The optic tectum of gymnotiform teleosts Eigenmannia virescens and Apteronotus leptorhynchus: A golgi study

THE OPTIC TECTUM OF GYMNOTIFORM TELEOSTS EIGENMANNIA VIRESCENS AND APTERONOTUS LEPTORH~NCHUS~ A GOLGI STUDY E. SAS and L. MALE-R Dcpartmcnt

of Anatomy.

Faculty

of Health Sciences, University of Ottawa. Ott;twa. Ontario KlH 8M5. Canada

451 Smjth

Rnxi.

Abstract Golg~. Nissl, Bielschowsky and cholinesterase techniques have been used to analyze the optic tectum of the ~cakly clcctric teleost tish Ei~mnranniu rirrscens and Aprcronorus keprorh~nc~huc. Six layer\ r~rc rcad~ly dlstlnguished: a fairly thick stratum marginale. a narrow stratum opticum and stratum librosum et grlseum supcrficiale. a well-developed stratum griseum centrale, a stratum album centralc and ii compact stratum prrivcntriculare. Fifty-six neuronal types are present. In regard to comparative aspects of tectai organization. it became apparent that although most neuron~~l rqpcs are similar to those reported m other telcostean fish, there are certain obvious differences such 35: ti) pyramidal ccl1 somata not confined to stratum fihrosum et griseum superficiale, but also clustered in tlte aci~acent stratuni opticurn. presenting stratified or diffuse basilar dendritic arbors: and a change from vertlcai IO oblique and almost horizontal neuronal orientation in the ventral and caudal &turn. (ii) The presence of pyramidal cells with aligned and misaligned apical and basal dendritic tieids. (ii)) PI cell of
The cbptio tectum of lower vertebrates as well as the superior colliculus of mammals arc important targets for highly topographical visual and multisensory input\. which convcrgc upon tectal neurons. This complex sensory information is fed via descending tcctol’ugal pathways to motor centers of the lower blain stem and spinal cord, thus resulting in the orienting hchavior of the animal towards stationary or moving objects. The deep tcctal layers have been shown to contrihutc to the des~~n~iing tcctofugal pathways presumably rcsponsiblc for the motor responses in frog, .‘N birds.“’ fish” and mammals.” in most vcrtcbratcs the tcctal celis in the superficial lavers rcceivc topographically organized visual 4i.Wh2.711Nhich is completely or partially inpui. 111-1: crossed according to the species, whereas the dcqx~r laycrb rcccive a wide variety of other sensory

.~llr/~~r~r~,r,cio,f.\ : IPI_, Inner plexiform laqcr; JAR, Jamming ;i\ oitiance response: SAC. Stratum album centrale: St GS. Stratum fihrosum et griscum supcrficiale; SGC, Stratum grismm ccnt~tk: SM. Stratum marginale: SO. St!-atum opt~cum: SP\‘. Stratum pcriventricuiare~ TS.

-rcbrtis w3nicircuktris

modalities,

including

auditory’.‘5 ” and somatctBesides these ubiquitous nonvisual sensory inputs. certain species have devclopcd special sensory organs, such as: heat sensors in rattlesnakes and pythons.‘h.‘2 electroreceptors in various teleosts.hx chemoscnsitivc finrays in the tclcost and these non-visual modalities Prionotus carolinus.‘b will also be represented in the tectum. Although a few superficial tectal units receive only visual and other deeper units only unimodal non-visual input. in most vertebrates the overwhelming majority of deep tectal neurons reccivc visual and ~~t~iti~n(~~i~~i sensory information. The visual and non-visual inputs to the tcctum at-c generally in topographic register (visual and Inl‘rared heat sensory input.2h.S’ visual and auditory information,*‘,” visual and somatosensory input” ‘_ ‘l”‘). and this alignment is dependent upon proper scnsorb input? Taking into account the above informatlon pointing to the large variety of sensory modalities converging upon tectal neurons also receiving visual input, it is not surprising to find that the clectrosensory system of Gymnotids reaches the tcctum‘.“““’ and that this input is also in topogr~~phi~ register wtth sensory,9.‘?,‘2.1h.17.19.30.hS

216

I?, SAS and

L.

