
Y(III)
= 0.42vis + 0.29 (111)+ 0.29 (VII)
(2b)
YUV)
= 0.33 vis + 0.33 (IV) + 0.33 (VIII)
(3b)
Y(V,)
= 0.5O(V,) + 0.50 (1X)
(4b)
Y(V,)
= 0.33 tel+ 0.33 deep + 0.33 (V,)
(5b)
Y(VII)
= 0.33 vis + 0.07 (111)+ 0.27 (IV) + 0.07 (VII) + 0.27 (VIII)
Y(VII1) = 0.17vis+O.13 tel+O.13(1) Y(IX)
+ O.l7(IV) +O.l3(V,)
+O.l7(VIII)
(6b) +0.13(1X)
= 0.13vis + 0.20 tel+ 0.20(I) + O.l3(IV) + O.lO(V,) + O.l3(VIII) + 0.10(1X)
Y(XIV) =
(1 -a) (XIV) + a {0.22 vis + 0.05 tel + 0.09 deep + 0.04 (1) + 0.15 (111) + 0.07 (IV) + 0.08 (V,) + 0.02 (V,) + 0.15 (VII) + 0.07 (VIII) + 0.08 (1X)}
(7b) (8b) (9b)
Y(VI)
= 0.3Ovis + 0.07 (111)+ 0.03 (IV) + 0.25 (V,) + 0.07 (VII) + 0.03 (VIII) + 0.25 (1X)
(lOb)
Y(X)
= 0.13vis+0.20tel+0.20(1)+0.13(1V)+0.10(V,)+0.13(V111)+0.10(1X)
(llb)
Y(XII)
= 0.06 vis + 0.07 tel + 0.39 deep + 0.03 (1) + 0.04 (111) + 0.02 (IV) + 0.15 (V,) + 0.04 (V,) + 0.04 (VII) + 0.02 (VIII) + 0.15 (1X)
(l2b)
y(XII1)
= 0.06 vis + 0.13 tel + 0.50 deep + 0.04 (1) + 0.03 (111) + 0.03 (IV) + 0.04 (V,) + 0.08 (V,) + 0.03 (VII) + 0.03 (VIII) + 0.04 (1X).
(l3b)
288 When each presynaptic strutture in the formulae lb-8b is replaced by its connectivity index formula (eg. (1) by y (1); (111)by y (111) etc.), these formulae constitute 8 equations with 8 unknowns, which can be solved in terms of afferent input (see section 3.2.2.). This yields the following connettive importance formulae (A) for alternative 1:
r(I)
= 0.07VIS + 0.92TOR + 0.02TEL
(IC)
T(III)
= 0.91 VIS + 0.04 TOR + 0.05 TEL
PC)
UIV)
= 0.74VIS+O.12TOR+O.l4TEL
(3c)
UV,)
= 0.39VIS + 0.29TOR + 0.32TEL
(4c)
I(V,) I(VII)
= 0.5OTEL + O.SODEEP
(5c)
= 0.77 VIS + 0.11 TOR + 0.12TEL
(6c)
T(VII1) = 0.47 VIS + 0.25 TOR + 0.28 TEL
(7c)
= 0.39VIS + 0.29TOR + 0.32TEL.
(Sc)
I(IX)
Subsequently, formulae 9b-13b can be solved in terms of afferent input when in these formulae each presynaptic strutture is replaced by its connettive importance formula. This results in: r(xIv)
= 0.61 VIS + 0.13~0~
+ 0.17~~~ + O.~ODEEP
I(vI)
= 0.64VIS+O.17TOR+0.19TEL
(lOc)
I(X) l-(X11)
= 0.39VIS + 0.29TOR + 0.32TEL
(llc)
= 0.26VIS + 0.13 TOR + 0.20TEL + 0.41 DEEP
(l2c)
I-(X111) = 0.17 VIS + 0.08TOR + 0.21 TEL + 0.54 DEEP.
(l3c)
(9c)
At last, formulae 14a-21a can be solved in a similar way, which yields: za (layer 7)
=
I.OUTOR
zb (layer 6)
=
l.OOVIS
zc (layer 516and 5)
= 0.89VIS + 0.05 TOR + 0.06TEL
zd (layer 415)
= 0.74VIS+O.12TOR+O.l4TEL
ze (layer 4)
= 0.39VIS + 0.29TOR + 0.32TEL
zf (layer 314)
= 0.03 VIS + 0.46TOR + 0.51 TEL
zg (layer 3)
= 0.50TEL + O.SODEEP
zh (layer 213and 2)
=
l.OtJDEEP.
7.2. Alternative2 This alternative implies that the axons of type XIV neurons are presumed to constitute 50% of ali contacts in layer 516 and 5 (zc); 25% of ah contacts in layer 415 (zd); 75% of al1 contacts in layer 4 (ze); 33% of ah contacts in layer 314 (zf) and 50% of al1 contacts in layer 3 (zg). The few contacts of type XIV axons that might be present in layer 6 and layer 2 (zb and zh) are neglected. This distribution is based on the following considerations. The percentages enumerated result in an average percentage of about 50%, as is in agreement with the percentage of S5 terminals in the tectum of Holocentrus’“, which are probably constituted for the major part by type XIV axon terminals (see section 2.2.2). The axons of type XIV neurons have no specific preference to terminate in the narrow layers 415and 314, and are assumed to make in these layers the same percentage of contacts as the other types of presynaptic elements (in layer 415: visual afferents, axons of type IV neurons and axons of type VI11 neurons; in layer 3/4: telencephalic afferents and axons of type 1 neurons). Their contribution in the wider layers 5,4 and 3 is assumed to be larger. The ratio between 50% (layer 5); 75% (layer 4) and 50% (layer 3) roughly reflects the preference of type XIV to terminate in layer 4 (see Meek and Schellartt5* and Fig. 5), and is also in accordante with the distribution of S5 terminals in Holocentrus ‘06. SO, with respect to the number and laminar distribution of type XIV axon terminals, this second alternative represents the most probable estimation that can be made at present. However, with respect to their degree of cellular specificity (the first alternative assumes 100% cellular specificity and the second one 0%). the reahty is probably situated somewhere in between both alternatives, since both seem too extreme (section 3.1.4.4.). Just as in alternative 1, the remaining presynaptic structures are presumed to follow the rules of the ‘quantitative laminar specificity hypothesis’ formulated in section 3.1.4.3. With respect to the presynaptic zones, this yields the following formulae: za =
l.OOtor
(l4c)
zb =
l.OOvis
(l5c)
zc = 0.17 vis + 0.17 (111)+ 0.17 (VII) + 0.50 (XIV)
(16~)
289 zd =
0.25vis + 0.25(IV) + 0.25 (VIII) + 0.25 (XIV)
(l7c)
ze
=
0.13 (V,) + 0.13 (1X) + 0.75 (XIV)
(l8c)
zf
=
0.33 te1 + 0.33 (1) + 0.33 (XIV)
(19c)
zg
=
0.17tel+0.17deep+0.17(V,)+O.SO(XIV)
(2Oc)
l.OOdeep.
(2lc)
zh =
Substitution
of formulae
14c-21c
in formulae
la-13a
yields the connectivity
index (Y) of each ce11 type in this second
alternative:
= 0.02vis + 0.90tor + 0.003tel + 0.003(1) + 0.003(111) + 0.01 (IV) + 0.01 (V,) + 0.003 (VII) + 0.01 (VIII) + 0.001(1X)
+ 0.03 (XIV)
(14 C-4
Y(III)
=
0.28vis
+ 0.14 (111) + 0.14 (VII) + 0.43 (XIV)
Y(IV)
=
0.25 vis + 0.25 (IV) + 0.25 (VIII) + 0.25 (XIV)
(34
Y(V,)
=
0.13 (V,) + 0.13 (1X) + 0.75 (XIV)
Y(V,)
=
0.17te1+0.17deep+0.17(V,)+0.50(XIV)
(44 (54 (64 (74 (84
Y(VII)
=
0.23 vis + 0.03 (111) + 0.20 (IV) + 0.03 (VII) + 0.20 (VIII) + 0.30 (XIV)
y(VII1)
=
0.13vis
+ 0.08 tel+
0.08 (1) + 0.13 (IV) + 0.03 (V,) + 0.13 (VIII) + 0.03 (1X) + 0.4O(XIV)
Y(IX)
=
O.lOvis + O.l3tel+
y(XIV)
=
0.13 vis + 0.03 tel + 0.08 deep + 0.03 (1) + 0.08 (111) + 0.05 (IV) + 0.02 (V,) + 0.01 (V,) + 0.08 (VII) + 0.05 (VIII) + 0.02 (1X) + 0.44 (XIV)
0.13(I)
Y(VI)
=
0.26 vis + 0.03 (111) + 0.03 (IV) + 0.06 (V,) + 0.03 (VII) + 0.03 (VIII) + 0.06 (1X) + 0.50 (XIV)
Y(X)
=
O.lOvis + O.l3tel+
Y(XII)
=
0.03 vis + 0.04 te1 + 0.37 deep + 0.02 (1) + 0.02 (111) + 0.01 (IV) + 0.04 (V,) + 0.02 (V,) + 0.02 (VII) + 0.01 (VIII) + 0.04 (1X) + 0.37 (XIV)
(124
y(XII1)
=
0.03 vis + 0.07 te1 + 0.46 deep + 0.03 (1) + 0.01 (111) + 0.02 (IV) + 0.01 (V,) + 0.04 (V,) + 0.01 (VII) + 0.02 (VIII) + 0.01(1X) + 0.28 (XIV).
(134
0.13(I)
The connectivity index formulae which yields the following connettive
+ O.lO(IV)
+ O.lO(IV)
+ O.O3(V,) + O.lO(VIII)
+ O.O3(V,) + O.lO(VIII)
ld-13d can be solved importance formulae
in terms of afferent for alternative 2:
+0.03(1X)
+0.03(1X)
+ 0.38(XIV)
+ 0.38(XIV)
input in the same way as indicated
(94
(104 (114
for alternative
1,
VI)
=
0.06 VIS + 0.91 TOR + 0.01 TEL + 0.01 DEEP
(1c)
T(III)
=
0.73VIS
(2e)
I(IV)
=
0.70VIS+0.08TOR+0.10TEL+0.12DEEP
(3e)
UV,)
=
0.55VIS+0.10TOR+0.14TEL+0.21DEEP
(4e)
I-07,)
=
0.34VIS+0.05TOR+0.27TEL+0.33DEEP
(5e)
r(vII) = 0.70VIS + 0.08TOR + 0.10 TEL + 0.12 DEEP
(6c)
I(VIII)
=
0.54VIS
(7e)
I(IX)
=
0.48VIS+0.19TOR+0.22TEL+0.12DEEP
I(XIV)
=
0.57VIS
+ 0.09TOR
+ 0.12TEL
I(VI)
=
0.68VIS
+ 0.07TOR
+ O.lOTEL+
I(X)
=
0.48VIS
+0.19TOR+0.22TEL+O.l2DEEP
l-(X11)
=
0.34VIS
+ 0.07TOR
F(XII1)
=
0.26 VIS + 0.06TOR
Formulae
za (layer 7)
+ 0.06TOR
+ 0.15TOR
+ 0.08TEL
+ 0.18TEL
+ 0.11 TEL+
+ 0.13DEEP
+ 0.13DEEP
(8e) + 0.22DEEP
(9e)
O.lSDEEP
(1Oe) (llc)
0.48DEEP
+ 0.13 TEL + 0.54 DEEP.
(12e) (13e)
14c-21c can be solved in a similar way, which yields:
=
l.OOTOR
(14d)
290 zb (layer 6)
=
1.00v1s
zc (layer 5/6 and 5)
=
0.69VIS
zd (layer 415)
=
0.70VIS+0.08TOR+0.10TEL+0.12DEEP
ze (layer 4)
=
0.55VIS
zf
=
0.21 VIS + 0.33 TOR + 0.38 TEL + 0.08 DEEP
(l9d)
zg (layer 3)
=
0.34 VIS + 0.05 TOR + 0.27 TEL + 0.33 DEEP
(2Od)
zh (layer 213 and 2)
=
1.00 DEEP.
(2ld)
(layer 314)
(15d)
+ O.lOTOR+
O.l4TEL+
(l7d)
2’ DLT FRI FRm mes NDL NGL NI NP NR
( 184
0.21 DEEP
ABBREVIATIONS ADc
( 164
+ 0.07TOR+0.09TEL+O.l5DEEP
area dorsalis centralis area pretectalis diencephalon nucleus dorsalis lateralis tegmenti formati0 reticularis lateralis formatio reticularis medialis mesencephalon nucleus dorsolateralis thalami nucleus geniculatus lateralis nucleus isthmi nucleus pretectalis nucleus rotundus
ACKNOWLEDGEMENTS
1 am greatly indebted to Doctors R. Nieuwenhuys, J. J. Eggermont and G. Vrensen for their interest and valuable suggestions during preparation of the
NRMT NRS Ret rhomb SAC SFGS SGC SM SO SPV Tect tel TL TS
manuscript, and to Dr. N. A. M. Schellart for critica1 reading of the manuscript. 1 am grateful to Mr. J. Maas for the drawings and to Mrs. M. SankatsingSjak Shie and Miss A. Siebring for their skilful secretarial assistance.
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722-730.
247
Elsevier
Functional Anatomy of the Tectum Mesencephali of the Goldfish. An Explorative Analysis of the Functional Implications of the Laminar Structural Organization of the Tectum J. MEEK Department of Anatomy and Embryology,
University of Nijmegen, Faculty of Medicine, Geert Grooteplein Noord 21, Postbus 9101, 6500 HB Nijmegen (The Netherlands)
(Accepted August 8th, 1983) Key worak: tectum mesencephali -
goldfish - teleosts - laminar organization - functional anatomy - circuitry analysis connectivity matrix - multimodal integration
CONTENTS 1. Introduction
.............................................................................................................................................
248
2. Survey of the structural tectal organization ....................................................................................................... 2.1. Tectal afferents ................................................................................................................................... 2.1.1. Origin of tectal afferents ............................................................................................................... 2.1.2. Topographicorganizationof tectal afferents ...................................................................................... 2.1.3. Laminar organization of tectal afferents ............................................................................................ 2.1.4. Quantitative properties of tectal afferents ......................................................................................... 2.2. Intrinsic tectal strutture ........................................................................................................................ 2.2.1. Tectal neurons ........................................................................................................................... 2.2.2. Synaptic organization of the tectum ................................................................................................. 2.3. Tectal efferents ................................................................................................................................... 2.3.1. Tectal targets ............................................................................................................................. 2.3.2. Efferent tectal cell types ................................................................................................................
251 251 251 251 253 254 255 255 256 258 258 259
3. A conceptual framework of tectal circuitry ....................................................................................................... 3.1. Startineooints .................................................................................................................................... .............................................................................. 3.1.1. The lamination pattern of tectal neuronalelements 3.1 .l .l. Tectal afferents .............................................................................................................. 3.1.1.2. Tectal interneurons ......................................................................................................... 3.1.1.3. Efferent tectal neurons ..................................................................................................... 3.1.2. Presynaptic tectal zones ................................................................................................................ 3.1.3. Postsynaptic determinationof neuronal input ..................................................................................... 3.1.4. The hypothesisof laminar specificity ................................................................................................ 3.1.4.1, Generai considerations ..................................................................................................... 3.1.4.2. Laminar specificity in tectal circuitry .................................................................................... 3.1.4.3. Quantitative elaboration of laminar specificity in tectal circuitry ................................................. 3.1.4.4. Considerations regarding type XIV neurons .......................................................................... 3.2. Calculation of the connectivity index and the connettive importance ................................................................ 3.2.1. Connectivity index ...................................................................................................................... 3.2.2. Connettive importance ................................................................................................................ 3.3. Analysis of tectal circuitry ...................................................................................................................... 3.3.1. Tectal circuitry involved in toral input processing ................................................................................ 3.3.2. Tectal circuitry involved in visual input processing ............................................................................... 3.3.3. Tectal circuitry involved in telencephalic input processing ..................................................................... 3.3.4. Tectal circuitry involved in ‘deep’ tectal input processing ....................................................................... 3.35. The connettive importance of tectal afferents in the different tectal layers ................................................. 3.3.6. The connettive relations of the tectal ce11types ................................................................................... 3.4. Critica1 evaluation of the framework presented ...........................................................................................
260 260 261 261 262 263 263 263 264 264 264 265 266 266 267 261 268 268 270 272 274 275 276 27X
0165-0173/83/$03.00 0 1983 Elsevier Science Publishers B.V.
248 4. Survey of physiological data .......................................................................................................................... 4.1. Toral input processing .......................................................................................................................... 4.2. Visual input processing ......................................................................................................................... 4.2.1. Responses after electrical stimulation of the optic nerve ........................................................................ 4.2.2. Visual responses of retina1 fiber terminals ....... .................................................................................. 4.2.3. Visual responses of tectal neurons ................................................................................................... 4.3. Deep tectal input processing-multimodality .............................................................................................. 4.4. Tectal efferents ...................................................................................................................................
279 279 280 280 280 281 283 283
5. Comparison
284
6. Summary
of structural and Conclusion
and physiological
data
................................................................................................
.............................................................................................................................
7. Appendix .......................................................................... ..................................................................... 7.1. Alternative 1 ...................................................................................................................................... 7.2. Alternative 2 ., ,. _. ..... _, ..
_.
Acknowledgements Abbreviations
._.....
References
.... ___. ,.
.___
285 286 287 288 290
._.
290
_.
1. INTRODUCTION
The tectum mesencephali or optic tectum constitutes the most highly developed part of the brain of fish (Figs. 1 and 2). In most teleosts this strutture is differentiated into 7 layers which from deep to superficial are indicated as follows: layer 1 or stratum periventriculare (SPV); layer 2 or stratum centrale (SAC); layers 3 and 4, together named stratum griseum centrale (SGC), while layer 4 is also called the inner plexiform layer (IPL); layer 5 or stratum fibrosum et griseum superficiale (SFGS); layer 6 or straturn opticum (SO) and layer 7 or stratum marginale (SM). In goldfish, the thickness of the tectum is about 600pm. A second marked feature of the tectum is the precise topographic organization of the retinotectal projection. A large number of aspects concerning the structure and function of the teleostean tectum has been investigated in a variety of species (Table 1). Unti1 now. however, no attempt has been made to obtain an integrated concept from al1 these data. The main purpose of the present paper is to explore in which way and to which extent such a functional anatomica1 concept is possible at present, in particular with respect to the laminar organization. This exploration is primarily based on the goldfish, since for this species the most complete set of data is available (see Table 1). In addition, data on other teleosts will be used for comparison. The design of the present paper is as follows: at
290
first, the results available on the structural tectal organization will be reviewed briefly and summarized in a number of schemes. Secondly, tectal circuitry will be analyzed qualitatively and quantitatively on the basis of the structural data available and the concept of laminar specificity. The starting points and methodology of this analysis will be presented in substantia1 detail in order to enable extensive evaluation
c
MOuhw-~
Fig. 1. The brain of the goldfish. a, in situ: b, dorsal view; c, latera1 view. b.olf.. bulbus olfactorius; cereb., cerebellum; hypoth.. hypothalamus; med. spiri., medulla spinalis; rhomb.. rhombencephalon; telenc., telencephalon.
249
Fig. 2. Transverse sections through the tectum mesencephali of the goldfish. Top: the position of the tectum shown at low magnification (Lux01 fast blue-Cresyl fast violet staining). TL, torus longitudinalis; TS, torus semicircularis; ‘ITB, tractus tetto-bulbaris. Bottom: the tectal layers in a section stained with Hematoxilin-Eosin, SAC, stratum album centrale; SFGS, stratum fibrosum et griseum superficiale; SGC, stratum griseum centrale; SM, stratum marginale; SO, stratum opticum; SPV, stratum periventriculare. The numerical indication of these layers and their boundary regions ls*is presented at the right side.
of the specific tectal- as well as the more genera1 neurobiological-applicability of the analysis performed. Thirdly, the inferences of the structural circuitry analysis will be compared with physiological data in
order to explore to which extent the functional anatomy of the teleostean tectum is unravelled at present and in which way more definite insight may be obtained in the future.
TABLE 1 Literature dealing with tetta of teleosts Goldfish (Carassio
Connections Afferents Retino-tectal (topographical) Retino-tectal (laminar)
auratus) Other cyprinids’
Other teleo&*
115,116,154,156,230 79,130,167,168,219,231,240
135,230 184,197,198
2,83,84,177
107,108,109,137,144
Efferents Retina1 projections
83,84 63,201,231,240,241
137 184,197,198,201
Retinopetal fibers
163,219,240,253
163,184
Other afferents
Morphology Development Comparative gross morphology Golgi-studies Ultrastructure Optic nerve and tract Neurochemistry Chemoarchitectonics Neurotransmitters Acetylcholine
Glutamate GABA Monoamines RNA/Protein synthesis Electrophysiology E.E.G. Evoked potentials Visual stimulation Optic nerve stimulation Nou-retina1 afferent stimulation Saccade-related Multi-unit responses Retinotectal topography Single unit responses, extra cellular Visual units
4,12,13,22,127,229,230 7,49,51,57,59,89,130,132,136,157, 186,188,198,258,268 11,27,54,109,110,164,207,224,234. 259 27,54,111.112,207,214,224,234 7,24,26,49,51,53,57,59,63,89,157, 175,186,188,189,201,258,268, 52,76,157,158,162,163,208,253, 256
142,155
15,117,118,185,190,217,218 8***,119,120,222,232,235,242,277 13,17,40,41,120,133,186,192,193, 225,226,255.263 6,31,32,106.118,12S,131,132 56,223,250,251
133,148,152,200
103,133,192,193
3,149,150,166,246,248,267 16,48,95,145,165,204
31,103,144
129.140
272
272
35-37,39,66,68,69,70,72, 160,178,187,213,221,228, 266 67 187,267 38
160
34,35,39,160.266
126,196,233
180 195,196
1
183
60,93,247
1,101,124,189,199,211,212 125,219,249,252
183,189,227 146 265
10,93,124,247 18-21.23,125,161,257,260-262 264
96
115,116,154
22,127,229,230
42,75,90,91,113-115, 138,176,199,215,216,249, 269,270,271 25,64,90,176 70,202
90,146,171,173,174,194, 209,210
73,74,90,91,92,134,141,205,206. 254,257,261,262,280
171 147,172
12.64,73,205 202 275
Behavioral responses After tectal stimulation After tectal ablation
239,279
45,119
Plasticity and specificity
55,97,220$
Non-visual and multimodal units Single unit responses, intracellular Tectal targets
Including: the crucian carp (Carassiw IOX.IOY.133.137.146.194.1Y7.198.227.230.265;
Tinca
tinca
carassius)
5.29,30,43,44,61,159 14,45,119
IW.119.126.144.147~171.172.173.174.196.20.2ll~.233;
lM).183.184~lR9.198~272;
Alburnus
the
alburnusl84.198;
Barbus
carp
(Cyprinw
fluvia~il&lY2.l98;
~a~pio)3l,l~l3.~~~7, ,dus
~p,9~1.163.201;
Phoxinus s~.~“.l~8;Rutilis rutilti’~J97.‘98; and Scardinus erythrophthalmusl~J98.
Results obtained with about 50 different species (except for the comparative morphological studies). The most frequently used Icralurus sp, l1.l8.19.20.21.22.23.3S,39.63,l33.160.1. species are: Salmo sp. 4.5.13.15.3l.35.39.73.74.90.91.117.118.133.134.1M1.185.180.198; Eugerres I27.MO.230;
plumien ffo/ocen,rus
54,,31.132,2S0,251.254,255.256.257.258.259.260.261.262.263.264.275. sp,26.54.100,226.259.275;
a,,d
other teleost. Review, with omission of previous literature. Only some recent reviews have been indicated.
Navodo,,
Aslyanax modes~usl~9Jl”.lll.l~2,2~~7.2S3,
~p,6.56.oJ.Zl7.2IX.234.26U~ N o
Lepomis
~p,24.14.60.6~,
more than 4 references dea1 with any
251 2. SURVEY
OF THE STRUCTURAL
TECTAL
ORGANI-
ZATION
ally to the tectuml37. The projection alic area dorsalis been investigated
2.1. 2.1.1.
Tectal afferents
source
of tectal
afferents
is the
retina, not only in teleosts, but in al1 vertebrates. A massive contralateral retinotectal projection has been described
of the telenceph-
to the carp tectum
has
in detail by Ito and Kishidai07, who
also published an extensive study on the connections of the carp torus longitudinalislas. The torus longi-
Origin of tectal afferents
The best-known
centralis
by many authors for a variety of tele-
osts, including goldfish (Table 1). Springer and Gaffney*a’ and Prasada-Rao and Sharmaiss recently reported a small additional ipsilateral retinotectal projection in goldfish and catfish, respectively. Although by far most retina1 fibers project to the tecturn, severa1 other brain centers receive retina1 projection as well, either exclusively contralateral or bilateral (for references, see Table 1). These centers include (1) the preoptic hypothalamic region; (2) nuclei in the dorsolateral and ventrolateral thalamus; (3) pretectal nuclei and (4) so-called accessory optic nuclei in the rostral mesencephalon. Detailed discussions on the retina1 projections and possible speciesspecific andior technique dependent variations have recently been presented by Springer and Gaffney240 and Prasada-Rao and Sharmai8s. Apart from the retina, in goldfish a number of nuclei project to the tectum as well, as has been demonstrated by Grover and Sharmas4 with the aid of retrograde HRP-transport. These nuclei include one telencephalic area (area dorsalis centralis), 3 diencephalic nuclei (nucleus dorsolateralis, area pretectalis and nucleus pretectalis), 6 mesencephalic structures (torus longitudinalis, contralateral tectal half, nucleus of the rostral mesencephalic tegmentum, torus semicircularis, nucleus dorsolateralis tegmenti and nucleus isthmi) and one rhombencephalic nucleus (nucleus reticularis superior) (Fig. 3A). The telencephalo-tectal projection in the goldfish has also been described by Airhartl and Oka and Uedai77. Whereas Grover and Sharmas4 found an exclusively ipsilatera1 telencephalotectal projection, Airhart* and Oka and Uedai77 described a bilatera1 projection. In the carp, Luitent37 has obtained results closely resembling those of Grover and Sharmas4 in the related goldfish. In addition, in the carp the nucleus preopticus appears to project to the tectum, while the pretectum projects not only ipsi- but also contralater-
tudinalis appears to project exclusively to the ipsilatera1 tectum, whereas afferents to this torus originate almost exclusively vula cerebelli
in the valvula cerebelliio*. The val-
is a cerebellar
actinopterygians, longitudinalisi70.
just
strutture
as the
With respect to non-cyprinid
only present in
mesencephalic
torus
teleosts the following
results are available. Telencephalo-tectal projections have been described for Eugerres, Holocentru.9, Zctalurusl* and 5 other specie@. Commissural intertectal fibers have been demonstrated in Eugerres,
Holocentru64 and Astyanax234. The isthmotectal projection has been studied extensively in Navodonll0.207. The torus semicircularis is the largest
nucleus of the mesencephalic tegmentum and receives most of its input from auditory and lateral-line sensory systernslos.1*1.170~214.The tectal projection of the torus semicircularis has recently been described extensively by Carr et al.27 for gymnotiform teleosts. These are electric fish in which the torus semicircularis receives an important electrosensory inputt*,z’. In such teleosts, the tectum receives a well-developed ipsilateral projection from the torus semicircularis, just as has been described for the non-electrosensory goldfish and carp. In Xiphophorus, Miinz et al.164 have described a population of LH-RH (luteinizing hormone-releasing hormone) positive fibers in the tectum, which probably originate from LH-RH positive neurons in the midbrain. 2.1.2. Topographic organization of tectal afferents The topographic organization of the retino-tectal projection is a general, well-known principle for al1 vertebrates. For goldfish, the retinotopic organization of the retinotectal projection has been investigated electrophysiologically by Jacobson and Gazetis%ii6 and histologically by Meyerts6. It has been confirmed by many authors who used the goldfish retino-tectal system for experiments dealing with specificity and plasticity of nervous connections (for review see refs. 5.5 and 97) and has been described for a number of other teleosts as wel14~12.13.22.1*7.135.*30. Recently, it has been shown that the optic nerve and
252
;I
,homb
or M Tect
I
Te
FRI
TL
i
-c
NDL
f
-
Ret i
7,
Ret C
B Fig. 3. Schematic representation of present knowledge concerning the extrinsic connections of the goldfish tectum. A: afferent tectal connections (for details and references. see section 2.1.1). B: efferent tectal connections (for details and references, see section 2.3.1).
tract
also
rather
have
complex
a retinotopic
one
organization,
(Astronotus223
albeit
and
a
gold-
fiShl6.48.2ll4),
Topographic order has been described for 4 other tectal afferent systems, unti1 now, however, each in different teleosts. First, the commissural intertectal fibers appear to connect preferentially homotopic tectal regions in Eugerres and Holocentrus54 as well as in goldfishsJ.84. Secondly, the projection of the torus longitudinalis to the tectum, extensively studied by Ito and Kishidalos in the carp, has a rostrocaudal topographic organization. Thirdly, the reciproca1 isthmotectal connections in Nuvodon appear to have a rather refined topographic organizationlllJ)7. Finally, the projection from the torus semicircularis to the tectum in the electrosensory gymnotiform teleosts also has a refined topographic organization,
which
is in spatial
register
with
the
retinotopic
mapl2.27,
Some additional reports concerning the topographic tectal organization should be mentioned. Fish and Voneida64 have reported a kind of somatotopic map in the blind fish Astyanux hubbsi and in the goldfish. In the latter anima], this map was reported to be roughly in register with the visuotopic map. However, it is unknown by which afferent system these somatosensory responses are provided to the tectum. Grover and Sharmas4 reported that in the goldfish the pretectal nuclei project preferentially to the rostral tectum, whereas afferents from the torus semicircularis, the nucleus dorsolateralis tegmenti and the reticular formation preferentially terminate in more caudal tectal regions.
253
Ret
TL
Tel
cTect
AP NP NI NRMT
only DLT
TS NRS
been
demonstrated
experimentally
in
the
carptas, the typical characteristics of the margina1 axons in different teleostslo3,1~.131~149 as well as the close correlation
between
the degree of development
of the torus and the margina1 layer in a large number of teleost@
indicate
that the torus projects
same tectal layer in all teleosts, including The reports
about
ents are somewhat
%C%? Resuks of retrograde
confusing.
tectal affer-
The degeneration
ex-
periments of Vanegas and Ebbessonzss on Eugerres and Holocentrus as well as the telencephalic HRP-in-
ISPV
%%%Z?Results of anterograde
the telencephalic
to the
goldfish.
tracing experiments tracing experiments
Fig. 4. Summarizing scheme of the lamination pattern of tectal afferents iti the goldfish. For details and references, see section 2.1.3. The interrupted hatching in the fifth column is meant to indicate that the experiments performed do not allow for conclusions about terminals in this zone.
2.1.3. Laminar organization of tectal afferents The present knowledge concerning the laminar distribution of afferent terminals in the goldfish tecturn is summarized in Fig. 4. The most detailed results have been obtained by means of anterograde tracing techniques, which clearly visualize afferent termination patterns. Additional information, although less precise, has been inferred from retrograde labeling experiments in which HRP was injected in the tectum at different depths. The laminar distribution of retino-tectal terminals in the goldfish has been analyzed with a variety of techniques, including degeneratior9, autoradiographyi30J6s, cobaltchloride219, cobaltous lysinez40 and HRPt67. These studies show a massive projection to the contralateral SFGS (layer 5) and the SO (layer 6), in particular its superficial part, with some sparse termination in the SGC (layer 3/4) and the SAC (layer 2). The projection to layer 314 was not observed with degeneration techniques23i, most probably because of the relative insensitivity of this technique. A comparable lamination pattern of retino-tectal fibers has been reported for a large number of other tele~,tS7.49.Sl.57.59.89.l30.l36.l57.1R4.l86.l88.l97.l98,258.268~
Afferents from the torus longitudinalis terminate in one single tectal layer, viz. the superficial margina1 layer (layer 7). This layer is only present in actinopterygians, as is the torus longitudinalis. Although the toral origin of the unmyelinated margina1 fibers has
jections
of Ito et al.109 in severa1 other teleosts
(in-
cluding the carp and the crucian carp), clearly show termination of telencephalic efferents in the ipsilateral stratum griseum centrale, especially in layer 3/4. Some sparse additional termination may be found in layers 6 and 2259or layer 415109.A similar telencephalic tectal termination pattern can be inferred for carpia7.137, goldfishsd and catfishii on the basis of tectal HRP injections. In al1 these teleosts tectai HRP injections result in labeling of neurons in the ipsilatera1 telencephalic area dorsalis centralis, and such labeling is only obtained when the HRP injection includes the SGC. Termination of telencephalic efferents in the SGC, and especially in layer 314, was recently confirmed for goldfish by Oka and Uedai” by means of a degeneration study. However, these authors also describe a contralateral projection. The degeneration experiments of Marotte and Mark144 and Airhart2, using carp and goldfish, respectively, are even more confusing, since these authors not only describe bilatera1 projections, but also termination throughout layers 3, 4 and 5. Whereas the latter results might be due to aspecific degenerative reactions, which may occur under certain conditions (see e.g. ref. 143), the incompatibility of the results of Oka and Uedai77 and those of Grover artd Sharmas4 is more difficult to explain. Leaving the problem of ipsi-versus bilatera1 projections undecided, it may be concluded that telencephalic fibers seem to terminate for the major part in the SGC, with a special concentration in layer 3/411.84.107.109.137.177.2S9~ The layers of termination of intertectal fibers have only been determined clearly in the teleosts Eugerres and Holocentrus with the aid of light- and electronmicroscopical degeneration studies54.io6. In these species the intertectal fibers terminate predominantly in layer 3, and for a small portion in layer 2. In 3 othcr
254 reports,
dealing
with Astyanax hubbsW,
goldfishs-i
than the number
of ganglion
cells, indicating
that
and carpis7, the termination leve1 of intertectal fibers was not indicated explicitly, but judging from the
some ganglion cells might give rise to more than one fiber in the optic nervei67. A number of about 200,000
drawings
optic nerve fibers has also been estimated
published
in these papers,
in these teleost
for Eu-
intertectal fibers also terminate in deep tectal layers (layers 2 and 3). The massive degeneration found in
gerre9.
layer 7 after section of the intertectal
ing fine-structural criteria - has roughly been estimated at 30 millionis~. However, this is most proba-
Marotte
and Mark144 is probably
the torus longitudinalis
commissure
due to damage
by of
(cf. Ito and Kishidai(rs).
The number of synaptic contacts made by retina1 fibers in the goldfish tectum - identified us-
bly a serious underestimation, since HRP labeling of retina1 terminals shows that their number is substan-
The lamination pattern of the remaining tectal afferents in goldfish can be inferred from the study of Grover and Sharma@, who placed HRP injections at
tially larger than expected on the basis of the generally used fine structural criteriar66. Using HRP label-
different
ing, Murray
levels in the tectum. They conclude
that ef-
ferents from the area pretectalis, nucleus pretectalis, nucleus of the rostral mesencephalic tegmentum and nucleus isthmi predominantly in the SFGS (layer 5), and that the nucleus dorsolateralis thalami projects to the mid-tectal leve1 (SGC). Terminals from the torus semicircularis and nucleus reticularis superior could only be labeled with deep tectal HRP-injections, including the SAC (layer 2). It has already been mentioned that these results are less conclusive with respect to the laminar organization than those based on degeneration or autoradiographic experiments. Apart from the difficulty of the rather large size of HRP injections compared with the thickness of the tectal layers, variations in axon diameter, in the extension and density of the terminations of individua] axons and in the rostrocaudal position of the different projections also affect these resultsx4. Carr et al.27 found that in gymnotiform teleosts the torus semicircularis also projects predominantly to the SAC (layer 2), with some additional projections to the SPV (layer 1) and the SGC (layer 3 and 4). 2.1.4. Quantitative properties of tectal afferents From a quantitative point of view the retina1 fibers constitute by far the most important tectal afferent system in goldfish. The number of retina1 ganglion cells is approximately 130,000 in goldfish of about 10 cm lengthi67 and a similar number has been preof similar sizer23 carps sented for crucian (120,00&180,000; mean value 140,000). Larger crucian carps may reach an average number of 200,000 ganglion cellW. At least 90% of the ganglion cells project to the tectum 167.The number of optic nerve fibers in goldfish of about 10 cm length has been estimated at about 165,0004X or 2OO,OOOi6s.This is larger
et al.167 have calculated
a number
of
about 50 million retina1 terminals per tectal half, but their data do not allow an estimation of the number of resulting synaptic contacts. As far as the goldfish is concerned, afferents from the torus longitudinalis are quantitatively the second in importance. The tectum is the only known target of the torus longitudinaliWJ64, and the importance of the toro-tectal projection can be judged from the number of cells in the torus, the thickness of the marginal layer, and from the number of synapses in the margina1 layer. For goldfish of about 10 cm, the number of toral cells may be estimated at 100,000 (preliminary ce11 counts in Nissl preparations) and the number of synapses made by the margina1 axons may be estimated at about 25 million (derived from the total number of contacts of type 1 neurons, see Meekis”). Among different teleosts large differences may occur in the relative thickness of the optic (layers 5 and 6) and margina1 (layer 7) layer.+J. The margina1 layer attains its largest thickness in Holocentrus12”.226, whereas it is smallest in Trachinocephalusl2”. The optic layers have their largest relative thickness in Navodonl2’). The goldfish has a ‘standard’ tectum in this respecti?(J. Quantitative data concerning the number of axons and synaptic contacts of other tectal afferent systems are not available at present. Only the following can be noted. The telencephalic projection might well be the third in importance, considering the rather large dimensions of the area centralis dorsalis, the large number of cells labeled after tectal HRP injections*(‘7 and the quite dense degeneration in the SGC after telencephalic lesionszsy. In Navodon the nucleus isthmi has a rather heavy projection to the tectum as welW. In severa1 teleosts the intertectal projection
255 is reported
characteristic
to be very sparse54.83.*4,106,137.234 and in
location
and
extension
of dendritic
goldfish and carp also only a small percentage of cells in the torus semicircularis seems to project to the tec-
trees and with characteristic axonal properties. Four ce11types have myelinated axons which leave the tec-
tums4.137. In contrast, the torus semicircularis of gymnotids has a rather heavy projection to the tectum27.
turn (type VI, X, X11 and X111), whereas 8 ce11 types
The heaviness
and XIV). The axonal properties
teleosts
of other projections
is uncertain.
the nucleus pretectalis,
Judging
to the tectum
are interneurons
of
from the small size of
area pretectalis,
nucleus
XV are obscure. as
dor-
follows:
(type 1, 111, IV, V, VII, VIII, The number type
1,
1X
of type 11, X1 and
of neurons
is estimated
5000-20,000;
type
111,
solateralis and nucleus of the rostral mesencephalic tegmentum in goldfishisi these centers probably give
2500-10,000;
rise to only few tectal afferents.
that the cytoarchitecture of the goldfish tectum consists of a fairly strictly organized frame, formed by
2.2. Intrinsic tectal strutture
the rather
2.2.1. Tectal neurons The neurons of the goldfish tectum have been studied with Golgi techniques by Leghissaiss, Meek and Schellartisz and Romeskie and Sharmazm. The results of Meek and Schellart are summarized in Fig. 5. These authors distinguish 15 ce11 types, each with a
rons, intermingled with the numerous and variable type XIV neurons. A detailed comparison of these results and those of Leghissa has been presented by Meek and Schellartlsz, and similarities and differences with respect to the results of Romeskie and Sharmazm have been discussed by Meekisi. Tectal cytoarchitecture has also been analyzed
grmp
1 _1
I
l
Ila
Ilb
X\,,\,
,
-
type
I
group type Irr
,--
2 Ill
XI
l-2
million.
infrequently
and Schellartlsz
occurring
conclude
type I-X111 neu-
VI
5_--_
-II
XIII ,
Meek
II_
IVa/b V
4
,
XIV,
type IV-X111, each 500-2000 and type
XIII 2
I
XIV[‘largél-,
~
_
XIV~small’l _
I ,_._~
XV. I
71
Fig. 5. Schematic representation of the cell types in the goldfish tectum (after Meek and Schellartisz). The soma sizes and dendritic extensions of type I-X111, have been drawn to scale using average values, whereas for type XIV and XV some typical neurons have been drawn. Unmyelinated axons have been drawn thinly, whereas myelinated axons leaving the tectum end with an arrow. The cell types and groups have primarily been distinguished on the basis of dendritic properties. Group 1 includes neurons with dendrites in layer 7 (type 1 and 11); group 2 includes monostratified neurons (with dendrites at a single level; type 111, IV and V); group 3 includes bistratified neurons (with dendrites at two separate levels; type VI, VII, VIII, 1X and X); group 4 includes mulrisrrarifiedneurons (type X1. X11 and X111); and group 5 includes non-stratified neurons (type XIV and XV). The calibration bar is 100 Pm.