MAL~K

Table 1. Thickness of the tectal lamina expressed as a percentage of the total tectal thickness Ap~eronotu.s

Eigenmmnia

Mid

Caudal

Mid

Caudal

18 18 31 15 IX

15 20 34 II 20

14 14 39 II 22

23 20 37 II 9

22 16 40 13 9

16 16 42 I1 15

100

77

72

100

64

54

Rostrai

SM SO/SFGS SGC SAC SPV Total

Rostra1

Measurements were made at rostra], mid and caudal levels and the bottom line (total) is percentage of tectal thickness in comparison with the thickest (rostra]) portion. These measurements were made at the dorsolateral aspect of the tectum; the percentages are somewhat different at the dorsomedial and ventrolateral aspects. Note that the caudal tectum is more drastically reduced in Apferonotusthan Eigenmunnia; this correlates with the reduced retinal input in the former species.“’

the visual input. 2,6 These two sensory modalities appear to converge on the same tectal cells, since Bastian’ reported that many cells of the optic tectum in Gymnotids gave good responses to both visual and electrosensory stimuli. Many other deep t&al cells of high-frequency Gymnotids are responsive to only electrosensory input and may be specialized to analyze electrosensory input related to communication.6’ The aim of this work is to compare the anatomical organization of the Gymnotid tectum with those of other non-electrosensory teleosts, and to correlate it with recent electrophysiological results in Gymnotid fish. METHODS

Rapid Golgi and Golgi-Kopsch material was drawn from a large collection prepared by Maler,4s and new additional material was prepared from 10 small Apteronotus lepforhynchus intracardially perfused with buffered aldehydes4* and stained with Valverde’s rapid Golgi method. Bielschowsky, cresyl violet and cholinesterase? material was also drawn from a previously prepared collection. Wheat germ agglutinin conjugated to horseradish peroxidase (Sigma Chemicals) was iontophoresed into the torus semicircularis of four ApteronotusIeptorhynchus,using pipettes broken to 10-20 pm. A Midgard constant current source was used with currents of 050.8 PA for 3-8 min. After 3-4 days’ survival times, the animals were perfused with 1.25% glutaraldehyde-1% paraformaldehyde in phosphate buffer, followed by 20% sucrose in buffer and sectioned the next day at 40 pm on a freezing microtome. The sections were treated according to the procedure of Mesulams’ and counterstained with neutral red. RESULTS

of Vanegas et al.,@ since this corresponds closely to the laminar pattern of Gymnotids, although the scheme of Meek and SchellartSo is used to designate the cell types, when found to be comparable. The laminar pattern and cellular morphology are generally similar in both species of Gymnotid and a We adopted the nomenclature

(see Fig. 1) for the tectal laminae,

distinction between Eigenmannia and Apteronotus will only be made where differences have been noted. Cytoarchitectonics of the gymnotid optic tectum

In general the Gymnotid tectum conforms to the teleost plan50,69as seen in Nissl, reduced silver and cholinesterase preparations (Fig. 1). From surface to depth the layers are: stratum marginale (SM), stratum opticum (SO), stratum fibrosum et griseum superficiale (SFGS), stratum griseum centrale (SGC), stratum album centrale (SAC) and stratum periventriculare (SPV). The SM and the deeper layers, SGC and SAC, are better developed than the thinner SO and SFGS (see Table 1). Acetylcholinesterase histochemistry (Fig. KY). There

is a dense band of cholinesterase in SO which extends slightly upwards into SM and downwards into superficial SFGS. A second band is present in deep SFGS. More moderate staining is also seen in mid SGC and somewhat more intense in SPV. The laminar distribution is similar to that found in other teleosts,‘i,‘4.‘6 but it is less complex in SO and SFGS, presumably due to the relatively poor development of these layers. In SO and SFGS the cholinesterase is present as patches. The patches in SO are aligned with and connected to those in SFGS. A patchy distribution of cholinesterase has been described for the mammalian superior colliculus mid gray layer,” but does not appear to have been seen in other teleosts. Toral a&rents to the rectum (Fig. ZA). A large toral input to the Gymnotid tectum has been demonstrated.6*638Recently we have repeated these studies using a more sensitive tracer (wheat germ agglutinin conjugated to horseradish peroxidase). Although our description6 was correct in terms of its topographical organization, we now62,63find that this projection is even more massive than previously suspected; because this result is so important for the functional correlation of our Golgi results, we include it in this paper.