256 with the Golgi-technique
Barbus fzu-
in the teleosts
viatilis’g2, Salmo irideus13.186, Eugerres plumieri263, Bagrus sp. and Ictalurus punctatu9,
Hemichromis
Poecilia32 and Holocentrusl06. Whereas some studies predominantly dea1 with glia cells12*.246or glycogenmetabolism248, most studies dea1 with cytological
bimaculatu_+~, Holocentrus rufus and H. ascensio-
synaptic
nk226. Taking
regard to the synaptic organization be noted.
al1 Golgi-studies
together,
it may be
concluded that, except for quantitative differences, the tetta of the teleosts studied are basically similar. This conclusion is supported by the comparative study of Kishidalzo on a variety of teleosts. A detailed comparison of various Golgi-studies sented by Meek and Schellartis2. Whereas
severa1 Golgi-studies
tectum tend to stress the variability
has been pre-
on the teleostean of the individua1
neurons133,200.*26.263,others emphasize a strict classification of ce11types on the basis of relevant similaritie@Js2. The schematic presentation of ce11 types in Fig. 5 is the result of the latter approach, presenting a classification of ce11 types with averaged characteristics determined in a quantitative waylS2. Such a presentation, which like al1 classifications necessarily includes some simplications, neglects some variabilities and favours some characteristics at the expense of others, might seem to be simplistic in view of the capriciousness of the Golgi-methods and the large variability of individua1 neurons. It should, however, be realized that (1) when a large number of neurons is investigated using a variety of Golgi modification@ a rather complete description of neuronal types may be obtained; (2) The variability of tectal neurons is often more apparent than rea1 because of incomplete impregnation, oblique planes of sectioning, and difficulties in defining tectal layers in Golgimaterial; (3) The method employed for classification by Meek and Schellartls2 clearly shows monomodal distributions for the location of specific dendritic trees; and (4) EM investigation has revealed that at least 6 of the ce11types distinguished by means of this classification have characteristic synaptic properties as welll50. The major advantage of a strict classification on the basis of well-defined characteristics is that it allows for integration of neuronal morphology with synaptology*5(J, circuitry (see section 3), as well as physiology (see section 5). 2.2.2. Synaptic organization of the tectum Severa1 aspects of the ultrastructure of the tectum of normal, adult teleosts have been studied, in particular in g~~~f~~~l49.l50.246.248.267, carp31.103, Eugerresl31,
properties
of the neuronal
elements.
and With
the following can
In layer 7, the margina1 layer, the thin, unmyelinated fibers from the torus longitudinalis make many synaptic contacts with the spiny dendrites of type 1 or pyramidal neurons. These contacts are of the asymmetric type and the presynaptic elements contain small round vesicles31~1~3~*06~‘~~,~~4.~4Y. Comparison of the ultrastructure
of the margina1 layer in carp (Cy-
prinus carpio) and trout (Salmo gairdneri) revealed that in the carp more convergent synapses occur (one terminal contacting two or more spines of the same neuron), whereas in trout the tota1 number of synapses is substantially larger-ll. In Holocentrus, which has the largest margina1 layer of al1 teleosts investigated SO far!*” a second type of presynaptic element, containing flattened vesicles has been described in layer 7106. Unti1 now, these have not been found in other ~~~~~~~~31.103,131.14Y, Layer 5, the SFGS, is the main region of retina1 termination (see section 2.1.3). As has been shown with degeneration experiments3~tl)h~l”* retina1 terminals contain large round vesicles and pale mitochondria with delated cristae, and make asymmetrical synaptic contacts. These criteria can also be used in norma1 EM rnaterial”,lO6,1”‘.‘““. Their frequency of occurrence in the SFGS has been estimated at 16% in Holocentrus and 18% in goldfish, while Meekls” has calculated that they form 1&20% of the synaptic contacts in the SFGS of goldfish. However, Murray and Edwardsl66, using HRP labeling of retina1 terminals, recently have shown that at least 37% of the terminal population in the SFGS is of retina1 origin. This means that a large portion of sections through retina1 terminals is not recognizable by pure morphological features, and that the previously reported frequencies are serious underestimations’66. The most important postsynaptic elements for retina1 terminals are small dendritic profiles- 1.1~13,11~6,131.150,166~ In addi_ tion, other structures are postsynaptic to retina1 terminals, including large dendritic shaftsl3~~t4Y~l50,sornatal49.tsO and profiles containing synaptic vesic~es103.106,14Y,
A variety
of non-retina1
presynaptic
elements
in
257 the SFGS has been describedlo3,106,131.149.Unti1 now,
SAC. In contrast,
the origin of these elements partly represent afferent
ic shafts of type XIV neurons,
is unknown. terminals
They might of various
sourcesi49 (see Fig. 4) and partly axon terminals
of
interneurons. In particular the population of Ss terminals (small terminals with small round vesicles) reported in Nolocenrrust06
might well represent
axonal
the synaptic density on the dendritwhich pass through the
SAC and SGC to reach the SFGS, is relatively
low.
The SAC or layer 2 is dominated by the occurrence of myelinated fibers, which partly represent tectal efferentsta3.tst~t49. However, fibers
represent
tectal
another
afferents,
portion
of these
terminating
pre-
terminals of type XIV or SPV neuronst4s. Postsynaptic structures in the SFGS show a large variability as
dominantly on the dendrites and ce11bodies of the efferent type X111 neurons and the basa1 dendrites of
well, and integration of hght- and electron-microscopic results in this layer is rather difficultia3.t~.tst.
the efferent
Meekt49.150 could identify
Fig. 4). The SPV or layer 1 is characterized
a number
of postsynaptic
structures on the basis of a combined study, each with characteristic synaptic
Golgi-EM properties.
The frequently occurring type I neurons, e.g., receive only few synaptic contacts on their ce11body and dendritic shaft, whereas the relatively rare type VI neurons receive much more synaptic contacts. A low density of synapses on type 1 or pyramidal neurons has also been reported for Eugerresist. Villani et al.267 describe that some neurons in the SFGS of goldfish exhibit degenerative changes after kainicacid treatment, whereas others do not. Judging from their ultrastructural features, the kainic-acid sensitive neurons belong to type 1, whereas the insensitive neurons belong to type VI (cf. refs. 149 and 267). In the SGC (layers 4 and 3) a variety of pre- and postsynaptic elements constitute a complex neuropil3*.~03.~0~.131.144.149. Only a smali portion of ah these elements has been identified. Ito et al.iw showed by means of degeneration experiments that in Hoiocentrus some of the S4 terminals (medium-sized terminals with various-sized, round vesicles) belong to telencephalic afferents, whereas some of the S5 terminals (small terminals with small round vesicles) arise from intertectal commissural fibers. However, comparison of the Golgi-EM results of MeektQ and the results of Ito et al.106 suggests that most S, terminals, which form 65% of al1 terminals in the SGC of Holocenfrus, represent type XIV axon terminals, whereas the S4 terminals, in particular those in Iayer 314, may represent type 1 axon terminalst49. Severa1 types of postsynaptic elements in the SGC have been identified and described by Meekt49.tsa in the goldfish with Golgi-EM. The ce11bodies and dendrites of the efferent type X11 or fusiform neurons have a rather large density of synaptic contacts, just as the dendrites of the efferent type X111 or multipolar neurons from the
type X11 neuronsi49.
the SAC may originate
These afferents
from various
sources
in (see
by the closely
packed celi bodies of the pe~ventricular (type XIV and XV) neurons, which are traversed by various fiber bundles3*.10~.131,144.*49.*46.*67. Synaptic contacts only occur on the somata of the most superficially located ce11 bodies, whereas deeper positioned neuronal somata are devoid of such contacts131.149.l~o.*~. Some authors have described junction-like specializations between somata and/or proximal dendrites of these neuronstas.149. Whereas the majority of these neurons is resistant to kainic-acid treatment, some of them show kainic-acid induced degenerative reaction+. Present knowledge concerning the synaptic organization of the teleostean tectum may be summarized as follows: first, in most teleosts (goldfish, carp, Eugerres) tectal synaptology appears to be straight-forward, since almost exclusively axo-dendritic and axosomatic synapses have been found31.lo.7.131.149.*6:.The only known exception is constituted by the few contacts between retina1 terminals and vesicle-containing profilestOs~t49. However, in the highly developed tectum of Holucentr~l*O.22b synapto~ogy appears to be somewhat more complicated, since in this tectum presynaptic dendrites (F2 type) and glomerular arrangements (S3 type) have been encountered as wellt06. Secondly, each tectal layer contains its own, characteristic set of presynaptic terminals, as has qualitatively been described by severa1 authors3*.t03,tst,t44 and has been quantified by Ito et al.106 for Holocentrus. The most striking features of this presynaptic lamination pattern are (a) the exclusive occurrence of toral afferent terminals in the marginal Iayer (layer 7)31.1~3~~~.~3~.~4Y; (b) the occurrence of retina1 terminals in the SFGS (layer S), which, however, constitute only a minor portion of the pre-
258 layer (about synaptic elements in this 2WO%)3.1(~6.13*.132.‘66;(c) The abundant occurrence (65%) of S, terminals most probably
in the SGC (layer 4 and 3)1’)6,
representing
axon terminals
of the
periventricular type XIV neuronsi4Y; and (d) The occurrence of severa1 types of myelinated afferent ter-
The most important differente between the results of Grover and Sharmas-i and those of other authors mentioned”4.‘37,224,234 concerns the tetto-isthmic projection,
which has not been described
for the gold-
fishss but was demonstrated in al1 other teleosts investigateds4.1’7.224.2’4. Moreover. Ito et al.ii’).ili and et al.207 demonstrated in Navodon modprojection is highly or-
minals in the SAC and deep SGC (layers 2 and 3)i@.
Sakamoto
Thirdly, the postsynaptic structures in the tectum (the dendrites and ce11 bodies of the tectal neurons)
estus that the tetto-isthmic
appear to have a characteristic density and number of synaptic contactsi”“. The average density of contacts
trophysiological evidente for the existence of a tectoishtmic projection in Holocentrus and Eugerres. In fact, in al1 classes of vertebrates investigated, the nu-
per ce11 type ranges from about IOOprn? neuronal ber of contacts neuronlsO.
15-80 contacts
per
surface, whereas the average numranges from about 200 to 5000 per
2.3. Tectal efyerents 2.3.1.
Tectal targets
The efferents of the goldfish tectum have been investigated by Grover and Sharmass. Their results, combined with those of Schmidt”” concerning tectoretina1 efferents in the goldfish, are summarized in Fig. 3B. A projection to the nucleus isthmi, not identified as a tectal target in the goldfishs-i is included in Fig. 3B for reasons to be dicussed below. The overall pattern of tectal efferents has also been investigated in the teleosts Ictaluru.94, Eugerres and Holocentru+.
the blind fish Astyanax hubbsP, and the carp Cyprinus carpiol37. These studies agree with the results of Grover and Sharmas” in describing ascending, bilatera1 projections to the nucleus rotundus and other pretectal ce11groups, a media1 projection to the contralateral tectal half and descending projections to the ipsilateral torus semicircularis, other ipsilateral dorsolateral tegmental areas, the ipsilateral lateral reticular formation and the contralateral medial reticular formation (Fig. 3B). The descending efferents constitute the largest efferent tectal tract (tractus tetto-bulbaris). Ebbesson and Vanegas and Luiteni37 describe an additional media1 projection to the torus longitudinalis. However, the toral afferents labeled by these authors represent at least in part the cerebello-toral afferents, which traverse the tectum before reaching the torus 1ongitudinalisi~‘s. A projection from the tectum to the torus semicircularis has also been described for electric gymnotiform tele()sts?7.2’4
dered,
and Williams
and Vanegas
cleus isthmi or its homologue,
provided
the nucleus
elec-
parabige-
minaliss7Jn receives the bulk of its input from the tectum mesencephali (teleosts,ii2.207: amphibians 85.X7.203.274. , reptiles,h”: birds,YY,i”“; and mamrnalsY.s’~,‘+t,l~“) and is considered as a ‘satellite system’ of the tectum or colliculus superiorsz. SO, a nucleus isthmi without tectal input would be quite unlikely. Most probably. the deviating results of Grover and Sharmasj with respect to the tetto-isthmic projection will have a technical explanation and not reflect a species differente. Consequently, also in the goldfish the nucleus isthmi should be considered as a tectal target (Fig. 3B), just as in other teleosts. The existence of a tetto-retina1 projection is a point of controversy in the literature. Anatomica]163,245,253.278 electrophysiological and studiesJ(rxJiY~~shhave clearly demonstrated the existence of retinopetal, centrifuga1 fibers in teleosts. However, the origin of these fibers is not certain. Electrophysiological results strongly suggest a tectal origin of retinopetal fibers. Using electrical stimulation of the optic nerve, Vanegas et al.256 found in Eugerres a fast-conducting population of fibers in the SO (layer 6) that showed severa1 characteristics of antidromic activation. Moreover, these fibers remained intact after eye-enucleation, which excludes a retina1 origin and suggests a tectal origin. Similar electrophysiological results were obtained by Schmidt?iY in the goldfish. Electronmicroscopical studies corroborated the persistente of large caliber (= fast conducting) fibers in the SO after eye-enucleationl32. Sandeman and RosenthaP recorded the activity of retinopetal fibers in the trigger fish Hemibalistes chrysopterus, which could be activated by visual, vestibular, vibratory and tattile stimuli. Their responses were weakened by ablation of the ipsilateral tectum and abol-
259 However,
these represent
other ce11types than those
ished by ablation of the contralateral tectum, strongly suggesting a tectal origin. Anatomica1 studies, using HRP injections in the eye or optic nerve, have yielded less consistent re-
in the SFGS and SGC, while those in the SFGS are not bipolar. Furthermore, the number of neurons la-
sults. Schmidt*is has reported
beled by Meyer and Ebbessonis’
for the goldfish the bi-
lateral labeling of a large number vertically oriented bipolar tectal
(about 1500) of neurons in the
SFGS. However, this labeling could not be obtained in norma1 specimen, but only when the eye had been enucleated 2-6 weeks before, and Springer and Gaff-
labeled by SchmidW,
was considerably
because they are located both
and Meyer et al.158
smaller than the number
of neurons
labeled by Schmidt*i9. Apart from the tectal neurons, Meyer and Ebbessonis’, Meyer et al.158 and Ebbesson and Meyers* labeled severa1 tel- and di-encephal-
in
ic nuclei as well, which were not labeled by Schmidt*ig. Other studies in severa1 teleosts did not at al1 result in
demonstrating tetto-retina1 neurons in goldfish. The identity of the neurons shown by Schmidt*is is anoth-
labeling of tectal neurons, but only of various nontectal sources of retina1 afferents, including a telen-
er problem. Some of them probably represent type 1 neurons (see Fig. 5), because of the characteristic bi-
cephalic nucleusi62J63, a preoptic nucleu9, a nucleus in the optic tract76 and a pretectal nucleus’62. Peyrichoux et al.184, using cyprinid fishes, could not at al1 produce reproducible labeling of retinopetal cells. SO, with respect to tetto-retina1 projections severa1 uncertainties exist, which may partly reflect speciesdifferencess*, but partly also may be due to technical reasonsisi. Nevertheless, the results of Schmidt*iY have been tentatively incorporated in Fig. 3B, since at present the existence of recto-retina] fibers cannot be excluded.
ney*m and Uchiyama
et al.253 did not succeed
furcation of the apical dendritic shaft at the boundary of layer 6 and 7 or because of the presente of a basa1 dendritic shaft in layer 4. Type 1 neurons, however, are clearly interneurons, not projecting outside the tectumi@J5*. Other neurons labeled by SchmidW might represent type VI neurons, which indeed have efferent axons. However, these axons are not of a large caliber and do not course through the SOi@,is*, as could be expected for tetto-retina1 fibres from the electrophysiological results (see above). Meyer and Ebbessoni57, Meyer et al.158, and Ebbesson and MeyerQ also labeled tectal neurons after HRP injection in the eyes of Synodontis nigriventris, Tetraodon fiuviatilis, and Julidochromis regani, respectively.
VI
X
\
Fig. 6. Summary of the present erences, see section 2.3.2.
knowledge
-4
tractus
concerning
XIV
XIII
XII
7
retIna
2.3.2. Efferent tectal ce11types Although most Golgi-studies remained unable to determine the character and course of tectal axons, Meek and SchellartiQ could prove on the basis of a
the efferent
tetto-bulbarls
tectal neurons
xv
/ nucleus Isthmi
and their targets
pretectum +contralat tectum
contralateral tectum
in the goldfish.
For details and ref-
260 modified
Golgi-Cox
tal neurons
techniqueids
have myelinated
that 4 types of tec-
axons leaving
the tec-
turn (type VI, X, X11 and X111, see Figs. 5 and 6). Electron
microscopica1
observations
confirmed
this
finding for type VI, X11 and X111 neuronst49. The investigations of Grover and Sharmas4 corroborated the efferent character
of type X11 and type X111 neu-
rons, since both types of neurons were labeled after HRP injections in the torus semicircularis or in the tractus
tetto-bulbaris.
According
to the results
of
Schmidtzis, extensively discussed in the preceding paragraph (2.3.1), the axons of type VI neurons might possibly terminate
in the retina. HRP injection
in tectal targets have not yet labeled neurons that could belong to type X. Both light- and electronmicroscopic investigations revealed that in goldfish type XIV neurons have unmyelinated axons with abundant collateral terminations within the tectumt49.*52. Similar findings have been reported for Hemichromis”” and Holocentrus**6. However, recent investigations using HRP injection in tectal targets revealed at least 3 sites of termination of type XIV axons outside the tectum (viz. the nucleus isthmi, the pretectum and the contralateral tectal half), which means that severa1 typr XIV axons also have collaterals that leave the tecturn. Ito et al.112 labeled a peculiar subtype of type XIV neurons after HRP injection in the nucleus isthmi of Navodon modestus. This subtype, with a dendritic as well as an axonal arborization in iayer 6, has also been demonstrated in the goldfish (Meek and Schellartis?, p. 101; see also their Fig. 16, and Fig. 5 of the present paper). Conceivably, also in the goldfish, the basa1 axon collateral of this subtype projects to the nucleus isthmi (Fig. 6). Grover and Sharma84 demonstrated in the goldfish two other targets of type XIV axons, viz. the pretecturn and the contralateral tectal half. HRP injection in the pretectum, including the area pretectalis and nucleus rotundus, but not the nucleus pretectalis and nucleus geniculatus laterahs, labeled monopolar neurons in the tectal layers 1 or 2, with an apical process reaching layer 5, thus allowing for identification as type XIV neurons. Retrograde labeling in the contralateral tectum was difficult to obtain. but in one out of 15 attempts, Grover and Sharmasj clearly labeled neurons in the SPV. Although some of the labeled cells had a peculiar multipolar shape, most of
them might represent
type XIV or type XV neurons.
A projection of type XIV neurons to the contralateral tectal half is supported by two other findings. First. O’Benarl76
recorded
closely resembhng
in the SPV electrical
the activity of intertectal
activity commis-
sural fibers as recorded by Mark and Davidsoni41. Secondly, Ito et al.106 describe degeneration of some axon terminals
of the S, type in the tectum Hofocentectal half. As is
trus after lesions in the contralateral
discussed by MeektQ, SS terminals closely resemble the axon terminals of type XIV axons as identified in the goldfish (see also section 2.2.2). It is important to note that most targets
of type
XIV neurons project back upon the tectum (nucleus isthmi, area pretectalis and contralateral tectum; cf. Fig. 3A). This implies that most efferent axons of type XIV neurons form part of extratectal feedback loops. The present knowledge concerning the projections of efferent tectal neurons is summarized in Fig. 6. Thus far. the tectal neurons projecting to the nucleus pretectalis, nucleus geniculatus lateralis and nucleus dorsolateralis thalami have not been identified. 3. 4 CONCEPTUAL
FRAMEWORK
OF TECTAL
CIR-
CUITRY
3.1. Starting points Two types of starting points underhe the conceptua1 framework of tectal circuitry to be presented. On the one hand, severa1 structural results as surveyed in the preceding section have direct implications for tectal circuitry. These include (1) the straight-forward synaptic organization of the tectum, which implies that axon-terminals can be considered as exclusively presynaptic structures. whereas dendrites, celi bodies and initial parts of axons are exclusively postsynaptic structures; (2) the characteristic lamination pattern of presynaptic structures; and (3) the characteristic location, extension and synaptic densities of postsynaptic structures. On the other hand, some assumptions have to be adopted about the interrelations of different types of presynaptic structures which coexist at the same tectal leve]. In the next paragraphs both types of starting points will be discussed in detail. For references, the reader is referred to the preceding survey of the structural tectal organization.
261 3.1 .l.
The lamination pattern of tectal neuronal el-
ements 3.1.1.1.
because of the presente pretectalis,
Tectal afferents. On the basis of the lami-
of afferents from the nucleus
area pretectalis
and nucleus
isthmi.
The
nation patterns of tectal afferents as discussed in the preceding section (Fig. 4), 4 main afferent tectal
nucleus of the rostral mesencephalic tegmentum provides signals of unknown modality to this zone. (3) The bulk of telencephalic afferents terminates
zones can be distinguished
in the SGC, particularly
(see Fig. 7, left third).
(1) Afferents from the torus longitudinalis nate in layer 7, which thus can be characterized
be considered as the telencephalic afferent zone. However, also the axons of type 1 neurons, which are
termias the
the recipients
toral afferent layer. Since the torus longitudinalis receives its signals predominantly from the valvula cerebellilss, layer 7 may also be called the cerebellar ferent layer226.
in layer 3/4, which thus could
of toral signals, terminate
in layer 3/4.
Consequently, this zone should preferably be considered as the telencephalic-toral (cerebellar) afferent
af-
zone. In addition, tegmenti
(2) Layer 5 and its border zones (layer 5/6 and 4/5;
axons of the nucleus dorsolateralis
and a few retina1 fibers terminate
in this
zone. For the sake of simplicity, these will be left out of discussion. (4) Layers 2 and 3 can be considered as the ‘deep’ tectal afferent zone. Afferents from the contralateral tectal half, torus semicircularis and reticular formation specifically terminate in this region. In addition, some retina1 fibers terminate in layer 2, and it cannot be excluded that the area pretectalis, nucleus pretectalis, nucleus isthmi and nucleus of the rostral mesencephalic tegmentum have some additional projections to this region as well. The recent finding of LHRH containing afferents which terminate specifically in layers 2 and 3 in Xiphophorusl64 as well as the occurrence of severa1 types of myelinated afferents in
see Fig. 2) contains the bulk of retina1 afferents, and in addition afferents from the nucleus pretectalis, the area pretectalis, the nucleus isthmi and the nucleus of the rostral mesencephalic tegmentum. The nucleus pretectalis and area pretectalis can both be considered as ‘visual’ nuclei, since they have an important bilatera1 input from the retina (for goldfish, see refs. 231, 240, 241). The nucleus isthmi may also be considered as a ‘visual’ nucleus, since it receives its input from the ‘visual’ nucleus pretectalisll* and from a subtype of type XIV cellslt*, which also must be considered as ‘visual’ (see below). SO, layer 5 and its boundaries may be designated as the ‘visual’ afferent zone, not only because of their retina1 input, but also
cell types
TL
AP NP NI Ret NRMT
cTect Tel TS DLT NRS
Ill
IV VII
v
VIII IX
XIV
VI
1 2
SPV
1
0 -,
postsynaptic strutture presynaptlc strutture efferent axon
Fig. 7. Summarizing scheme of the laminar organization of the neuronal elements in the goldfish tectum. With respect to the tectal afferents, the main results as summarized in Fig. 4 have been indicated. With respect to the tectal ce11 types, the average position of the dendritic trees and axon terminals has been indicated (without indication of their extension) as summarized in Fig. 5. For details the reader is referred to section 3.1.1.
262 these layersi@ indicate
that the significante
of the
sively in the visual afferent
‘deep’ tectal afferent zone is not yet fully understood. The various kinds of non-visual responses that can be recorded
from the tectum are probably
‘deep’ tectal afferents. 3.1.1.2. Teda1 interneurons. pattern
of tectal neurons
provided
VI1 neurons). (c) Interneurons with their dendrites in layers 3 and 4 (type V neurons). (d) Interneurons with their dendrites both in the ‘visual’ and in the tel-
via
encephalic-toral The
stratification
in summarized
layer (type 111, IV and
(cerebellar)
afferent
layer 3/4 (type
VI11 and 1X). (e) The less strictly organized and very numerous type XIV neurons, which have their main dendritic tree in the visual afferent layer 5, and addi-
in Fig. 7
(middle and right thirds) which is derived from Fig. 5 by means of the following modifications. TO stress
tional dendrites
in other tectal layers.
the lamination pattern, only the average location of dendrites and axons is presented, without indicating
With respect to the axon terminations of tectal interneurons, Fig. 7 shows a rather refined stratifica-
their extension.
tion pattern in comparison with the pattern of tectal afferents. The axons of type 1 neurons specifically
Information
ce11bodies is omitted,
on the localization
of
since they do not seem to have
terminate in layer 3/4. The axons of the interneurons of group b, c and d terminate in layer 5, 415 or 4 in such a way that each of these layers contains the axon terminals of one monostratified or horizontal neuron and one bistratified neuron (layer 5: type 111 and
any specific significante in tectal circuitry deviating from that of dendrites. On the basis of the position of the dendrites of tectal interneurons in the 4 afferent zones described above, 5 groups of neurons can be distinguished (Fig. 7). (a) Interneurons with their dendrites mainly in the toral (cerebellar) rons). (b) Interneurons PRESYNAPTIC
type VII; layer 4/5: type IV and type VIII; layer 4: type V and type 1X). A portion of the axons of type V neurons terminates in layer 3. Apart from this, the
afferent layers (type 1 neuwith their dendrites exclu-
ZONES
POSTSYNAPTIC CHARACTERISTICS of some cell types type
7
:Tor
6
: Vis
+
516 j
: Vis + Ill
+ VII + XIV
4/5
: Vis+
+ VIII + XIV 9$_
I
type Ill
type
XIV
type VI
type XII
typexlll,
‘>g’
4 314
IV
: : Tel
213 ; : Deep
Fig. 8. Some organizational characteristics of pre- and postsynaptic structures in the goldfish tectum. A: laminar organization of the presynaptic tectal structures (afferents and axons of interneurons), which allows the distinction of eight presynaptic zones (see section 3.1.2). The presynaptic zones distinguished continue as gray bands in part B of this figure. B: characteristic position, extension, synaptic density and number of synaptic contacts of the postsynaptic structures of 6 important tectal cell types in the presynaptic zones distinguished (modified after Meektso). Both the dendritic lengths and the horizontal dendritic extensions have been drawn to scale, using average valuestsa. The diameters of the structures drawn indicate their mean circumference. Each dot represents 10 synaptic contacts.
263 ‘deep’ afferent layers 2 and 3 are very poor in axon terminations of interneurons as compared to the more superficial layers 4 and 5. The axons of type XIV neurons, which show many individua1 variations, terminate predominantly in layers 5, 4 and 3 with a preponderante in layer 4, the only tectal zone in which most probably no afferent terminals occur. In addition, some axons or collaterals of type XIV neurons project outside the tectum. 3.1.1.3. Efferent tectal neurons. Four types of neu-
shafts, ce11bodies and initial parts of axons are exclu-
rons project outside the tectum with myelinated axons and without recurrent collateralization in the tec-
consideration,
turn. Comparison of these efferent neurons (group f in Fig. 7) with the tectal interneurons reveals that type VI neurons show some correspondence with group b in having their dendrites in or near the visual afferent layer, and that type X neurons show a close correspondence to group d with dendrites in layer 415
posed to occur to some extent in layer 3.
as well as in layer 3/4. Type X11 and X111 constitute a separate group of multistratified efferent neurons. Three tectal ce11 types have obscure axonal properties (group g in Fig. 7). These will be left out of consideration in the next paragraphs.
sively postsynaptic or receptive structures. Combination of the 4 main afferent zones with the laminar distribution of the axons of tectal interneurons allows a distinction of 8 presynaptic zones or laminae, each of which contains a characteristic population of presynaptic structures; these zones are listed in Table 11 (cf. Figs. 7 and 8). It should be noted that the few axons of type XIV neurons
that might occur in layer 3/2+2 are left out of and that telencephalic
not strictly confined
afferents
are
to layer 314, but are also sup-
3.1.3. Postsynaptic determination of neuronal input The postsynaptic structures of the tectal ce11 types (dendrites, dendritic shafts, ce11 bodies and initial parts of axons) each have a characteristic average location in the different tectal layers (Figs. 5 and 7), and consequently also in the different presynaptic tectal zones distinguished. In addition, the dendritic trees have a characteristic
average extension
(Fig. 5)
and at least 6 tectal ce11types have characteristic aptic density
patterns
along their receptive
syn-
surface
3.1.2. Presynaptic tectal zones .4 conceptual framework of tectal circuitry implies a tentative description of the connectivity patterns
(Fig. 8). This characteristic location, extension and synaptic density together result in characteristic average numbers of synaptic contacts of the different
between the different types of pre- and postsynaptic structures. In the goldfish tectum this is greatly facilitated by the straight forward synaptic organization, i.e. the almost exclusive occurrence of axo-dendritic and axo-somatic synapses (section 2.2.2). This means that more peculiar contacts as e.g. triads, glo-
ce11 types in the different presynaptic tectal zones (Fig. 8), which may vary from zero (when no receptive surface is present in a presynaptic zone) or almost zero (e.g. the ce11 bodies of type 111 and XIV and the apical dendritic shaft of type 1) to thousand or more (e.g. type 1 in layer 7; type X11 in layer 4 and layer 2/3; type X111 in layer 2). It will be clear that the connectivity patterns of the tectal ce11 types are to a great extent determined by their characteristic average postsynaptic properties in the different presynap-
merular arrangements, dendro-dendritic and axo-axonal contacts can be left out of consideration, and that axon terminals can be considered as exclusively presynaptic structures, whereas dendrites, dendritic TABLE
11
Layer 7, with toral afferents
(tor)
Layer 6, with visual afferents
and axons of some type XIV neurons
Layer 516 and 5, with visual afferents Layer 4/5, with visual afferents Layer 4, without
afferents,
Layer 314, with telencephalic
and axons of type 111, VI1 and XIV
and axons of type IV, VI11 and XIV
but with axons of type V,, 1X and XIV afferents
Layer 3, with ‘deep’ and telencephalic Layer 312 + 2, with deep tectal afferents
(vis + XIV) (vis + 111 + VI1 + XIV) (vis + IV + VI11 + XIV) (V, + 1x + XIV)
and axons of type 1 and XIV
(tel + 1 + XIV)
afferents
(deep + tel+
and axons of type V,, and XIV
(dccp).
V, + XIV)
264 tic tectal zones
(Fig. 8). For a precise
evaluation,
however, the contribution of different types of presynaptic structures that occur in each presynaptic tec-
The absence of cellular specificity in the goldfish tectum is, apart from the general considerations presented above, supported by the following considera-
tal zone should be considered
tions. First, optic nerve terminals
as well. As will be out-
appear
to termi-
lined in the next section, these contributions may be approximated by presuming the presente of laminar
nate on al1 types of postsynaptic structures investigated in layer 5, which clearly indicates the absence
specificity.
of cellular specificity for this important
3.1.4.
afferent. Retina1 fibers even seem to occupy equa1 percentages of the postsynaptic sites present on the
The hypothesis of laminar specificity 3.1.4.1. General considerations. In a laminated brain strutture, the organization of synaptic connections may, in principle, reveal complete unspecifici-
ty. laminar specificity or cellular specificityr3’.
Lami-
nar specificity, as defined by Maler et a1.139, implies that presynaptic structures are specific with respect to their layer(s) of termination. but not with respect to the different types of postsynaptic structures present in that layer(s): they are presumed to terminate without preference on al1 types of postsynaptic structures within their layer of termination. In contrast, cellular specificity means that presynaptic structures only terminate on specific postsynaptic structures within a layer. Although a number of cellular specific connections have been described (e.g. the contacts between climbing fibers and Purkinje cells in the cerebellum (e.g. ref. 179) or the contacts between the axons of chandelier cells and the initial parts of pyramidal ce11 axons in he visual cortexsR.**2.?JX ), by far most types of synaptic contacts in the brain of vertebrates do not the cellular reveal specificity at leve1 ). This suggests that in (e.g. 78 88.98.139.lXl.1Yl.236.?37.273.276 laminated brain structures not SOmuch (chemo-) specific ce11to ce11interactions. but rather a refined lamination pattern of pre- and postsynaptic elements with competitive intralaminar interactions is used as a mechanism to realize specificity of synaptic connections, and renders the concept of laminar specificity rather plausible. The attractiveness of this concept of laminar specificity. even indicated as the ‘sine qua non’ of laminated structurest”. is that it may explain the formation of complex circuitry patterns in terms of relatively simple anatomica1 organizing principles. 3.1.4.2. Laminar specificity in tectal circuitr),. The concept of laminar specificity as defined in the preceding section implies both the existence of presynaptic zones and the absence of cellular specificity within these zones.
different
types of postsynaptic
type of tectal
structures
5150. Secondly, the similar, characteristic of contacts on al1 postsynaptic structures
in layer mean size in certain
layers, dendrites of type XIV excluded, might indicate that these structures are al1 contacted by the same population of presynaptic elementsts’). Thirdly, the concept of laminar specificity is closely associated with mechanisms of competition. Within the goldfish tectum, the different presynaptic structures that occur in each presynaptic zone might well compete for available postsynaptic sites, since the different types of postsynaptic structures each have a restricted, predetermined number of synaptic contactst”” (see section 2.2.2 and Fig. 8). The results of Murray et al.167, who found the same retina1 terminal density in tetta with a norma1 and with a ‘compressed’ retinotectal projection, are also in support of competitive mechanisms regulating synapse formation. Adoption of the hypothesis of laminar specificity for the goldfish tectum completes the set of structural organizing principles that are necessary as starting points for a tectal circuitry diagram. In summary, these organizing principles are (cf. Fig. 8): (a) the occurrence of presynaptic tectal zones or laminae. each with a characteristic population of presynaptic structures; (b) determination of interlaminar interrelations (i.e. interrelations between presynaptic structures in different presynaptic zones) by the characteristic location, dimensions and synaptic density of the postsynaptic tectal structures; and (c) determination of intralaminar interrelations (i.e. interrelations between presynaptic structures within a single presynaptic zone) by rules of laminar specificity. The resuhing tectal circuitry diagram which emerges from these principles is drawn in Fig. 9. This figure is derived from Fig. 7 by introduction of the following modifications: (a) axons have been drawn as lines; (b) information on the dendritic extensions and frequency of occurrence of tectal ce11 types is in-
265
TL
lLTLl
7.
NP VIS AP Ret NI NRMT
TEL (NDL) cTect TS NRS (Ret) dendrltk 0 1
r
-
I
dendrltc
~75 ,.uum (7 75-199ANn 200-3C0pm cl >300,um
norma1 1arge
number
of
0 fy
5c!o- 2cw 2500-10000 5000-20000
B
1-2 milhon
Fig. 9. Circuitry diagram of the goldfish tectum. Dendritic shafts are indicated by vertical bars and dendritic trees by horizontal bars. The latter are located as indicated in Fig. 7. Type XIV neurons have been drawn in a deviating way because of their peculiar properties (see section 3.1.4.4). Axons have been drawn as lines and are also located as indicated in Fig 7. In addition. the possibly efferent collaterals of some type XIV axons (see Fig. 6 and section 2.3.1) have been indicated. Neurons with obscure axonal properties (type 11, X1 and XV) have been omitted. (Supposed) synaptic connections are indicated by arrows. The dendritic extension, the dendritic density and the number of neurons per tectal half (according to Meek and SchellartiQ) are encoded as indicated left below in this figure. The cell groups indicated (a-f) have been discussed in sections 3.1.1.2 and 3.1.1.3 (see also Fig. 7).
cluded;
(c) (presumed)
synaptic
contacts
are indi-
cated by arrows; and (d) type XIV neurons have been drawn in a special way because of their peculiar role in tectal circuitry, which will be outlined below. 3.1.4.3.
Quantitative elaboration
ficity in tectaf circuitry.
of laminar speci-
The tectal circuitry diagram depicted in Fig. 9 reveals a complex pattern of intratectal connections. For an evaluation of the relative importance of these connections, a quantitative analysis is necessary. Such a quantitative circuitry analysis needs additional assumptions in the field of the laminar specificity hypothesis. For. interlaminar interrelations may be quantified on the basis of the characteristic numbers of synaptic contacts of the postsynaptic structures in the different presynaptic zones (Fig. 8). However, for precise quantification of intralaminar interrelations too few data are available. For example, in layer 5 the axons of about 200,000 retina1 ganglion cells terminate, but only 2500-10,000 type 111 axons and 500-2000 type VI1
axonsts*. The number of other types of presynaptic structures in this layer is unknown. The number of synaptic contacts made by each type of presynaptic strutture is also unknown, except for the number of retina1 fiber synapses, which has been estimated at about 30 milliont50 or more than 50 millionl@ (see section 2.1.4). For other layers a similar lack of quantitative data is encountered. In the absence of more precise data, the most simple ‘quantitative laminar specificity hypothesis’ has been adopted for a first approximation. This reads: Within a certain presynaptic
zone al1 types of presyn-
aptic elements distinguished
(as indicated
are presumed
in Fig. 8),
to make equa1 tota1 numbers of synaptic
contacts, the axons of type XZV excepted.
Assumptions regarding type XIV axons will be presented in the next section, and severa1 implications of the remaining part of this quantitative laminar specificity hypothesis will be discussed in more detail in section 3.4.
266 3.1.4.4.
Considerations
regarding
type XIV
rons. Type XIV neurons
constitute
ulation
from the remaining
of cells, deviating
ce11 types by their
large
frequency
a peculiar
neu-
based on the morphological
pop-
XIV axonsis2 as well as on the distribution of SS terminals in the tectum of Holocentrusl”6, which most
tectal
of occurrence
(about 1000 times more than other tectal ce11 types), their heterogeneity and their less strict dendritic and axonal lamination pattern (Fig. 5). These properties of type XIV neurons require separate quantitative assumptions
for their synaptic connections,
since the
quantitative laminar specificity hypothesis formulated above does not seem to be useful for these numerous cells. Fora quantitative analyses of tectal circuitry, two alternatives will be considered with respect to type XIV neurons. Both alternatives only apply to the average intratectal connectivity pattern of the tota1 population of type XIV neurons. For a more detailed analysis of possible subtypes too few data are available at present (see also section 3.4). First, the axons of type XIV neurons will be presumed to make exclusively synaptic contacts with type XIV dendrites, and not at al1 with other types of neurons. In other words, their axonal synaptic contacts are considered to be completely cellular specific. Although this assumption is probably too extreme, a certain degree of preference for mutua1 synaptic contacts is not unlikely for type XIV neurons, since both their dendrites and axons have smaller synaptic contacts than the remaining structures in the same layersis”. The major advantage of this presumed alternative is that it allows the analysis of the rather strictly organized circuitry of type I-X111 neurons. The results of this analysis, in turn, can be used as a basis for evaluation of the influente of type XIV cells in tectal circuitry. It should be noticed that this alternative does not imply that other axons would not contact type XIV dendrites. These contacts are presumed to follow the rules of the quantitative laminar specificity hypothesis formulated above. The second alternative that will be considered implies complete absence of cellular specificity for type XIV axons. Their synaptic contacts are now presumed to be laminar specific with the following quantitative elaboration: axons of type XIV cells are supposed to constitute 50% of al1 contacts in layer 5 and 516; 25% of al1 contacts in layer 415; 75% of al1 contacts in layer 4; 33% of al1 contacts in layer 314 and 50% of al1 contacts in layer 3. As is outlined in detail in the appendix (section 7.2), this distribution is
probably
characteristics
of type
are for the major part constituted
by type
XIV axons (section 2.2.2). Thus, with respect to the distribution of type XIV axon terminals, this condition represents
the most plausible
ent. However,
it is extreme
estimation
in presuming
at pres-
no cellular
specificity at al1 for type XIV axon terminals (see above). Consequently, the two alternatives to be considered for type XIV represent two extremes, somewhere in between of which the reality may be expected. Details with respect to both of these conditions are presented in the Appendix (section 7). 3.2. Calculation
of the connectivity
index
and the
connettive importance
On the basis of the starting points outlined above both a qualitative and quantitative structural analysis of tectal circuitry is possible. The quantitative part of this analysis will be performed in terms of connectivity index and connettive importance, which will be defined and explained in the next paragraphs.