Fig. I. Photomicrographs of transverse sections through the optic tcctum. (A) Bielschowsky stain shows laminar distribution of axonal plexuses. (B) Ntssl stained section illustrates the layers of the tectum: SM. stratum marginale: SO, stratum opticum: SFGS. stratum tibrosum et griseum superficiale; IPL. mner plexiform layer: SGC. stratum griseum centralc: SAC. stratum alhum centrale: SPV. stratum periventriculare. Tectal laminae in (A) and (B) are aligned. (C) Specific laminar distribution of acetylcholinesterase in the tectum of Apteronotus. Bar: 50 nm.

Fig. 2. Photomicrographs of transverase sections of optic tectum. (A) Following horseradish peroxidase injection into the torus semicircularis, note sublaminar segregation of toral input in SAC, mid SGC, and a patchy termination of tufts in SFGS (arrows). (B) Horseradish peroxidase filled retinotectal afferents in superficial SO, SO/SFGS border, mid and deep SFGS, mid SGC and SACSPV interface. The retinal projection is only dense at SOjSFGS boundary. This material was taken from our companion paperO) to assist the reader. Bars: 50 pm.

SFGS

SGC

f’SM

SFGS

C

Fig. 5. Camera lucida drawing of pyramidal cell types. Pyramidal cell in (A) has a semiovoid soma. a stratified basilar dendrite and an axon (ax) which forms a “descending” loop in SGC. (B) Two pyramidal cells that form part of a cluster, one has a semiovoid spinous soma, with a basilar arbor confined to SFGS. the second cell shown in dotted lines is a pyramidal cell with fusiform soma with the basilar arbor in mid SGC. (BI) Insert shows an example of a pyramidal cell with two apical dendrites, and a lack of basilar trunk. (B2) Insert is an example of assymmetric pyramidal cell. (C) Pyramidal cell with inverted pyramidal shape, has stratified basilar arborizations in mid and adjacent deep SGC. The axon descends without a recurrent loop. (D) Pyramid with fusiform, sparsely spinous soma, and a diffuse pattern of the basilar dendrite. The axon forms a small “ascending” loop hefore descending to ramify within its basilar dcndritlc field. Arrows indicate axon. Insert in (D) shows detail of somatic spines of a pyramidal cell. Bar for (A. B, C and D): 25 pm. Bar for (BI) also applies for (82) insert: 50 /irn.

219

The

optic

tectum of Gymnotid

fish: a Golgi

t.lg. 3. Camera lucida drawings of Golgi- Kopsch preparations. intcrneurons: (A) glioform cell; (B) horizontal cell with round 3 /tm.

Tor,ll tibcrs end in moderate numbers within SAC and deep SGC. as previously noted. They form a very dense (crminal field in the mid cellular layer of SGC uhich continues unabated through the inner plexiI’orm laqer (IPL). Small tufts of terminals continue Into SFGS; where they reach into approximately the middle of this lamina. These tufts in SFGS (Fig. 2A) l’orm ;i \cry regular array and the terminal patches arc ncvcr in the neuropil below the cell clusters 01 superficial SFGS’SO border (see below). Thus, the clectroscnsory input to SFGS is in patches disjunct fr-om I hc retinal input. which preferentially terminateh upon the cell clusters (Fig. 2B).

A description of the neuronal types and composltinn of the neuropil of each layer will follow. .S/~r//rr/~ mwgide. As in other teleosts the stratum marginale contains the densely packed parallel fibers nhich arise from the cells of the torus longitudln;~lis.7ii One cell type with a round soma and a ~cond glioform cell type (Fig. 3) have been seen in the SRI: both types of neurons are very sparsely distributed. The cell with a round soma has one or IV,O thin dendrites which run horizontally within SM and scarcely branch. These dendrites rarely bear hplnous processes; a fine axon originates from the ticndriric shaft and courses horizontally. The plioform neuron has a characteristically fusiform anti rugged soma, with several thin dendrites which branch rcpcatedly within a small volume of

A

study

Two types of stratum marginale (SM) soma. .Arrow indicates axon (ax). Bar

SM. The dendrites spine.