Connectivity diagram and numbers of contacts
-
b
____J
r
c
-15orz=!=l
c
I y(l)~O50(b)+0.20(1)+0.3O(c) y (2)=040(a)+0.25(b)+O
Connectivity index
Connectlve
~ r(l)=0.63(B)+O37(Cl
‘mportance
i
r(2)=040
a
35 (1
)
CA)+ 0.47(B)+O.f3(C)
b
c
-100%
1
A
B
C
4100%
Fig. 10. Some quantitative connectivity parameters, iliustrated by a simple (hypothetical) circuit. For definitions, calculations and details, the reader is referred to sections 3.2.1 and 3.2.2.
267 3.2.1, Connectivity index Connectivity indices are meant to indicate the relative contribution of different types of presynaptic elements to the tota1 population of receptive synaptic contacts of a ce11type, They represent the ratio between the number of contacts of each type of presynaptic element with a particular ce11type and the tota1 number of receptive contacts of that ce11 type. TO take an example (see Fig. 10): if neurons of ce11type 1 have on average 250 contacts with afferents of type b, 150 contacts with afferents of type c and 100 synaptic contacts with axons of neighboring type 1 neurons, the connectivity index (y) of ce11type 1 with respect to type b equals 250/500 = 0.5 or 50%. In formula: y(l,b) = 0.5 The formulae with respect to type b and type 1 axons are: v(l,c) = 0.3 $,l)
= 0.2
a summarizing formula is: y(1) = 0.5(b) + 0.3(c) + 0.2(l). The values calculated can also be presented in a matrix (Fig. 10). The connectivity indices of the tectal ce11types, as calculated in the appendix, are presented in Table 111, which represents a matrix of tectal circuitry. The procedure followed may be summarized as follows (for details the reader is referred to the appendix): For type 1,111, VI, X11, X111 and XIV, the relative contribution of presynaptic structures occurring in different presynaptic zones is estimated on the basis of the number of contacts on the ce11types in these different presynaptic zones (see Fig. 8). For type IV, V, VII, VIII, 1X and X, where these numbers of contacts are not available, the relative contribution of presynaptic structures occurring in different presynaptic zones is estimated on the basis of the extension of their different receptive components in the different presynaptic zones (see Fig. 5), which supposes a homogeneous synaptic density along these components, The relative contribution of presynaptic structures occurring in the same presynaptic zone is approximated on the basis of the quantitative laminar specificity hy-
pothesis formulated in section 3.1.4.3. This implies an equa1 ~ont~bution of al1 pres~aptic structures in a single presynaptic zone, except for axons of type XIV. The connectivity indices of the tectal ce11types are calculated for both altematives considered with respect to type XIV axons, which means at first without taking account of the influente of type XIV axons, and secondly by assuming an extremely large influente of type XIV axons (see section 3.1.4.4). 3.2.2. Connettive importance Each tectal neuron can be considered as a relay station in the multiple pathways between tectal afferents and efferents (see Fig. 9). TO be able to evaluate the significante of the tectal ce11types in this respect, a parameter has been calculated which quantifies the tota1 set of mono-, bi-, and multi-synaptic connections between afferents and ce11types, This parameter has provisionally been termed ‘connettive importante’ since it indicates the importance of afferents exclusively on the basis of quantified connettive relations and should be distinguished from conceptions like electrophysiological, neurochemical, or functional importance. Mathematically, eonnective importances are calculated by algebraic solution of the connectivity indices-formulae in terms of afferent input. This solution is possible on the basis of the principle that, because of the integrative properties of neurons, the connectivity index of a certain ce11type represents, in fact, the connectivity index of each axonal synaptic contact of that ce11type. TO take an example (Fig. 10). If y(l) = 0.5(b) + 0.3(c) + 0.2(l), substitution of y(l) for (1) leads to the following result: y(l) = 0.5(b) + 0.3(c) + 0.2 y(l), or y(l) - 0.2 y(1) = 0.5(b) + 0.3(l), or I’-(l) = 0.63(B) f 0.37(C). TO distinguish them from ~onne~tivity indices, connective importances are indicated by capitals (IY, B and C instead of y, b and c). The formula just calculated means that the connettive importance of afferents of type b for ce11 type 1 is 63% (I(l,B) = 0.63) whereas the connettive importance of afferents of type c for ce11type 1 is 37% (I(l,C) = 0.37). TO
268 take ce11type 2 of Fig. 10 as another example: If y(2) = 0.40(a) + 0.25(b) + 0.35(l), substitution of I( 1) for (1) yields the following result:
type XIV neurons
Together y(2) = 0.40(a) + 0.25(b) + 0.35 I(l), y(2) = 0.40(a) 0.37(C)}, or
+
0.25(b)
+
3.1.4.4).
The calculation
with Fig. 9, these matrices provide the ba-
sis for the analysis of tectal circuitry to be presented
or
0.35
(section
of tectal connectivity indices and connettive importances is outlined in detail in the appendix (section 7).
(0.63(B)
+
in the next section. 3.3 Anafysis of tectal circuitry
y(2) = 0.40(a) + 0.25(b) + 0.22(B) + 0.13(C), or In this section
I(2) = 0.40(A) + 0.47(B) + 0.13(C).
The
connettive
importance
just
defined
the tectal circuits
involved
in the
processing of the 4 main streams of tectal input are analyzed on the basis of the starting points, diagram may
be
called overall connettive importance since it is related to mono-, bi-, and multi-synaptic connections. This overall connettive importance may be split up into direct and indirect connettive importance. The direct connettive importance indicates the relative contribution of direct, monosynaptic afferent contacts to the contacts of each ce11 type, and equals the connectivity index of the ce11types with respect to the afferents. The indirect connettive importance indicates the importance of bi- and multi-synaptic connections between afferents and ce11types, and equals the differente between the overall and direct connettive importance. A suitable way to present quantitative aspects of circuitry is a matrix with both connectivity indices and connettive importances. From such a matrix the numerica1 importance of the different types of connections of a ce11 type can be seen as well as that of the direct and indirect connections of the afferents. TO take ce11 1 of Fig. 10 as an example: the direct connettive importance of afferents of type b is 50% (= connectivity index); the overall connettive importante is 63%, and consequently the indirect importante is 13%. Furthermore, it can be seen whether the connettive relations between afferents and ce11 types are exclusively monosynaptic (OCy=I; e.g. connections between a and 2 in Fig.10). exclusively bi- or multisynaptic (O=y
(Fig. 9) and matrices (Table 111) presented. First, tectal circuitry will be described without consideration of the axons of celi type XIV (i.e. the first alternative for type XIV, see section 3.1.4.4 and the Appendix). This part of the analysis is illustrated by Figs. 11-14. The design of these figures is basically similar to that of Fig. 9, with the following modifications: (1) the cells have been placed in a rough sequence of importante with respect to their significante for the type of input under discussion; (2) cells which are not involved in a particular circuit have been omitted; and (3) the connettive importance of the type of input discussed is presented. Secondly, the results of this analysis will be compared with the second alternative type XIV (see section 3.1.4.4 and the appendix), which imphes an extremely large influente of this cell type. The comparison of both alternatives for type XIV is illustrated by Figs. 15 and 16. 3.3.1.
Tectal circuitry involved
in toral input proc-
essing
(i.e. afferents of the torus fongito layer 7 and terminate exclusively on the apical dendrites of type 1 neurons (Fig. 11). Although type 11 neurons have processes in layer 7 as well, there is good evidente for Eugerres and Holocentrus that these processes are presynapticr”6.22Q64. Their small number in the tectum of cyprinids might explain why these structures have not been observed in the goldfishI@ and the carp31,1”3. Judging from the distribution of synapses on type 1 neurons, the direct connettive importance of toral input for these neurons is as large as 90%. The axons of type 1 neurons terminate specifically in layer 3/4. where severa1 types of postsynaptic structures occur, including the basa1 dendritic tree of type VIII. type Tora1 afferents
tudinalis), are confined
269 TABLE 111 Two connectivity matrices of the goldfish tectum, based on the starti@ points and methods outlined in section 3.1 and 3.2, respectively
Matrix A holds for the first alternative assumed for type XIV axons, matrix B for the second alternative (see section 3.1.4.4.). The procedures and calculations applied are detailed in the appendix (section 7). A Ce11
Type of axon
tvpe
vis
tor
3 42 33 33 17 13
90
1
111 IV
VII VIII 1X V‘t V, XIV VI X X11 X111
Type of input te1
deeo
Os
1
III
IV
VI1
VIII
0,
0, 29
2
0, 29
2
7 13 20
22a
33 5a
30 13 6 6
20 7 13
13 20 33 9a
7
33 27 17 13
v,
XIV
v,
0,
0,
13 10 50
13 10 50
VIS
TOR
TEL
DEEP
7 91 74 77 47 39 39
92 4 12 11 25 29 29
61
13
2 5 14 12 28 32 32 50 17
50 10
64 39 26 17
17 29 13 8
19 32 20 21
33 4a
15a
7 39 50
33 27 17 13
IX
20 3 4
4 3
7a
3 13 2 3
15n
7 4 3
7a
3 13 2 3
8a
25 10 15 4
Sa
25 10 15 4
2a
100 (l-a)
4 8 + 100%
connectivity index t
t
41 54 + 100%
‘L annective importance f
B Ce11
Vi.?
1
111 IV VI1 VI11 1X V, V,
Type of input
Type of axon
2 28 25 23 13
10
tor
te1
90
0,
1 03
IV
III 03
14 3
8
8 13
13 17
17 8
XIV
13
3
VI X x11 X111
26 10 3 3
13 4 7
t
deep
37 46
3 13 2 3
1
VII
03
1x
v,
V3
XN
VIS
TOR
TEL
DEEP
17
3 43 25 30 40 38 75 50
6 73 70 70 54 48 55 34
91 6 8 8 15 19 10 5
1 8 10 10 18 22 14 27
1 13 12 12 13 12 21 33 22
1
14 25 20 13 10
3
25 20 13
10
8
5
8
3
3 10 1 2
3
2 1
VIII
2 1
connectivity index t
1X and type X neurons, ce11 bodies of type 1X and type X neurons, and dendritic shafts of type X11, type X111 and type XIV neurons (Fig. 11). Some of the type XIV neurons may have considerable dendritic trees in this layer as well. Thus, the most important candidates for further processing of toral input are type VIII, type 1X and type X neurons. Type VI11
3
3
3 13
3 13
5
2
2
1
44
57
9
12
3
10 1
6 3 4
6 3 4
2
1
1
50 38 37 2 28 4 -+ 100%
68 48 34 26
7 19 7 6
10 22 11 13
15 12 48 54 + 100%
?- connettive importance f
and type 1X neurons are interneurons, which may bring about an upward transport of information from layer 314 to layer 4/5 and 4, respectively. From layer 41.5,a further upward transport to layers 5 and 516 can be effected by the axons of type VII neurons. At this tectal level, however, the connettive importance of toral information is rather low (about lo%, Fig. 11).
270
tor 6
--
The i
_ -
connectlve
Importance toral
XIV
of
Input
Fig. Il, Tectal circuitry involved in the processing of input from the torus longitudinalis. The tectal neurons and their dendrites, axons
and (presumed) synaptic contacts are visualized as explained for Fig. 9. The neurons have been placed in a rough sequence of importante with respect to the type of input presented. The connettive importance of this input for the tectal cell types is indicated by the interrupted or black lines drawn as continuations of the tectal axons. These lines encode the connettive importance as calculated in the appendix for the first alternative (see Table MA). Completely black lines indicate a connettive importance of 100%; white lines would indicate a connettive importance of 0%. For further details, the reader is referred to section 3.3.1.
A great number of synaptic contacts between the axons of type XIV neurons and the other ce11types (the second alternative for type XIV, see section 3.1.4.4) would decrease the connettive importance of toral signals in tectal circuitry. since type XIV neurons are in general no important targets for type 1 axon terminals (Fig. 15 and 16). The most direct route from the toral input in layer 7 to tectal output is a two-synaptic pathway via type 1 and type X neurons. The connettive importance of toral input for type X neurons, however, is not very large (about 30% in the first alternative). The other tectal efferent neurons seem to be influenced to a still lower extent by toral signals, while this influente is provided mainly by pathways involving 3 or more synapses (Fig. 11). SO. the circuitry involved in the processing of toral information in the tectum has a number of peculiar
characteristics. No tectal efferent neuron is directly contacted by toral afferents. Al1 toral input is received by one specific type of interneuron, which conducts toral information downwards to one specific layer (layer 314). In this layer, again interneurons constitute most of the postsynaptic structures, which, in turn, effect an upward transport of toral information. Only one efferent neuron (type X) has dendrites specifically in layer 314, but the connettive importance of toral input for this efferent ce11type is not larger than 30%. Consequently, there seems to be a remarkable discrepancy between the large amount of toral input to the tectum and the low degree of representation of this input in the tectal outflow. 3.3.2.
Tectal circuitry involved in visual input proc-
essing
As described
in section
3.1.1.1,
the layers 5/6, 5
271 d
b --AA. Ill
IV
VII
VIII
IX
C
a
e
v
I
XIV
f VI
x
XII
XIII
_-----Il1
NP AP vis Ret
-___--
i
V,, vis
_---------_----_ ------
NRMT 4
-
3
1
Il"'
I
I
I
’
:>
’
’
;
:
0
I i
Ii
-
-
XIV
-
-
XIV
-
-
XIV lV
-
-
-
-
-
VIII ,X v4 I
XIV
The connettive importance of visual Input
I,
Fig. 12. Tectal circuitry involved in the processing of visual input. For explanation and details, the reader is referred to the legends of Figs. 9 and 11 and to section 3.3.2.
and 4/5 receive visual input by way of the retina1 fibers as well as by afferents from the nucleus pretectalis, the area pretectalis and the nucleus isthmi. Although these layers may also contain a small number of non-visual afferents (section 3.1.1. l), for the sake of simplicity the input of layers 415, 5 and 516 (the SGFS) will be considered as 100% visual in the following discussion. The visual afferents most probably make synaptic contacts with al1 tectal ce11 types except for types V and XV, the only ce11 types without dendrites in the visual afferent layers (Fig. 12). Type 111, IV and VI1 neurons may be considered as specific visual interneurons, since they have their postsynaptic structures exclusively in the visual afferent layers. They may also process some non-visual information by way of contacts with the axons of type VI11 neurons (type IV and VII) or of type VI1 neurons (type III), but this is probably only a low percentage (Fig. 12). The axons of type 111 and of type VI1 neurons terminate in layer 5 or 5/6, where no other interneurons have axon terminals, except type XIV, which will be discussed below. This stresses the importance of this layer for visual information proc-
essing, since not only the visual afferents appear to terminate in layer 5, but also the axons of the visual interneurons type 111 and type VII. Type IV neurons have their axon terminals in layer 4/5. Apart from the visual afferents, layer 4/5 also contains the axons of type VI11 neurons, which may provide some non-visual information from deeper tectal levels (Fig. 12). This suggests that layer 4/5 is somewhat less ‘visual’ than the remaining part of layer 5. Layers 4 and 314 may only receive ‘indirect’ visual input via the axons of type 1X and type 1 respectively, which bring about a downward transport of visual information. The connettive importance of visual input for type 1 cells is only about 5%, whereas this value for type 1X neurons is about 40% (Table 111). The connettive importance of visual input for type XIV neurons is about 60% under both alternatives assumed (Table 111). The main effect of a large number of contacts between axons of type XIV neurons and dendrites of other cell types would be a strong downward flow of visual information from SFGS to SGC, where type XIV axons have many terminals (Figs. 7 and 12). This, in turn, would in particular en-
272 large the influente of visual information on the tectal efferent neurons (Table 111and Fig. 16). Most likely,
al1 types of efferent
tectal
neurons
have direct synaptic contacts with visual afferents (Fig. 12). For type VI and type X11 this has been confirmed in the electron-microscopei49.
According
to
the present analysis type VI neurons represent the most ‘visual’ efferent neurons, since they are located in the visual afferent layers (Table 111 and Fig. 12). The position
of the dendritic
trees of type VI cells
raises some questions, however. Ultrastructural studies revealed that their apical dendritic tree, preferentially
located in the superficial
part of layer 6, is
not contacted by retina1 fiberst@J50. Since interneurons equally have no axon terminals in this region, except for some type XIV neurons, it is not clear which presynaptic structures make contacts with the apical dendritic tree of type VI neurons. Possible candidates are the retina1 terminals that constitute the thin superficial band of the retino-tectal projection (Fig. 4), which then should have ultrastructural characteristics deviating from the bulk of the retinotectal fibers (section 2.2.2). Other candidates are fibers from the nucleus pretectalis, area pretectalis, nucleus isthmi or nucleus or the rostral mesencephalic tegmentum, which, then, should terminate specifically in the superficial part of layer 6. It is important to notice that Laufer and VanegaG have described large axons at this tectal leve1 which do not degenerate after eye-enucleation. Although Laufer and Vanegasi considered these fibers as tectal efferents, it is equally conceivable that they constitute non-retina1 afferentslsl. Disregarding these uncertainties, the apical dendrites of type VI neurons are assumed to receive 100% visual input (Fig. 8). The basa1 dendritic tree of type VI neurons, preferentially located in layer 4 just below layer 4/.5, also makes no synaptic contacts with terminals identified as retina1 fibersi@J50. Although it might be possible that the axons of type IV, type VI1 and type 1X neurons make some synaptic contacts with the basa1 dendritic tree of type VI, most probably type XIV axons make most of the synaptic contacts on this dendritic tree. This would be in line with the high frequency of occurrence of type XIV axons in this layer and with the small size of the synaptic contacts of the basa1 dendrites of type VI cellst50. This implies that, at least for layer 4, the second alternative assumed for
type XIV seems to be more realistic than the first one (see section 3.1.4.4). The connettive efferent
importance
of visual input for the
ce11 types X, X11 and X111 is at least 40%,
25% and 15%, respectively (Table 111). Most of the visual information reaches these neurons via bi- or multi-synaptic pathways (Table 111 and Fig. 12) although al1 these tectal efferent neurons constitute monosynaptic pathways between visual input and tectal output as well. The percentages enumerated increase with increasing type XIV neurons
involvement
in tectal circuitry
of the axons of (Table 111 and
Fig. 16). Summarizing, the characteristics of the circuitry involved in visual input processing in the tectum are about the contrary of those of the circuitry involved in toral input processing. Whereas toral input is received by a single type of neuron, visual input is directly provided to almost al1 tectal neurons, and whereas toral afferents do not contact efferent neurons directly, al1 efferent neurons have direct contacts with visual afferents. A further contrast between toral and visual input processing is the simplicity of the toral afferent layer 7 (only one type of presynaptic element and one type of postsynaptic element) and the complexity of the visual afferent layer (layer 5 and its boundaries), where at least 9 types of presynaptic elements and 13 types of postsynaptic elements are involved in tectal circuitry. A further characteristic of visual input processing is the occurrence of severa1 types of visual interneurons which make synaptic contacts close to the contacts made by the visual afferents, an arrangement not realized for the toral input. Visual input seems to have a relatively high influente on the tectal outflow, whereas the toral influente on this outflow seems to be low (Fig. 16). 3.3.3.
Tectal circuitry involved in telencephalic
input
processing
Tectal circuitry involved in the processing of telencephalic input resembles to some extent the circuitry involved in toral input processing, since telencephalic afferents terminate at the same tectal leve1 (layer 3/4) to which type 1 axons convey their toral information (cf. Figs. 11 and 13). Accordingly, just as has been discussed for toral input (section 3.3.1), some part of the telencephalic input to layer 314 is trans-
273
&A, IX
~_
VIII
v
IV
VII
f
a
b
c
d
Ill
I
x
XIII
e XII
VI
XIV
7
6
-
Tel
.
.