have small nodosities

and a rare

Strufutn opticurn. SO contains a sparse population of horizontal cells as well as the somata of pyramidal cells displaced upwards from SFGS; the latter cell type will be discussed with the SFGS pyramid. The horizontal cells are of two distinct types (Fig. 4). One type has a small rounded soma and thin dendrites which branch sparsely within SO. This ccl1 has been observed in other teleosts, and corresponds to Type III (a. b, or c) of Meek and Shellart.i” The other horizontal cell has a flask-shaped soma with its narrow portion pointing to SFGS and giving rise to two dendrites which ramify entirely within SFGS. Typically the dendritic arbor is histratified with one set of branches just below SO and the other roughly in the middle of SFGS; the distal dendritic branches bear fine spines. An axon usually arises from the thicker dendrite and it descends into SFGS; but its further distribution is unknown. This cell type is probably Type III (e) of Meek and Shellart.“’ Stratun~,fihroswn et grisrum suprrficialc. The SFGS contains the somata of pyramidal, bipolar and horizontal cells. The pyramidal cells are by far the predominant cell type of this lamina and this category includes numerous subtypes.

The soma of these cells can assume a scmiovoid. fusiform. pyramidal or inverted pyramidal shape. and according to the subtype and location of the somata.

SM

FIN. 4. Projection drawings of horizontal cells of SO. Axons (ax) are indicated by arrows Bar for (A) and (B): 25 /urn. Bar in (C) 50 ilrn. This and following figures are drawings from rapid Golgi preparation\ unless otherwise specified.

317 ---

E. SAS

and L.

it may possess a significant number of spines. The presence of somatic spines was not reported in other studies of teleost tectum. The somata of pyramidal cells are scattered throughout the depth of SFGS. At the boundary of SFGS and SO. however. they tend to form clusters of two or three cells; it is these clustered pyramids which can intrude into SO. Although we have not studied this point systematically, it is clear that each cluster can contain more than one pyramidal subtype (see Fig. SB). Typically every pyramidal cell has in addition to its apical dendrite within SM, at least two other tiers of dendritic arborizations. A superficial tier in the uppermost portion of SFGS at the SO boundary, and a second tier at SFGSjSGC border. When a third dendritic tier is present, it reaches mid SGC (layer 314 of Meek and Shellarts’). For the most part the dendritic tiers within SFGS and SGC he on the same vertical axis; although on some occasions we found pyramidal cells with the arbors in SFGS and SGC misaligned. Such asymmetric pyramidal cells have not previously been described, and since the morphologic asymmetry may have functional significance, we will describe them separately.

Symmetrical pyramidal cells (Tjjpe I qf Meek and Shellart 50) Most pyramidal cells have an apical dendritic shaft ramifying in SM, a basilar dendritic shaft arborizing in SFGS and SGC, and an axon whose terminal field overlaps that of the basilar dendrites. Exceptions to this rule are: (a) the pyramidal cell with two apical dendrites and no basilar arbor, similar to Ramon y Cajal’s” cell “G” (Fig. 146); (b) the pyramidal cells with a basilar dendritic tier in SFGS, but none in mid SGC, and (c) pyramidal cells without a basilar tier in superficial SFGS, but rather raimfying in SGC. The more common type of pyramidal cell has a narrow thorny dendritic tier in SFGS just below SO. This dendritic arbor may arise directly from the soma, from the apical dendrite or from direct or recurrent branches of the basilar dendrite, but it always has the same appearance and is usually less than IOOpm in width. Because these dendrites ramify in that part of SFGS receiving the densest retinal input,h3 we will refer to it as the optic dendritic tier of the pyramidal cells (Fig. 2B). In some cases, especially in Apteronotus, this optic dendritic arbor is apparently lacking; but then the dendritic trunk passing through the retinoreceptive region of SFGS, is very rich in spines. Perhaps this pyramidal subtype receives less visual input than those pyramids with an optic dendritic tier. The apical dendrites have a small number of spines as they pass through SFGS, they usually bifurcate in SO and give rise to an extensive exuberantly spiny arbor in SM. The apical trees have thick, only slightly tapering dendrites which arborize over 20&4.50~m

MALEK

and overlap extensively with the amcal irccs OI adjacent pyramids. The basilar dendritic tree always has one dendrittc arbor either in SFGSjSGC border, or in the inner plexiform layer (IPL), and may have an additional arborization in mid SGC. Mostly these hasilat arborizations are horizontally stratified, but rn one pyramidal cell subtype the basilar dendrite ramifies diffusely downward from SFGS to mid XX’. The basilar dendritic branches are much thinner than the apical dendrites and are only sparsely spiny. Because the basilar dendrites overlap so extensively m IPL. it is difficult to estimate their horizontal spread, but this is probably at least 200-3OOpm. and is far grcatcr than the spread of the optic dendritic tier. The deeper branches of the basilar dendritic tree are in a position to receive electrosensory input from the torus semicircularis (TS) (see Fig. 2A), and will bc described as the electrosensory dendritic tier. One variety of pyramidal cell deserves special mention-this is the pyramidal cell with the triangular soma which is very frequently found in the Apteronotid fish. This pyramidal subtype differs from the others in the following features: (a) the optic dendritic tier is lacking; (b) the soma gives off two thick apical dendritic branches which inittally run horizontally along the SMjSO boundary; (c) the tertiary branches of the apical tree are obliquely oriented, and arborize over partially overlapping territories within SM; (d) the basilar dendrite ramifies within mid SGC (electrosensory tier). This cell type has been described in the goldfish by Romeskie and Sharma. 6” The pyramidal cell axon usually arises from the basilar dendrite, but can also originate from the soma or the apical dendritic trunk. The axonal plexus of a pyramidal cell is always vertically aligned with its dendritic tiers. Although the axon of a pyramidal cell may dcsccnd to deep SGC, it usually describes a loop and ascends to form a horizontal terminal plexus in exactly those strata of SFGS and SGC where its basilar dendrite ramifies. On a few occasions short delicate nodous collaterals were observed at the turn of the loop, when the axon descended deep into SGC, thus pointing to a clear difference in the axonal pattern of a subtype of pyramids. Asymmetric pyramidal cells (Fig. 5) Some pyramidal cells were found with the optic dendritic tier not aligned with the electrosensory dendritic tier. No other distinguishing features of the dendrite or axon appears to be present; however the asymmetry of the dendritic fields is striking and may relate to functional attributes (see Discussion). The asymmetric pyramid has not been described previously, but the other SFGS pyramids have been reported in numerous other teleosts. The pyramidal cell’s basilar dendritic arbor in IPL has been illustrated in the goldfish, ” but has not otherwise been

SM This

(a)

neuron

incidental

spine.

one side

of

spinous The

I[

descends

ramifies

soma

dendrltic

P

IPl

is

/ +\ ax

at

IPL

arhorlration

telcost:

within

mid

typically SGC

only

the

has ken

deepel

noted.

01‘ lhc

icnglh

boundal->

is

MCII dcvclopod

(IPI.).

diversity

of neuronal

bell

fusiform.

us

a

Lo arc

ported

in other

;I striking

types

A

prcscnr

in

Ci~mnotid~.

strata.

and

Xi(‘)

p! r:tmldal.

\ariet!

;I\

an ;IWII

nc‘uron M lth

gangl~<>n~c

;I

of multipolar.

01‘ niultipolai-

Itian

tliow

and surprisin~l!

to

and ;15 ;I deep

c‘
pl riform.


telcost<.

;I\ \i\ell

S
consl\tlns

wider in

rcscmblancc

7(‘)

The

undescribed

SO.

neurons

&Y-

Its o\in dendritlc

(mid

border).

horirontal.

heretofore

ascending

(Fig.

intcrmcdlate SAC

modcratclg

after si\~ng ott‘collalur;lls

deep cellular

(SGC

small

scmlcii-cular

within

to SGC

neuropll

lield

pi-c\ Iou\

cell has

;I small

formin, (I

and

spine.