:eI
_------
v3 -
-
XIV
2
1
The connectlve importance of telencephalic input
Fig. 13. Tectal circuitry involved in the processing of telencephalic input. For explanation and details, the reader is referred to the legends of Figs. 9 and 11 and to section 3.3.3.
ferred upward via the axons of type VIII, 1X and VI1 (Fig. 13), and the most important type of efferent neuron for telencephalic information is probably type X. A large influente of type XIV neurons would likewise decrease the influente of telencephalic input on the tectal outflow (Fig. 16). The main differences between the circuitry for toral input processing and that for telencephalic input processing concern the involvement of type 1 neurons and layer 7 in toral information processing, and the fact that telencephalic afferents are probably less strictly concentrated in layer 3/4 than the axons of type 1 neurons. Consequently, in contrast to the situation for toral input, there does exist a monosynaptic pathway from the telencephalic input to the tectal output via type X neurons and probably also via type X11 and type X111 neurons. Of the latter two, type X111 neurons might be the most important ones in this respect, since their dendrites in layer 3, preferentially located just below layer 3/4, might well have synaptic contacts with telencephalic afferents
(Fig. 13). Type X11 neurons receive most of their telencephalic input via contacts of their dendrites in layer 4 with axons of type 1X. However, for the same reasons as discussed above for the dendrites of type VI neurons in layer 4, type XIV axons probably constitute most of the presynaptic elements of the dendrites of type X11 neurons in layer 4. This would reduce the telencephalic influente on type X11 neurons substantially (Fig. 16). The ratio between telencephalic and toral input in layer 3/4 is not clear, since the number of telencephalic afferents, as well as the number of contacts made by these afferents is unknown. Under the conditions assumed by adopting the quantitative laminar specificity hypothesis (section 3.1.4.3), telencephalic input seems somewhat more important than toral input because of the involvement of type 1 neurons, but this is merely hypothetical. A striking point, however, is the competing character of the telencephalic and toral (i.e. cerebellar) afferent systems in tectal circuitry. The larger the influente of either one, the smaller
274 C
,,--\ V
.._
, cXIII
f
~_L_ XIV
~\ Xll
e
~.
_
XIV (‘large’)
,
9 -J\_., xv
7
6
5 XIV
XIV XIV (‘large’) XIV
----
v3
3
XIV
NRS c. iecr.y (RetI
‘deep’
2
1
The connettive of ‘deep’ tectal Input
’ 1
’ ’
! importance
’ ’
:
I
’ ’
I i
1
]
I
I
i l
!
_j
Fig. 14. Tectal circuitry involved in the processing of ‘deep’tectal input. For explanation and details, the reader is referred to the legen& of Figs. 9 and 11 and to section 3.314. -
the influente of the other will be, since both have to be integrated to a large extent by the same postsynaptic structures. It should be mentioned that afferents from the mesencephalic nucleus dorsolateralis also terminate in the SGC. For the sake of simplicity, however, these have been left out of discussion. The importante of this afferent system is obscure at this moment. The same holds for the few retina1 fibers terminating at this tectal level. 3.3.4. Tectal circuitry involved in deep tectal input proces~ing The so-called ‘deep’ tectal afferents, including fibers from the contralateral tectum, the torus semicircularis, the reticular formation, the retina and presumably severa1 other systems (see section 3.1.1.1), terminate almost exclusively directly on the large tectal efferent neurons, type X11 and type X111, which
have large dendritic trees in the deep afferent layers 2 and 3 (Fig. 14). Interneurons hardly occur in these layers, except for some type V neurons in layer 3, and the dendritic shafts of type XIV neurons. SO, in this respect the circuitry involved in deep tectal input processing seems to be the opposite of the circuitry involved in toral input processing, since deep tectal afferents terminate predominantly on efferent neurons, whereas toral afferents terminate exclusively on interneurons. Visual and telencephalic input processing take an intermediate position in this respect, since visual and telencephalic afferents terminate on both intemeurons and efferent neurons. A large number of contacts of type XIV axons with al1 tectal ce11 types would result in a substantial upward transport of deep tectal input to layers 4 and 5 (Fig. 15) and would increase the influente of deep tectal input on tectal interneurons as well as on efferent tectal neurons (Fig. 16).
275 without
1
tor
influente
fi
of type XIV
/-%
vis
......................** .... ~.?.%:::>:.Y.-* :.:~.:.:.:.:.:~.:.:.:.:.~ ...........I.. %%%z%%-::. ............................
tel
deep
influente
tor
’
vis
A
of
type
--~ tel
XIV I deep
7
*:z::::::.V.V:. m............. .~~\:;%:%~~~%~* ..zCzxx.~~~~~ %%%%V~.f’.‘.‘.‘.: 6
.::: : :
1..
:.
..:.
5
::
..’
:
.’
_:
:
:.::..
:
::..:
...:::. 4 .,
:.:
El
50% -_OY_
. . .:
:. :...
.,.,
..
nndirect connectlve Importance
; .:
3
2
Fig. 15. The direct and indirect connettive importance of the main types of tectal input in the different tectal layers. Part A holds for the first alternative and is based on formulae 14a-21a and 14b21b (see appendix, section 7); part B holds for the second alternative and is based on formulae 14c-21c and 14d-21d. For further details and discussion, the reader is referred to the text (section 3.3.5).
The circuitry involved in deep input processing in the tectum may, however, be more complex than suggested above for two reasons. Firstly, type XV neurons, a population of neurons with dendrites predominantly in layer 2 and 3, are not included in the preceding discussion because their axonal properties are obscure. Nevertheless, they will be involved in the deep input processing because of their dendritic properties. A portion of type XV neurons might well be interneurons with axons terminating in the tecturn, but others give rise to tectal efferents, as indicated by Romeskie and Sharmazm. Secondly, in particular the so-called ‘large’ subtype of type XIV neuronsls* may have considerable dendrites in layer 2 and/or 3. Consequently, these cells might have a still more important function in the integration of visual and ‘deep’ tectal input than the bulk of type XIV neurons (Fig. 15). Both Meek and Schellartl52 and Romeskie and Sharma*m consider these large type XIV
neurons cells . 3.3.5.
as interneurons,
just as the other type XIV
The connettive importance of tectal afferents in
the different tectal layers In the previous sections of this chapter the circuitry involved in the processing of the 4 main streams of tectal input has been analyzed. From this analysis the following stratification pattern emerges with respect to the connettive importance of the different types of tectal input (Fig. 15; for calculations, see the appendix, section 7). The 4 levels of distinct tectal input (see section 3.1.1.1) remain clearly distinguishable. However, in the interjacent layers a considerable mixing of the different modalities may be brought about by tectal interneurons, in particular in layer 3 and in layer 4 (Fig. 15). Only the boundary between layer 7, the toral input layer, and layer 6, the visual input layer is very sharp. Consequently, layer 7 can
276 be considered exclusively as a relay station for toral (i.e. cerebellar) input to the tectum, with no other re-
drites in layer 314).
lations with the deeper tectal layers than via the api-
Type 111, IV and VII neurons may be considered as visual interneurons, since the direct as well as the in-
tal dendrites of type 1 neurons. In this respect, type 1 neurons could equally well be considered to be tectal
direct connettive importance of visual input for these neurons is relatively large. Type IV and VII have
afferent
very extensive dendrites which make them suitable fora function in spatial interaction and integration of
elements
as to be tectal interneurons.
other sharp boundary 2 and layer
can be observed
1, the stratum
contains exclusively tic contacts.
between
periventriculare,
celi-bodies
Anlayer which
with very few synap-
The remaining part of the tectum, layers 2-6. is constituted by closely interrelated layers with only gradua1 transitions
from one layer to another.
The
superficial part, layers 6 and 5. is predominantly involved in visual information processing (Fig. 15), whereas the deep layer 2 is almost exclusively involved in ‘deep’ information processing. In layer 3 a considerable mixing of visual and ‘deep’ input might occur by means of the action of type XIV neurons (cf. Fig. 15A, B). In layer 314, just in between the deep. predominantly non-visual and the superficial, visual layers, the telencephalon and the cerebellum exert their influente, the latter after interposition of the torus longitudinalis. In layer 4 some degree of mixing between visual, telencephalic and toral information is realized. The connettive importance of visual input in this layer strongly depends on the involvement of type XIV cells (cf. Fig. 15A, B). Layer 41.5is remarkable because of the large extension of severa1 dendritic trees, suggesting an important function in spatial integration of visual input. The overall pitture of the connettive importance of the 4 main types of tectal input in the different tectal layers as presented in Fig. 15 clearly suggests that the laminar organization of the tectum is primarily relevant for multimodal integration. 3.3.6. The connettive relations of the tectal ce11types The connettive relations between the 4 main types of tectal afferents and the tectal ce11types, as numerically presented in Table IH, are visualized in Fig. 16 and have been analyzed in detail in section 3.3.1.-3.3.4. In summary, the following may be noticed. Type 1 neurons may be considered as the tectal afferents for toral (cerebellar) input. In addition, they may process some amount of visual input (via dendrites in layer 5) and telencephalic input (via den-
visual signals. The location of their dendrites in layer 4/5 may also indicate a function in integrating visual input with some amount of telencephalic and toral input, which reaches layer 415 by means of the axons of type VI11 neurons.
The bistratified
character
of type
VII may suggest that this type of neuron integrates more aspects of visual information than type IV and type 111 neurons. Type 111 neurons seem to be the most visual interneurons (Fig. 16) which is also suggested by their relative high percentage of direct contacts with retina1 fibersis”. Since their dendrites are not SO extensive, they are more likely involved in tempora1 aspects of visual Signa1 processing than in spatial aspects. The bulk of type XIV neurons can also be considered as visual interneurons (Fig. 16), although for some subtypes other modalities may be important as well. Their large number with respect to the number of retina1 and other afferents and their large variability make this ce11 type suitable for a number of specialized functions in Signa1 processing. Type V neurons, indicated as non-visual interneurons in Fig. 7, constitute a heterogeneous population, receiving different types of input depending on their position in layer 3 or 4 (Fig. 16). Their morphology suggests a function in spatial interaction between different tectal regions. Type XV might represent a second type of non-visual interneuron, involved in the processing of deep tectal input. Type VI11 and 1X probably integrate 3 different types of input: visual, telencephalic and toral input. Visual input seems the most important modality for type VIII, which has substantially larger dendrites in layer 415 than in layer 3/4, whereas for type 1X the toral/telencephalic input may be more important. This tendency is stressed when the position of the ce11 body and the origin of the axon is taken into consideration (see section 3.4). Among the efferent neurons, type VI neurons are probably specialized to transmit visual information beyond the tectum. Their receptive surface may integrate al1 aspects of visual information processing
277 “without” TOR VIS
type XIV TEL DEEP
VIS
with type XIV TOR TEL DEEP
B
Fig. 16. The connettive importance of the main types of tectal input for the tectal cell types, visualized by means of surface areas. Black parts indicate the direct connettive importance, grey parts the indirect connettive importance, and the total surface of the squares indicates the overall connettive importance. The size of the surface areas encodes the values calculated in the appendix and presented in Table 111as arranged in 10 classes: l-2,3-6,7-12, 13-20,21-30,31-42,43-56,57-72,73-90 and 91-100% connettive importance. Part A holds for the first alternative, part B for the second one. For further details the reader is referred to the text (section 3.3.6).
from layer 6,5 and 4. Type X neurons seem to be important for transport of toral and telencephalic information out of the tectum, integrated with visual information. The large efferent neurons of type X11 and type X111 may integrate information from al1 tectal input systems. For type X111 neurons, however, the deep tectal input seems to be dominant (Fig. 16). The importance of deep afferents is stressed by the
location of the ce11body and axon origin of type X111 neurons in layer 2. For type X11 neurons visual input is relatively more important than for type X111 neurons. The ratio between the influente of the distinct types of tectal input on type X, X11 and X111 depends to a large extent on the influente of type XIV neurons (see Fig. 16). The large degree of connettive differentiation as
278 shown in Fig. 16 suggests that the tectal ce11types can be considered as elements which each receive a characteristic sample out of the multimodal information available in the different presynaptic tectal zones.
proximation, it is clear that insight in tectal circuitry will be greatly improved when more becomes known with respect to their degree of cellular specificity, their number of axon terminals, the qualitative and quantitative characteristics of various subtypes, their
3.4. Critica1 evaluation of the framework presented
importance volvement
The analysis presented is not meant as a definite description of tectal circuitry - for this too little in-
(section 2.3.2).
formation
is available
at present -
but as a concep-
as origin of tectal efferents and their inin various extratectal feed back loops
The framework presented may be refined in several ways. The first one is to consider not only the num-
tua1 framework. This framework is constituted by a connectivity diagram (Fig. 9) and two matrices of
ber of synaptic contacts, but also their degree of symmetry, size and position. Incorporation of these addi-
connectivity indices and connettive ble III), and is primarily designed
tional synaptic characteristics in the connectivity matrices may be expected to have the following conse-
importances (Tato summarize the
structural data available in such a way that optimal comparison and integration with physiological data may be established. In particular Figs. 11-16 subserve this purpose. The framework constructed. however, is also useful to define precisely where and how it should be reinforced, refined and filled in to arrive at a more precise and definite description of tectal circuitry. In this respect the following may be noticed. Reinforcement of the frame should primarily be achieved in the field of the intralaminar interactions between presynaptic elements. These have been approximated by the rather plausible concept of laminar specificity, but the validity of this concept should be tested further. Only when the intralaminar distributions of presynaptic elements on the receptive surfaces of the different ce11 types have been analyzed qualitatively as well as quantitatively, a more definite mode1 of tectal circuitry comes into prospect. It should be noticed however, that adoption of the concept of laminar specificity is of rather low importance for the conclusions presented with respect to the multimodal integrative capacity of the tectum. This type of integration mainly depends on inter- (and not intra-) laminar interrelations, and it has been discussed that interlaminar interrelations are determined by the characteristic postsynaptic properties of the tectal ce11types. A second field of reinforcement of the frame to be mentioned concerns type XIV neurons. The function of this large population of neurons has been approximated by assuming two extreme alternatives for the intratectal connections of the ‘average’ type XIV neurons. Although this appears useful for a first ap-
quences. With respect to the degree of symmetry of synaptic contacts, it may readily be assumed that symmetrical synapses (with pleomorphic vesicles) are inhibitory, and consequently must get a negative sign in the connectivity matrices, whereas asymmetrical synapses (with round vesicles) are excitatory. Further, synapses with large contact zones most likely have a larger influente than synapses with small ones. This tends to enhance the direct connettive importance of afferents (see Meekis”, Table 2), whereas the connettive importance of type XIV neurons in tectal circuitry would be reduced, since their axons have relatively small contact zonesis(J. With respect to the position of synapses, it may be expected that contacts close to the axon hillock have a larger influente than more dista1 contacts. In general, this tends to enhance the functional differentiation between the tectal neurons as suggested by Fig. 16. Comparison of type X11 and X111, e.g., reveals that the axon hillock of type X111 is located in layer 2, which tends to enhance the connettive importance of deep tectal input for type X111. In contrast, the axon hillock of type X11 is situated more close to the visual layers 5 and 6. Equally. comparison of the position of the axon hillock of the related ce11 types VI11 and 1X in layer 415 and 314 respectively enhances the importance of toral and telencephalic input for type 1X. However. the position of synapses may also oppose their numerica1 properties. For example, the few retina1 fibers that contact type 1 neurons are close to the axon hillock. which tends to enhance their connettive importance for type 1 at the expense of that of the numerous toral afferents. Likewise, the relatively few retina1 fibers that terminate
279 in layers 3/4 and 2 are situated
close to the axon hill-
ock of the efferent type X11 and X111 neurons, might enlarge
the importance
tectal outflow. In spite of their relevance, characteristics mentioned rated in the connectivity reasons.
Firstly,
of visual input for the the additional
synaptic
have not been incorpomatrices for the following
the size and degree
might only incidentally
which
be incorporated,
of symmetry since for
most types of connections in this respect no data are available at present. Secondly, it is still obscure which parameters should be exactly considered: is it the diameter, the circumference or the surface of the contact zones, or should one consider the complete apposition zone? Should one consider the distante to the axon hillock, its root, its square or something else and how should one incorporate the diameter of dendrites and the occurrence of spines? How should the large number of contacts be taken into account which are intermediate between clearly asymmetrical and symmetrical contacts, and what is the relation between these parameters and types of neurotransmitters? These are al1 questions pertaining to the interface of histology and physiology, and incorporation of some rather arbitrary structural factors would not facilitate, but rather obscure an integration of structura1 and functional data. Consequently, it seems at this moment most useful to base a first approximation of tectal circuitry exclusively on the number of synaptic contacts, and to postpone the incorporation of additional factors unti1 more structural and physiological data have become available. A large number of additional refinements of the framework may be mentioned. TO arrive at a more precise description of tectal circuitry, not only the 4 main types of tectal input, but each type of afferent should be considered separately; equally not only average characteristics of tectal neurons should be considered, but also variations and deviations. Further, more data should be obtained with respect to the axonal arborization pattern of severa1 interneurons, the synaptic properties of severa1 ce11 types, topographical variations, etc. Considering the tota1 set of refinements as well as reinforcements enumerated, it may be concluded that the framework constructed represents the most simple concept of tectal circuitry possible at present, since it considers only average structura1 characteristics and the most simple quantitative
laminar specificity concept, whereas it neglects possible variations, diviations, complications and specializations.
It is, consequently,
not a fina1 result,
starting point for further research. A definite filling in of the framework
but a
has to be
achieved by electrophysiological studies. Morphologica1 research, however, precise it may be, only demarcates
the potentialities
of circuitry.
tent and in which way these potentialities under
different
conditions
TO what exare utilized
may only be understood
by physiological research. In the next sections it will be explored to which degree such an integration of physiological
and structural
present for the teleostean
data may be achieved
at
tectum.
4. SURVEY OF PHYSIOLOGICAL
DATA
In order to facilitate comparison of the circuitry framework presented and tectal physiology, in the present section the relevant physiological data are briefly surveyed. This survey is predominantly devoted to single unit studies, with special attention to the localization and identification of the units recorded. An extensive list of physiological studies is presented in Table 1. 4.1. Tora1 inputprocessing Some electrophysiological aspects of the processing of toral input in the tectum have been investigated by Vanegas et al.264 in Eugerres and Holocentrus by means of electrical stimulation of the margina1 tectal axons and subsequent extracellular recording of the electrical events throughout the depth of the tectum. The results can be easily interpreted on the basis of the morphology of type 1 or pyramidal neurons, which are the only targets of margina1 axons31.103.106.131,149.150. According to Vanegas et al.264 the most important electrical events after stimulation of the margina1 fibers are: (1) spike propagation along these fibers with a conduction velocity of 0.20 or 0.16 m/s; (2) monosynaptic depolarization of the apical dendrites of type 1 or pyramidal neurons; (3) an attive current sink at the leve1 where the apical dendrites of type 1 neurons converge to the dendritic shaft; and (4) an activation of the axon terminals of type 1 neurons in layer 314. It is remarkable that this tectal afferent system, which receives its principal in-
280 put from the cerebellum,
has many
group terminates
physiological
more superficially
than the more
characteristics strongly reminiscent of that part of the brain, particularly of the parallel fiber-Purkinje ce11
slowly conducting group. Histological verification of the recording site showed that their regions of termi-
system*@. Sajovic
nation roughly correspond respectively*W62. Current
and LevinthaPos
showed
that in
the zebrafish severa1 periventricular or type XIV neurons also respond to electrical stimulation of the torus longitudinalis.
These responses
may interact
in
various ways with responses elicited by electrical stimulation of the optic nerve (see section 4.2.3). The functional significante of the toral afferents to the tectum is obscure, since no further electrophysiologica1 data are available.
However,
lations on the basis of comparative
some specuanatomica1
and
behavioral data have been made. The presente of a valvula cerebelli, projecting to a torus longitudinalis which projects, in its turn, to type 1 tectal neurons via a peculiar margina1 layer, is unique for actinopterygians. The valvula cerebelli seems to some extent linked with the lateral line system, which may be mechanoreceptive as well as electroreceptive in teleosts. Both mechanoreceptorsss and electroreceptor.9 may have topographically organized projections to the valvula cerebelli. Conceivably, the valvular-toral-tectal system might allow for correlation of the visually perceived environment and the environment as perceived by means of the lateral line system. Another, related function ascribed to the torus longitudinalis is opto-static correlations,lo4. Both functions are especially important for maintaining posture in watert*O. It is noteworthy in this context that the torus longitudinalis and the stratum marginale of the tectum reach their highest degree of development in fishes that actively move, either from shallow to deep water or in turbulent water. In contrast, these structures are only poorly developed in epipelagic or bottom-dwelling fishesm). 4.2. Visual inputprocessing 4.2.1.
Responses after electrical stimulation of the op-
tic nerve
Electrical stimulation of the optic nerve has revealed that two retina1 fiber populations with different conduction velocities terminate in the SFGS. This has been demonstrated for Eugerres plumierPJ6*, goldfish*isJs* and carpl46. A laminar profile analysis of postsynaptic potentials occurring after electrical stimulation of the optic nerve showed that the fastest
to layer 5 and layer 415, theories indicate that the
electrical potentials which can be recorded extracellularly in a laminated strutture after massive electrical stimulation of a horizontally entering fiber system, exclusively represent the activity of long, vertically oriented dendrites or dendritic shafts7iJW19. The activity of horizontally are abundant
oriented
dendrites,
which
in layer 415 and 5, is not represented
in
these potentials. Consequently, especially type 1, X11 and XIV neurons have been considered to be responsible for the postsynaptic phenomena recordedzisJs7. Al1 3 of these types of neurons indeed have been shown to make contacts with optic nerve fibersl49~lso. Type 1 neurons are most probably contacted by the slow conducting fibers in layer 415, as could be concluded from the depth of recordings of postsynaptic action potential@ or the distribution of electrical sources and sinks through the tectal layerW. Type X11 and type XIV neurons may be contacted by both ‘slow’ and ‘fast’ conducting retina1 fibers. A tentative scheme correlating the electrical events recorded with the morphology of type X11 and/ or type XIV neurons has been proposed by Vanegas*s4. The retina1 fibers that terminate in layer 2 have a slower conduction velocity than both populations of fibers terminating in layer 5 and 4/5219. The results of Schmidt*lg did not allow for conclusions about ce11 types that are postsynaptic to this third population of retina1 efferents. Recently, Matsumoto et al.147 succeeded in intracellular recording of tectal neurons after electrical optic nerve stimulation, using in vitro preparations of the carp tectum. They could distinguish severa1 response types. and found that monosynaptically activated neurons exclusively occur in SFGS and SGC (layers 5, 4 and 3), whereas bisynaptically driven neurons occur in SFGS, SGC as well as SAC (layers 5-2). 4.2.2. Visual responses of retina1 fiber terminals A number of papers deal with responses of single tectal units after visual stimulation of the contralateral eye. For a correct interpretation of the results obtained it is necessary to know whether the responses
281 271). However,
these types of responses
represent the activity of retina1 fiber terminals or the activity of intrinsic tectal neurons. A definite elucida-
do not show any specific stratification
tion was recently
one type
achieved
by Rowezoz and Niida et
al.172 by means of intracellular
recording
and subse-
quent dye injection. Most investigations, however, used extracellular recording, for which more indirect ways of discrimination have to be applied. Reliable cellularly
criteria to distinguish recorded
between
the extra-
activity of retina1 fiber terminals
and tectal neurons were established by Sutterlin and Prosserz49 and O’Benari76, using electrical stimulation of the optic nerve and subsequent measurement of the latency of the spike response. Units firing after a latency period smaller than 2 ms are in general retinal fibers, whereas tectal neurons mostly fire after a latency of 3 to IO msl72,176.199.205.249.257.262, In addi_ tion, the spike responses of tectal neurons and retina1 fibers upon electrical stimulation of the optic nerve differ with respect to (1) the number of spikes elicited, (2) habituation, (3) maximal frequency of firing and (4) the shape, amplitude and time course of the action potentials. In particular the last aspect was used by Guthrie and Bank@-92 for identifying the responses of intrinsic tectal units. Galand and Liège73 used the depth of recording as a criterion. Units in layers 3 and 4 were considered as tectal neurons, since no retina1 fibers occur in this layer. However, units in layer 5 may be both retina1 fibers and tectal when no further criteria are availneurons, able73.1~,2is~*16. Jacobson and Gazetis, Cronly-Dillon42, Zenkin and Pigarevzso, Niida and Sato173.174, Ramstad and Hughesi94, Warzok and Mark@, Waterman and Hashimoto2” and Waterman and Aoki270 al1 made recordings of tectal units without identifying these units. However, judging from the location of the recording site in the SFGS and the use of meta1 electrodes, their results most likely represent optic fiber responses. Meta1 electrodes appear to be very selective in recording the activity of retina1 fiber activityi76.249 whereas micropipettes, filled with a salinesolution, may record the activity of both fiber terminals and neurons, with preference for the latteri76.249. Retina1 fibers that terminate in the tectum show a number of different types of responses after visual stimulation of the contralateral eye (e.g. sustained as well as transient on, off and on-off responses; movement and direction selectivity; E-vector sensitivity; refs. 42, 73, 115, 174, 176, 194, 249, 269, 270,
of stratification
pattern
in general
pattern.
Only
has been
men-
tioned, viz. by Jacobson and Gazeiis, who noticed that in layer 415 of the goldfish tectum only sustained responses
occur. This was confirmed
by Cronly-Dil-
lo@, Warzok and Marks*@ and O’Benari76, and was also reported for the zebrafishzos, but not for carpi74,is4. It is obscure whether these sustained responses may be ascribed to the slowly conducting population
of fibers which also occurs in layer 4/5*19.
There are presently no data about the functional significance of the retina1 fibers which terminate in layers 314 and 2. 4.2.3. Visual responses of tectal neurons Extracellular recordings of tectal units allow for a distinction of 3 populations of visual tectal neurons. One population is located in layer 5 and 415, the SFGS, a second one in layer 4 and 3 and a third one in layer 1. Sutterlin and Prosser249 and O’Benari76 found in the SFGS a particular population of neurons showing spontaneous firing in the dark, inhibited by light as well as by electrical stimulation of the optic nerve (type 1 of Sutterlin and Prosserz49 and the simple non-habituating cells of O’Benari76). The tectal neurons recorded by Schellart et al.215 also occur in the SFGS, but these showed partly different characteristics. The neuronal population described by Guthrie and Banksso~si.s* was not localized in any specific layer, but includes neurons in the SFGS as well. Apart from tectal neurons, terminals from the nucleus pretectalis, area pretectalis and nucleus isthmi which terminate in the SFGS might also be responsible for the responses observed. Their visual responses would at least have long latencies and other characteristics related to transsynaptic stimulation. Neuronal responses in layers 4 and 3 (the SGC) and layer 2 (the SAC) distinguish themselves by a number of peculiar characteristics. These may include the occurrence of rhythmic spontaneous activity90.249, habituation (newness-neurons)73.9*+176; large receptive fields and binocularity73,90 and a rather large ‘plasticity’ in responsei76. In addition, multimodality is encountered in the SGC and SAC (see below). There are no indications regarding specific ce11 types which would be responsible for these responses. Guthrie and Banks92 distinguished 8 types of re-
282 sponses,
based on specific visual stimulation
condi-
spike recordings
in layer 1 is unclear.
In the frog, the
tions. These could be recorded from layer 1 up to layer 5, with a slight preference for layer 4/5, 314 and 1.
same problem is encountered. In this animal, Gruberg and Lettvinss showed that the ce11bodies of peri-
This might be correlated with the larger density of ce11 bodies in these layers, but does not allow for
ventricular neurons revealed no or very erratic electrical activity. However, in the nucleus isthmi, a celi
identification
mass getting
of specific ce11 types.
might even suggest that the response
In contrast,
it
types distin-
guished are randomly distributed over the different morphologically distinguishable ce11types. Electrical responses tivity of periventricular
in layer 1, representing the acneurons, have been recorded
in the goldfish by O’Benarl76 and in the zebrafish by Sajovic and Levinthal~“s.2”6. The recordings of O’Benari76 revealed multi-unit burst-like activity of simultaneous firing neurons suggesting electric coupling. This might be correlated with the gap-like junctions between these cells (section 2.2.2). In most recordings, the activity could be changed by visual stimuh, which is in keeping with the occurrence of synapses with retinai fibers on the dendrites of these neuronst4sJso. According to O’Bena9, visual stimulation elicits a large variety of response-types in layer 1. which are sometimes rather irreproducible or ‘piasti?. Sajovic and Levinthalzos classified units in layer 1 of the zebrafish tectum on the basis of their responses on a fhckering spot. Most of them could be classified as type 1 (silent in the dark; phasic response at ON and OFF), type T (tonically firing in the dark; phasic response at ON and OFF), type S (silent in the dark; tonic response at ON) or type B (spontaneously firing in bursts). These 4 types also show characteristic responses to other visual stimmi, as e.g. moving spots, spots of different size, bars of varying orientation and surround stimulation~~~. Aithough most of these units were encountered in layer 1. thus representing type XIV neurons, severa1 were observed in more superficial layers as wellz~s. According to Sajovic and LevinthaW. these superficial recordings should be ascribed to dendrites or axons of the periventricular neurons, since they are physiologically indistinguishable from recordings in layer 1. Guthrie investigat~ng tectal neurons in the and Bank+, perch, also included SPV cells in their results, and equally could not distinguish the activity of SPV neurons from that of other tectal neurons. Because the axon hillock of the periventricular or type XIV neurons is situated far away from the cell body. viz. in layer 415, the functional significante of
its input
in the frog exclusively
from
periventricular tectal ceIWs7, good and well-defined responses could be recorded. Gruberg and Lettvir@ conclude that the somata of periventricular cells have no essential function in the electrical activity of these neurons. A similar situation present in teleosts. Also in teleosts,
might well be SPV- or type
XIV neurons are the most important afferent elements for the nucleus isthmiliz and in the nucleus isthmi well defined electrical activity can be recorded after stimulation of the tectum27s. SO, severa1 types of responses recorded in layer 1 might represent only residua1 electrical activity coming from the more superficially located axon hillock, rather than the full electrical activity of these neurons. The intracelluiar recordings of Rowezoz in Ambloplites rupestris revealed a type of visual tectal neuron with a cell body in the boundary region between layer 7 and 6 and dendrites in layer 5 or below. These neurons might well correspond to type 111neurons in the goldfish. since these neurons have some more deeply located branches in teleosts with a highly developed visual system, to which Ambloplites belong@. Type 111 neurons indeed receive monosynaptic retina1 [email protected]” and represent a visual type of tectal interneuron (see Fig. 16). The neurons identified by Rowe*@ showed a quite characteristic type of response, (on-off burst cells), but were not selettive for specific stimulus conditions. The intracellular recordings and subsequent dye injections of Niida et al. 172in Carassius carassius, a species closely related to Carassius auratus, identified visual neurons in layer 1 (type XIV), in layer 314 (which might be type 1X or type X neurons), in layer 4i5 (which might be type IV or type VI1 neurons) and in layer 5 (type 1 neurons), as is in accordante with previous extracellular recordings. By far most recordings were obtained from type I neurons, which is probabiy caused by the large frequency of occurrence of these neuronsis? and by their good endurance to electrode penetration, due to their large dimensions in the direction of electrode penetration. Type 1 neurons showed a number of different types of
283 responses,
corresponding
to the responses
recorded
extracellularly in layer 59OJ76JisJ49. The most remarkable result of Niida et al.172 is the complete absente of any correlation between the type of response recorded and the ce11 type identified. Type 1
from the contralateral tectum, the torus semicircularis and the reticular formation have been demonstrated. There are no physiological indications about the tectal ce11types which may be responsible multimodal
for the
responses.
Only a single recent paper fully deals with multi-
neurons showed a number of different types of responses, whereas other types of neurons showed the
modality
same type of response as some type 1 neurons. Recently, Sajovic and Levinthapas have investi-
tiani*. This author studied tectal single unit responses in Apteronotus albifrons, a weakly electric fish in
gated some interactions
which the torus semicircularis
between
visual and toral in-
put processing in the tectum of the zebrafish. applying simultaneous electrical stimulation
When of the
optic nerve and the torus longitudinalis, a substantial number of tectal neurons shows severa1 kinds of synergistic as well as antagonistic effects. These effects were recorded in layer 1 as well as more superficially and did not show any correlation with the type of visual response recorded nor with the laminar position of the recording site*os. Consequently, it is unknown which of the intratectal pathways present (Fig. 9) are involved in the different types of visuo-toral interactions recorded. 4.3. Deep tectal inputprocessing-multimodality With respect to non-visual responses in the tectum of teleosts, most reports are rather fragmentary. Sutterlin and Prosser*@ and Guthrie and Bank@ have reported spontaneously firing neurons in deep tectal layers that do not respond to visual stimulation. Galand and Liège73 described 3 types of multimodal units for deep tectal layers: visuotactile units; visuolateral line units and visuo-acoustic units. Visuotactile units in deep tectal layers have also been described by O’Benari76. Visuo-lateral line responses and visuo-acoustic units have also been described by Callens et al.25 and Niidai71, respectively, however, without referente to a particular tectal layer. Guthrie and Bank@ recorded the activity of deep tectal neurons during electrical stimulation of the fasciculus longitudinalis lateralis in the rhombencephalon. This type of stimulation could have both excitatory and inhibitory effects on deep tectal neurons. Fish and Voneida reported somatosensory responses, predominantly recorded in layer 1. SO, severa1 types of multimoda1 responses have been demonstrated in the tecturn, and these predominantly or perhaps even exclusively occur in deep tectal layers, where afferents
in the teleostean
ry information
tectum,
viz. that of Bas-
provides
electrosenso-
to the deep tectal layersn.
Bastiarri
describes that the visuo-topic and elettro-topic tectal maps are in spatial register, and that visual and electrosensory stimuli exert strongly interactive influences on many tectal neurons, most of which are located in layers 2 or 3. It should be mentioned that multimodality has frequently been demonstrated in the tectum of other vertebrates, including the salamander Ambystomas6, the lizard Zguana243, the 0~1122, the mouse46.47, the golden hamster*s, the rabbitsi and the cat77J44. In al1 these animals superficial tectal layers are exclusively involved in visual information processing, whereas deep tectal layers contain auditory, somatosensory and/or multimodal units as well. The visuotopic, acusticotopic, and somatotopic maps constituted by these units appear to be in spatial register with each other29.47,86.122.243,244
TO my knowledge, there are no data available concerning the electrophysiological properties of telencephalic afferents to the tectum. 4.4. Tectal efferents Apart from the studies on possible retinopetal tectal efferents, discussed in section 2.3.1, only two electrophysiological studies dea1 with other tectal efferents. Mark and Davidsoni41 recorded single unit activity in the intertectal commissure of Astronotus ocellatus. These units showed rhythmic spontaneous activity in the dark, which was mostly inhibited by increasing levels of background illumination, but could not be changed by patterned visual input, such as light or dark objects or moving stimuli. Wilhams and Vanega+ recorded electrical activity in the nucleus isthmi, nucleus rotundus, nucleus dorsolateralis tegmenti and corpus glomerulosum after electrical stimulation of the tectum in Eugerres and Holocentrus.
284
Their results confirm the anatomica1 demonstrations of tectal projections to the nucleus isthmi, nucleus ro-
might be well possible that visual input would appear
tundus
that according to Ebbessonjo the type 1 neurons of the visually well developed teleost Holocentrus re-
and nucleus
of the dorsolateral
tegmentum,
whereas the possible projection to the corpus glomerulosum is new. Neurons in the nucleus isthmi showed a characteristic burst of spikes after tectal stimulation. The responses in the nucleus rotundus (or nucleus prethalamicus)
showed two distinct excit-
atory components. Electrical stimulation
of the tectum of teleosts elic-
its severa1 types of movernents5.28,3”,44,‘59.
conjugate eye The direction
and of
body these
movements depends on the tectal site which is stimulated, suggesting a kind of motor-map within the tecturn5,‘59. These behavioral responses should be effectuated via tectal efferents. Eye movements elicited by tectal stimulation may be mediated by the nucleus pretectalis, which receives bilatera1 tectal input (see Fig. 3) and projects to the oculomotor nuclei63. Body movements may be mediated by the reticular formation, which is an important target of tectal efferents and projects to the spinai cord. The nucleus pretectalis, area pretectalis and the nucleus isthmi may be involved as well, since these tectal targets project to the cerebellum63J4.137. 5. COMPARISON LOGICAL
OF
STRUCTURAL
AND
PHYSIO-
DATA
Out of the physiological results surveyed, only few aspects can be correlated with the conceptual framework of tectal circuitry presented in section 3. The first aspect concerns the functional properties of type 1 neurons as reported by Vanegas et al.264 and Niida et al.172. Their large involvement in toral input processing264 is in good agreement with tectal circuitry. However, their pronounced responses upon visual stimulationl72 are at first sight somewhat surprising, because they have only few contacts with retina1 fibers. On the one hand this might indicate that the position of the retina1 terminals close to the axon hillock of type 1 neurons indeed increases the efficacy of their synaptic contacts substantially. On the other hand, purely visual stimuli are rather unphysiological, and the experiments of Niida et al.172 do not indicate the balance between toral and visual stimulation. When both toral and visual input would be provided to type 1 neurons in a physiological ratio, it
to be of relatively
low importance.
It is noteworthy
ceive no retina1 input at all, which would be a remarkable species differente with goldfish149 and Eugerresl31. However, the statement of Ebbessons” can only be evaluated after publication of more experimental detail.
A second aspect to be discussed is the lack of correlation between the type of response recorded and the ce11type identified, as reported by Niida et al. 172and also indicated by the results of Guthrie and Bank@. When neurons with a similar morphology and synaptology indeed would appear to subserve completely different functions, elucidation of functional anatomy becomes without prospect. However, it seems presently more plausible to postulate that the criteria used for electrophysiological characterization (on andlor off responses; transient andlor sustained responses) were not the most relevant ones for the neurons studied, and that the use of other visual as well as multimodal stimuli might well uncover common functional aspects of distinct ce11 types. The tectum mesencephali of teleosts probably is no analyzer of on-off or transient-sustained responses, but primarily of other aspects of visual as well as non-visual information. Apart from the aspects discussed above, comparison of structural and physiological data concerning the teleostean tectum reveals in general a great cleft between both types of data. This cleft is on the one hand caused by factors specific for tectal research, on the other hand also by more general neurobiological obscurities. In addition to the gaps in our anatomica1 knowledge, discussed in section 3.4, two main specific problems may be mentioned. At first, the physiologically investigated units have only rarely been identified morphologically, which greatly hampers integration of morphology and physiology. However, recent intracellular tectal recordings7”,‘47,172.~“~ indicate that in this respect substantial improvement may be expected in the near future. Secondly, by far most physiological studies on the teleostean tectum exclusively investigated visual responses of tectal neurons, whereas the important multimodal integrative capacity of these elements, as suggested by tectal cytoarchitecture and demonstrated in severa1 other
285 vertebrate classes, has escaped physiological attention. However, Bastiarri has recently studied multimoda1 (electrosensory and visual) integrative aspects more systematically, and his experimental design seems promising to obtain in the future a more complete pitture
of multimodal
information
processing
in
the teleostean tectum. In addition to the specific tectal problems mentioned, severa1 general neurobiological uncertainties prevent
integration
of structural
and functional
data.
tectal connectivity electrophysiological
in the goldfish is proposed, data conceming
(3) the
the teleostean
tectum are surveyed and (4) the degree of correlation between the structural and physiological data available is discussed. Apart from the retina, from at least 10 other these projections
tectal afferents
brain centers.
originate
At least 5 of
appear to be topographically
nized. Tectal afferents, neurons reveal a characteristic intratectal
orga-
as well as synapses lamination pattern.