7H).

axon ramilics

a mid

th~nncr

arc

the

SFGS

bipolar. an)

bt-anchcs

ticld. and descends

Iaycr

lat-gc

branching

and

a( the XC‘

supcrticial

in

sccondar)

;I

ha\

sparscl>

Iypc of‘ horizontal

ticld. The

ccII

thlcl,

horirontall)

branches

This

described

single

cell type (Fig.

exhlblts

and

Lbhcrc II

c)nly J rare or~cntcd dcndrltlc

twice

(c) A third spinous

liclci.

soma

(11~‘

horder

of horvonk~l

;I

nodohitics

1‘~

of this

horizontal

dritic

type The

;I

Icast

laniinai-

(‘I-0111

an

from

IMO \parscl>

narro\\

the SFGS’SGC‘

and

trunk.

and prcscnt len$h

or

ulth

;II-IW\

7A).

second

rounded

W~~I

shal‘t

one

;I

ccl1 originates

towards

(Fig. A

(b)

gi\cs

forming

of this

rounded

dcndritlc

and

the cell

branches.

axon

The

has ;I small A single

~mc

ccl/\

rcbear

rc‘pc~r~cd

111

the frog.“’ This

cell type possesses

occasional or~entcd spinous ar!

spine:

and

in the vertical dcndritic

originates

shortly

ax011 course

A

IS

and

given off‘which

\\;I\ not

forming

at the SFGSWX

dclicalcl~

bifurcates.

dcndt-ites

two

confined

spinous into

(Fig.

The

SGC 6A).

large

and SAC

and

SGC: class.

cell gives rise to dendrite

The

multipolar

cells

of Mech and Shcllart.“’

along

dendrite coursing

the opposite

dcsccnds

bound-

boundary.

bipolar

from

imprqnatcd)

-

soma with an

polar

one at the SO:‘SFGS

(FIN. 6H). Another

ascending

an

round

slender

from the ascending for a short distance

could be followed St
small

plant

fields.

and the other

axon

;I

two

thus

SGC

they

Al-c

boundary hill

in the straltmi

(Types

most and

Ol‘kll

the uhua1 I~>cation of the

and XIII,

li~~llld

Ic\s frequcntl!

bc considcrcd album

Xlll

ccnlralc.

SOI~~;I n11l

togcthcr

Ill

SAC‘

III ciccp ;I\ otrc

and in c‘;~li bc \~,~rcd

c‘;I\c’

which pole.

an

(its further

Allhotigh SGC

lhc

p!raniids

with a$ccnding

of

XC

and

lhe

ayon to SO arc multipolar-\.

ccl1 01‘ the>

224

SFGS-

/i

SAC

f ax

SPV

A

\

5M

so

CSAC

The optic tectum of (rqmnotid

will

hc discussed

The

soma

LISU;III~ Sonic

of

separately the

located of them

at the end of this

medium-sized

in SGC

cells

and less frequently

rcscmblc

ccl1 Types

IX

drites.

seclion.

multipolar

is

in SAC.

Four

mediutn-strcd

he designated (a) Thts

The

apical

\+ithin

dcndrires

dendrite

r>pc

“b”

in SGC.

u,hich

ascends

to SFGS.

dcnJr_iIic

shaft

arccnd\

towards

been noted. both

species

especially was

not

of

(c) Type scvcral

“c”

type

frequency

of this

nat-rob

ccl] (Fig.

tine.

of this

leave the

in SGC

modcratcly

:I short

towards

number

deep

illustrated

(Fig.

l4D).

The

alon onI!

tn S(i<’

is vet-1 rare:

dcndritc

SO.

:I

iI hits

gt\es ;t few lint

These

locall!

dcndritch

111deep 111uppc~.

c;trr\

spincx.

ccl] \\~th similar bk

onI\ :I

The

and gi\c< ;t rccurrcnl

onI!

;I\OII

collalcral

appcarancc

Kome\htc

it

dcndrita

br:tnching

of long-stcmmcd

in IPL

SGC‘.

been

XD)

which

ticcp SI:GS

,~nc! was

one side. that ramil)

and adjacent ;t plexus

S
W~:I

diztancc

cell (Fig. soma

This

ovoid rami-

ih an eaoccdingI>

high-frequency has never

dondrtte and then

appears

and

ha\

Sharma’“’

to be unique

the apical

may

and

sensor!

tectal input.

collaterals

hale

not

in

SC;<‘.

is \cry

common

Gytnnotid of other

dccpcr SGC‘.

i>

numerous

ot

ccl] type has a bipolar field

(Fig.

has a multipolar spinous,

radiating

A vcr!

neuron

tclcosts

mid

in

and

This

ha\c ;I role

OE)

The

ctrcumscribed also laden uith tn

IPL

soma

SFGS.

dcn-

axon

and

The

at-iscs

clthcr

it

ncuroli

to

the

clcctroli~und

bc tii\pl;tccd

an irt-cguI;tr

ct~ntoui.