Essentially, neuroanatomical research leads to a description of the synaptic connections of neurons (see
Tectal efferents
section 3), whereas neurophysiological research leads to a description of the electrical (spike) responses of neurons for various stimuli under various conditions. SO, integration of anatomy and physiology (functional anatomy) implies determination of the relations between synaptology and spike-responses. In this respect, a number of uncertainties exist. For example, what is the basic differente between neurons receiving few synaptic contacts (e.g. type XIV, receiving f 200 contacts) and neurons receiving many synaptic contacts (e.g. type XIII with + 5000 contacts)? How is the relation between the number of synaptic contacts activated and the frequency of the spike response? How many synapses should be excited to drive a neuron into saturation? When do synaptic contacts (excitatory or inhibitory) integrate linearly or non-linearly. What is the relation between the size or topographic position of a synaptic contact and its effect on the axonal spike responses? etc. etc. Al1 these aspects probably depend on general neurobiologica1 rules with respect to the integrative properties of the neuronal surface, but these are at present to a large extent unknown. Only when more knowledge of these basica1 neurobiological processes becomes available, a more detailed insight in the functional anatomy and circuitry of brain centers, including the teleostean tectum, comes into prospect.
types. The structural data surveyed allow the construction of a conceptual framework of tectal circuitry on the basis of 3 starting points. (1) The existence of at least 8 presynaptic zones or laminae, each containing a characteristic set of presynaptic structures (afferents and axons of interneurons). (2) The fact that the tectal postsynaptic structures (somata and dendrites of tectal neurons) each have a characteristic location, extension and synaptic density, which determines the relative importance of the different presynaptic zones for each ce11 type. (3) The laminar specificity hypothesis, which implies that presynaptic structures that coexist in a particular presynaptic zone terminate without preference on al1 types of postsynaptic structures within that zone. The conceptual framework of tectal circuitry is quantified in terms of connectivity index and connective importance. Analysis of the framework constructed Ieads to a detailed description of the intratectal pathways in-
6. SUMMARY AND CONCLUSION
The present paper is aimed at an exploration of the possible functional significante of the laminar organization of the goldfish tectum at both the cellular and the synaptic level. For this purpose (1) the data concerning the strutture of the teleostean tectum are surveyed, (2) a conceptual framework of the intra-
project
to at least 10 brain centers,
and have unti1 now been shown to arise from 6 ce11
volved in the processing of the 4 main streams of tectal input (i.e. visual, toral, telencephalic and ‘deep’ input). It was concluded that the laminar organization of the tectum is primarily relevant for multimodal integration and that the tectal ce11 types each receive a characteristic sample out of the multimodal information available in the different tectal layers. The physiological data available do not yet allow testing of the tentative conclusion formulated for two main reasons: (1) the tectal units which have been electrophysiologically investigated have only rarely been identified morphologically; and (2) by far most physiological studies exclusively used visual stimulation or electrical stimulation of the optic nerve, whereas other modalities or tectal afferents have
286 only incidentally The combined
received physiological topographical
zation of the teleostean
attention.
and laminar
from selected
organi-
tectum is in particular
suita-
ble for the localization and selection of objects in the environment on the basis of integrated multimodal information
(including
visual, acoustical,
and tattile information)
lateral line
and the subsequent
tion of the eyes, head andlor
body toward
orienta-
objects.
appears to be constant tebratesun. However, mechanisms
This general
throughout al1 classes of verthe underlying intratectal
are far from understood.
the present paper provides framework which facilitates these mechanisms
tectal function
It is hoped that
a functional anatomica1 a further elucidation of
in the tectum of teleosts.
or away
7. APPENDIX The connectivity indexes and connettive importances presented in Table 111and Figs. 11-16 have been calculated as follows. (Starting points, definitions and main outlines have been given in sections 3.1 and 3.2). Firstly, 8 presynaptic zones are distinguished. These are (see also section 3.1.2. and Fig. 8): Layer 7
zone a (za)
Layer 6
zone b (zb)
Layer 516and 5
zone c (zc)
Layer 415
zone d (zd)
Layer 4
zone e (ze)
Layer 314
zone f (zf)
Layer 3
zone g (zg) zone h (zh).
Layer 213and 2
Secondly, the connettive relevance of the different presynaptic zones for the ce11types distinguished is estimated either on the basis of the number of synaptic contacts as presented by Meek 150(see Fig. 8) or on the basis of the dendritic extensions as presented by Meek and Schellartis* (see Fig. 5). This yields the following formulae:
Tw 1
Judging from the numbers of synaptic contacts in the different presynaptic zones, the relevance of za:zb:zc:zd:ze:zf 1900:10:40:120:20:20, from which the following connectivity index (y) can be formulated: y(I) = 0.90za + 0.01 zb + 0.02 zc + 0.06zd + 0.01 ze + 0.01 zf.
Type 111
Ga)
This cell type confines its dendrites to layer 415. Consequently y(IV) = l.OOzd.
Type V
(la)
Judging from the numbers of synapses, zb:zc = 60:390 or ~(111)= 0.13zb + 0.87~~.
Type IV
=
(3a)
The neurons which are confined to layer 4 (type V,) give y( V,) = 1.00 ze
(4a)
The neurons which are confined to layer 3 (type V,) give y(V,) = l.OOzg. Type VI1
Judging from the dendritic extensions, zc:zd = 1:4, or y(VI1) = 0.20~~ + 0.80zd.
Type VI11
(6a)
Judging from the dendritic extensions, zd:ze:zf = 2:1:1, or y(VII1) = 0.50zd + 0.25 ze + 0.25 zf.
Type 1X
(sa)
(7a)
Judging from the dendritic extensions, zd:ze:zf = 2:1:2, or 7(1X) = 0.40zd + 0.20ze + 0.40zf.
(Sa)
287 Judging from the numbers of synapses, zc:zd:ze:zf:zg:zh
Type XIV
= 90:40:30:15:10:15, or
Y(XIV) = 0.45~~ + 0.20zd + 0.15ze + 0.08zf + O.OSzg + 0.08zh.
(9a)
Judging from the numbers of synapses, zb:zc:zd:ze = 2:2:1:5, or
Type VI
Y(V1) = 0.2 zb + 0.2~~ + 0.1 zd + 0.5 ze.
(IOa)
Judging from the dendritic extensions, zd:ze:zf = 2:1:2, or
Type X
Y(X) = 0.40zd + 0.20ze + 0.40zf.
(lla)
Judging from the numbers of synapses, zc:zd:ze:zf:zg:zh
Type X11
= 2:1:5:1:2:6, or
Y(XI1) = 0.12~~ + 0.06zd + 0.29ze + 0.06zf + 0.12zg + 0.35zh. Judging from the numbers of synapses, zc:zd:ze:zf:zg:zh
Type X111
Y(XIII)=0.08zc+0.08zd+0.08ze+0.08zf
(l2a)
= 1:1:1:1:3:5, or
+0.25zg+0.42zh.
(l3a)
Thirdly, the contributions of different presynaptic structures in each presynaptic zone are estimated on basis of the ‘quantitative laminar specificity hypothesis’ formulated in section 3.1.4.3. and the considerations regarding type XIV neurons made in section 3.1.4.4. This leads to different formulae for both alternatives to be considered, which now will be dealt with separately. 7.1. Alternative 1 As pointed out in section 3.1.4.4, this alternative implies that type XIV axons are assumed to make exclusively synaptic contacts with type XIV dendrites, and not with other cell types. Other axons are presumed to follow the rules of the ‘quantitative laminar specific hypothesis’ formulated in section 3.1.4.3. This yields the following formulae with respect to the presynaptic zones (cf. Fig. 8): za =
l.OOtor
(l4a)
zb =
l.OOvis
(l5a)
zc = 0.33vis + 0.33 (111)+ 0.33 (VII)
(l6a)
zd = 0.33 vis + 0.33 (IV) + 0.33 (VIII)
(l7a)
ze = 0.5O(V,) +0.50(1X)
(l8a)
zf = 0.50tel+O.50(1)
(l9a)
zg = 0.33 tel+ 0.33deep + 0.33 (V,) zh = l.OOdeep
(20a) (2la)
Substitution of formulae 14a-21a in formulae la-13a yields the connectivity index (Y) of each cell type in this first alternative: Y(I)
= 0.03 vis + 0.90 tor + 0.005 te1 + 0.005 (1) + 0.007 (111)+ o.02 (IV) + 0.005 (V,) + 0.007 (VII) + 0.02 (VIII) + 0.005 (1X)
(lb)
Y(III)
= 0.42vis + 0.29 (111)+ 0.29 (VII)
(2b)
YUV)
= 0.33 vis + 0.33 (IV) + 0.33 (VIII)
(3b)
Y(V,)
= 0.5O(V,) + 0.50 (1X)
(4b)
Y(V,)
= 0.33 tel+ 0.33 deep + 0.33 (V,)
(5b)
Y(VII)
= 0.33 vis + 0.07 (111)+ 0.27 (IV) + 0.07 (VII) + 0.27 (VIII)
Y(VII1) = 0.17vis+O.13 tel+O.13(1) Y(IX)
+ O.l7(IV) +O.l3(V,)
+O.l7(VIII)
(6b) +0.13(1X)
= 0.13vis + 0.20 tel+ 0.20(I) + O.l3(IV) + O.lO(V,) + O.l3(VIII) + 0.10(1X)
Y(XIV) =
(1 -a) (XIV) + a {0.22 vis + 0.05 tel + 0.09 deep + 0.04 (1) + 0.15 (111) + 0.07 (IV) + 0.08 (V,) + 0.02 (V,) + 0.15 (VII) + 0.07 (VIII) + 0.08 (1X)}
(7b) (8b) (9b)
Y(VI)
= 0.3Ovis + 0.07 (111)+ 0.03 (IV) + 0.25 (V,) + 0.07 (VII) + 0.03 (VIII) + 0.25 (1X)
(lOb)
Y(X)
= 0.13vis+0.20tel+0.20(1)+0.13(1V)+0.10(V,)+0.13(V111)+0.10(1X)
(llb)
Y(XII)
= 0.06 vis + 0.07 tel + 0.39 deep + 0.03 (1) + 0.04 (111) + 0.02 (IV) + 0.15 (V,) + 0.04 (V,) + 0.04 (VII) + 0.02 (VIII) + 0.15 (1X)
(l2b)
y(XII1)
= 0.06 vis + 0.13 tel + 0.50 deep + 0.04 (1) + 0.03 (111) + 0.03 (IV) + 0.04 (V,) + 0.08 (V,) + 0.03 (VII) + 0.03 (VIII) + 0.04 (1X).
(l3b)
288 When each presynaptic strutture in the formulae lb-8b is replaced by its connectivity index formula (eg. (1) by y (1); (111)by y (111) etc.), these formulae constitute 8 equations with 8 unknowns, which can be solved in terms of afferent input (see section 3.2.2.). This yields the following connettive importance formulae (A) for alternative 1:
r(I)
= 0.07VIS + 0.92TOR + 0.02TEL
(IC)
T(III)
= 0.91 VIS + 0.04 TOR + 0.05 TEL
PC)
UIV)
= 0.74VIS+O.12TOR+O.l4TEL
(3c)
UV,)
= 0.39VIS + 0.29TOR + 0.32TEL
(4c)
I(V,) I(VII)
= 0.5OTEL + O.SODEEP
(5c)
= 0.77 VIS + 0.11 TOR + 0.12TEL
(6c)
T(VII1) = 0.47 VIS + 0.25 TOR + 0.28 TEL
(7c)
= 0.39VIS + 0.29TOR + 0.32TEL.
(Sc)
I(IX)
Subsequently, formulae 9b-13b can be solved in terms of afferent input when in these formulae each presynaptic strutture is replaced by its connettive importance formula. This results in: r(xIv)
= 0.61 VIS + 0.13~0~
+ 0.17~~~ + O.~ODEEP
I(vI)
= 0.64VIS+O.17TOR+0.19TEL
(lOc)
I(X) l-(X11)
= 0.39VIS + 0.29TOR + 0.32TEL
(llc)
= 0.26VIS + 0.13 TOR + 0.20TEL + 0.41 DEEP
(l2c)
I-(X111) = 0.17 VIS + 0.08TOR + 0.21 TEL + 0.54 DEEP.
(l3c)
(9c)
At last, formulae 14a-21a can be solved in a similar way, which yields: za (layer 7)
=
I.OUTOR
zb (layer 6)
=
l.OOVIS
zc (layer 516and 5)
= 0.89VIS + 0.05 TOR + 0.06TEL
zd (layer 415)
= 0.74VIS+O.12TOR+O.l4TEL
ze (layer 4)
= 0.39VIS + 0.29TOR + 0.32TEL
zf (layer 314)
= 0.03 VIS + 0.46TOR + 0.51 TEL
zg (layer 3)
= 0.50TEL + O.SODEEP
zh (layer 213and 2)
=
l.OtJDEEP.
7.2. Alternative2 This alternative implies that the axons of type XIV neurons are presumed to constitute 50% of ali contacts in layer 516 and 5 (zc); 25% of ah contacts in layer 415 (zd); 75% of al1 contacts in layer 4 (ze); 33% of ah contacts in layer 314 (zf) and 50% of al1 contacts in layer 3 (zg). The few contacts of type XIV axons that might be present in layer 6 and layer 2 (zb and zh) are neglected. This distribution is based on the following considerations. The percentages enumerated result in an average percentage of about 50%, as is in agreement with the percentage of S5 terminals in the tectum of Holocentrus’“, which are probably constituted for the major part by type XIV axon terminals (see section 2.2.2). The axons of type XIV neurons have no specific preference to terminate in the narrow layers 415and 314, and are assumed to make in these layers the same percentage of contacts as the other types of presynaptic elements (in layer 415: visual afferents, axons of type IV neurons and axons of type VI11 neurons; in layer 3/4: telencephalic afferents and axons of type 1 neurons). Their contribution in the wider layers 5,4 and 3 is assumed to be larger. The ratio between 50% (layer 5); 75% (layer 4) and 50% (layer 3) roughly reflects the preference of type XIV to terminate in layer 4 (see Meek and Schellartt5* and Fig. 5), and is also in accordante with the distribution of S5 terminals in Holocentrus ‘06. SO, with respect to the number and laminar distribution of type XIV axon terminals, this second alternative represents the most probable estimation that can be made at present. However, with respect to their degree of cellular specificity (the first alternative assumes 100% cellular specificity and the second one 0%). the reahty is probably situated somewhere in between both alternatives, since both seem too extreme (section 3.1.4.4.). Just as in alternative 1, the remaining presynaptic structures are presumed to follow the rules of the ‘quantitative laminar specificity hypothesis’ formulated in section 3.1.4.3. With respect to the presynaptic zones, this yields the following formulae: za =
l.OOtor
(l4c)
zb =
l.OOvis
(l5c)
zc = 0.17 vis + 0.17 (111)+ 0.17 (VII) + 0.50 (XIV)
(16~)
289 zd =
0.25vis + 0.25(IV) + 0.25 (VIII) + 0.25 (XIV)
(l7c)
ze
=
0.13 (V,) + 0.13 (1X) + 0.75 (XIV)
(l8c)
zf
=
0.33 te1 + 0.33 (1) + 0.33 (XIV)
(19c)
zg
=
0.17tel+0.17deep+0.17(V,)+O.SO(XIV)
(2Oc)
l.OOdeep.
(2lc)
zh =
Substitution
of formulae
14c-21c
in formulae
la-13a
yields the connectivity
index (Y) of each ce11 type in this second
alternative:
= 0.02vis + 0.90tor + 0.003tel + 0.003(1) + 0.003(111) + 0.01 (IV) + 0.01 (V,) + 0.003 (VII) + 0.01 (VIII) + 0.001(1X)
+ 0.03 (XIV)
(14 C-4
Y(III)
=
0.28vis
+ 0.14 (111) + 0.14 (VII) + 0.43 (XIV)
Y(IV)
=
0.25 vis + 0.25 (IV) + 0.25 (VIII) + 0.25 (XIV)
(34
Y(V,)
=
0.13 (V,) + 0.13 (1X) + 0.75 (XIV)
Y(V,)
=
0.17te1+0.17deep+0.17(V,)+0.50(XIV)
(44 (54 (64 (74 (84
Y(VII)
=
0.23 vis + 0.03 (111) + 0.20 (IV) + 0.03 (VII) + 0.20 (VIII) + 0.30 (XIV)
y(VII1)
=
0.13vis
+ 0.08 tel+
0.08 (1) + 0.13 (IV) + 0.03 (V,) + 0.13 (VIII) + 0.03 (1X) + 0.4O(XIV)
Y(IX)
=
O.lOvis + O.l3tel+
y(XIV)
=
0.13 vis + 0.03 tel + 0.08 deep + 0.03 (1) + 0.08 (111) + 0.05 (IV) + 0.02 (V,) + 0.01 (V,) + 0.08 (VII) + 0.05 (VIII) + 0.02 (1X) + 0.44 (XIV)
0.13(I)
Y(VI)
=
0.26 vis + 0.03 (111) + 0.03 (IV) + 0.06 (V,) + 0.03 (VII) + 0.03 (VIII) + 0.06 (1X) + 0.50 (XIV)
Y(X)
=
O.lOvis + O.l3tel+
Y(XII)
=
0.03 vis + 0.04 te1 + 0.37 deep + 0.02 (1) + 0.02 (111) + 0.01 (IV) + 0.04 (V,) + 0.02 (V,) + 0.02 (VII) + 0.01 (VIII) + 0.04 (1X) + 0.37 (XIV)
(124
y(XII1)
=
0.03 vis + 0.07 te1 + 0.46 deep + 0.03 (1) + 0.01 (111) + 0.02 (IV) + 0.01 (V,) + 0.04 (V,) + 0.01 (VII) + 0.02 (VIII) + 0.01(1X) + 0.28 (XIV).
(134
0.13(I)
The connectivity index formulae which yields the following connettive
+ O.lO(IV)
+ O.lO(IV)
+ O.O3(V,) + O.lO(VIII)
+ O.O3(V,) + O.lO(VIII)
ld-13d can be solved importance formulae
in terms of afferent for alternative 2:
+0.03(1X)
+0.03(1X)
+ 0.38(XIV)
+ 0.38(XIV)
input in the same way as indicated
(94
(104 (114
for alternative
1,
VI)
=
0.06 VIS + 0.91 TOR + 0.01 TEL + 0.01 DEEP
(1c)
T(III)
=
0.73VIS
(2e)
I(IV)
=
0.70VIS+0.08TOR+0.10TEL+0.12DEEP
(3e)
UV,)
=
0.55VIS+0.10TOR+0.14TEL+0.21DEEP
(4e)
I-07,)
=
0.34VIS+0.05TOR+0.27TEL+0.33DEEP
(5e)
r(vII) = 0.70VIS + 0.08TOR + 0.10 TEL + 0.12 DEEP
(6c)
I(VIII)
=
0.54VIS
(7e)
I(IX)
=
0.48VIS+0.19TOR+0.22TEL+0.12DEEP
I(XIV)
=
0.57VIS
+ 0.09TOR
+ 0.12TEL
I(VI)
=
0.68VIS
+ 0.07TOR
+ O.lOTEL+
I(X)
=
0.48VIS
+0.19TOR+0.22TEL+O.l2DEEP
l-(X11)
=
0.34VIS
+ 0.07TOR
F(XII1)
=
0.26 VIS + 0.06TOR
Formulae
za (layer 7)
+ 0.06TOR
+ 0.15TOR
+ 0.08TEL
+ 0.18TEL
+ 0.11 TEL+
+ 0.13DEEP
+ 0.13DEEP
(8e) + 0.22DEEP
(9e)
O.lSDEEP
(1Oe) (llc)
0.48DEEP
+ 0.13 TEL + 0.54 DEEP.
(12e) (13e)
14c-21c can be solved in a similar way, which yields:
=
l.OOTOR
(14d)
290 zb (layer 6)
=
1.00v1s
zc (layer 5/6 and 5)
=
0.69VIS
zd (layer 415)
=
0.70VIS+0.08TOR+0.10TEL+0.12DEEP
ze (layer 4)
=
0.55VIS
zf
=
0.21 VIS + 0.33 TOR + 0.38 TEL + 0.08 DEEP
(l9d)
zg (layer 3)
=
0.34 VIS + 0.05 TOR + 0.27 TEL + 0.33 DEEP
(2Od)
zh (layer 213 and 2)
=
1.00 DEEP.
(2ld)
(layer 314)
(15d)
+ O.lOTOR+
O.l4TEL+
(l7d)
2’ DLT FRI FRm mes NDL NGL NI NP NR
( 184
0.21 DEEP
ABBREVIATIONS ADc
( 164
+ 0.07TOR+0.09TEL+O.l5DEEP
area dorsalis centralis area pretectalis diencephalon nucleus dorsalis lateralis tegmenti formati0 reticularis lateralis formatio reticularis medialis mesencephalon nucleus dorsolateralis thalami nucleus geniculatus lateralis nucleus isthmi nucleus pretectalis nucleus rotundus
ACKNOWLEDGEMENTS
1 am greatly indebted to Doctors R. Nieuwenhuys, J. J. Eggermont and G. Vrensen for their interest and valuable suggestions during preparation of the
NRMT NRS Ret rhomb SAC SFGS SGC SM SO SPV Tect tel TL TS
manuscript, and to Dr. N. A. M. Schellart for critica1 reading of the manuscript. 1 am grateful to Mr. J. Maas for the drawings and to Mrs. M. SankatsingSjak Shie and Miss A. Siebring for their skilful secretarial assistance.
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