IO 1%tth

and spine\ dendritic

tree’ r;tmtfic\

arca in deep SGC‘. spines.

Since

thih

is t!l~tcall>

somelime\ ha

basilar

and tinally

tclcost. fish.


cell body

can

soma

lower

OLII- kno~+lcdgc.

to Gymnot~d

excrcsccnces $ptny

to

in anolhcr

specificall\

but

ccl1 I\ pc 111 both

but.

been dcscribcd

sotna

from

common

Gqmnotids

the

dendritic XF)

to

“d”

in mid the

itt

1(> deep

This

an

apical

leaves

in the tcctutn

and

The

dendrite

in the caudal tectum.

A variant

configuration Lvitlt

high

rcportcd

axon

have

arises

local

neuronal

prevalent

amphibians.

axon latter

SFGS:

This

XC) basilar

branches

the

to ascend

modcrvtc forms

branches

from

and an ascending

SFCiS

vet-lically

branchlcts

arises

spheroid

SGC.

tout-SC’ hort/oncall>

ascend

II cell in the frog.”

prominent

The

it

SGC.

in SFGS.

The

Type (Fig.

spinous as

in

and may thus

a small

and a more

gives fatrly

sparsely

:I

and

have not been identified.

neurons Mith

ramifies

spinous.

resembles

perikarya

fying

some

ccl]

(d) Type

XH) lbith

dendrite

perpendicular

SW

local collaterals

(b)

which

gives

arc moderately

cell (ypc strongly thorn!

gtbtng this

oriental

(Fig.

apical

and also ramifies

cell type is seen to enter tcctum:

soma

;I prominent

dendrite

SGC

after

stna]]

they will

which

most

predon-

in SGC:

a. b. c and d.

cell has an ovotd dircctcd

cells with

are found

as types

contour.

larerally

multipolar

dendrites

of

while

obserccd

vertical

rug&

\omc

SGC. of

and X of Meek

and Schellart.5’ inantI)

lish. ;I G~>l,y ~~uci>

accndc

SFGS. forms

The

to ramit\

Ihen ;t small

fr<>ni

lhc

hort/onLall:,

continue\ bouquet

5om;t

obct- :I

;tp~c:tl dendrite.

01

Ihrottgh

tn SM. the

The apical

I:. 5~s

SFGS

SFGS

MID SGC

SAC

and L.

MALER SFGS

Yr

SFGS

The optic tectum

of Gymnotid

lish: ;I Golgi

rtudy

SO SFGS

”

:

b Fig. 9. Bipolar cells of SGC. (A) Type “a” bipolar with an asymmetric basilar dendrite. and an axon (a\-) with collaterals in SGC which appears to leave the tectum. (B) Type “b” bipolar with soma in deep SGC‘. (C and F) Type “c” bipolars are present in different suhlaminac of SGC. (D) 1 ypc “d” bipolar with soma m superficial third of SGC. (E) This cell is a bipolar variant of type “b” medium size multipolar: it5 axon also ascend\ to SFGS, and the soma lies in mid SGC. Laminae a\ indicated in the adjacent fi_eurc.t<;) Infrequent type “e” bipolar cell with soma in superficial SGC, shows an asymmetric apxal arbor m SFGS. Bar for (A,B,C,D and E): 25pm. Bar in (F). (G): 501lm.

dcndrltc and ascends to SO after giving some collaterals in SFGS. This axon is found to extend over ;I ~idcr area than the dendritic trees. therefore only part of the axonal plexus is aligned with the dcndritic arbor. The thick longer axonal branch possibly leaves the tectum via SO. On numerous occasions the axon of the ccl1 has been observed crossing the proximal segment of the apical trunk of the pyramidal cell of SF
Two pyramidal cell types are found in SGC: one is heavily invcstcd with spines and the other has a non-spinous basilar arbor in SGC and only a sparse amount of spines in the apical arbor at SO,!SM bordt_Y.

The somata of this ccl1 type is typically pyramidal m shape and is located in midcellular or adjacent deep sublamina of SGC. It has a basilar dendritic tree which ramifies widely within SGC; occasionally dendritic branches are given off at right-angles to this horizontal arbor to ramify downwards within deep SGC. The apical dendritic tree gives off two horizontal at-hors one in mid SGC and a second at SO. The

dcndritic tiers in SGC arc richly endov.cd \vith spines. The apical dendritic trunk has a small number (~1 spines except when it passes through SO. uherc it is bare. Its terminal branches in SO are moderately spinous. The axon Icaves the basilar dendrite and dcsccnds towards SAC. but it has not been fully impregnated. Ramon y CajalTh (Fig. 146b) is the only author who has described pyramidal cells of SGC with an efrerent axon in the tclcost tcctum. but his illustration doe\ not indicate whcthcr these cells arc spiny.

Thcsc pyramids have ;I very planar. non-spinous basilar dendritlc tree with wide horizontal spread in SGC. The sotna is located in SGC and gives rise to an apical dendrite which divides at the SOXM boundary. The peculiarity of this pyramidal cell. IS the lack of spines or appendages in the basilar arbor. while possessing a moderately spinous dendritic ticld in SO!SM border. The tine and smooth appearance of the basilar branches makes the idcntitication of the axon difficult.

Bipolar cells xc vertically

oriented

neurons

which

are not homogeneously distributed through the depth of SGC since particular types are found at specific depths in this layer. (a) Type “a” has an ovoid soma located in deep SGC. with an apical dendrite which terminates forming a small nodous, scarcely spinous arbor in SFGS. The basilar dendrite is oriented towards one side of the soma and has a sparse arbor in deep and adjacent mid SGC. The axon arises from a dendrite at the SGCiSFGS border and courses downwards giving some collaterals in SGC; it passes through SAC, and it appears to leave the tectum (Fig. 9A). (b) Type “b” bipolar has an elongated soma in deep SGC (Fig. 9B). and two polar dendrites. The basilar trunk forms a confined, delicately spinous arbor in SAC. whereas the apical arbor bifurcates in mid SGC. The axon of this cell was not impregnated. This neuron is comparable to cell “b”. Fig. I2 of Schroeder et ~1.~’ (c) Type “c“ bipolar was observed as frequently in mid as in deep SGC (Fig. 9C and F); the elongated soma gives rise to a thick short and smooth apical process. which bifurcates and forms a moderately spinous narrow arbor in SFGS. The axon arises from the basilar aspect of the cell and was observed descending into SAC. This is probably a projection neuron of SGC. In Eigenmannia both types “b” and “c” bipolars have a more spherical soma than in Apteronotus. A comparable cell is shown by Vanegas et al.“’ (Fig. 3, cell “d”); Ram6n y Caja15* (cell “b”. Fig. 146); and Meek and Schellart.‘” (d) Type “d” bipolar has an ovoid soma in the upper third of SGC: it presents a few thorny spines (Fig. 9D) and gives rise to a single thick basilar trunk with a sparse arborization in mid and deep SGC. The short apical dendrite is thick and breaks up into a bouquet of nodous branches with few spines, that spread in SFGS and SO or SOiSM border. The apical and basilar arbors of this subtype arc wider than those of the previous type of bipolars. The axon originates from the basilar dendrite at mid SGC level, and appears to take an ascending course. We have not encountered a description of this cell type in the literature of teleost tectum. (e) Type “e” bipolar cell (Fig. 9G) was infrequently observed; the soma is located close to the SGCjSFGS border, with a basilar dendrite which descends and ramifies in deep SGC forming a cone-shaped sparsely spinous delicate arbor. The apical dendrite arborizes in the SGCjSFGS border, having its branchlets oriented towards one side. The axon of this cell was not impregnated. This neuron perhaps is analogous to bipolar cell “e”. Fig. 10 of Schroeder et al.,w and cell “b”, Fig. 3 of Vanegas er uI.,~” with the varient that their cells have symmetrical dendritic trees. Fus$orm

cell

The large fusiform cell with the shepherd’s axon (Fig. 19B) has the same characteristics

crook as de-

scribed in other teleosts, Type XII cell 01 Llcch and Schellart.” fusiform vertical cell of Romcskic .tnd Sharma.“’ fusiform with shepherd’s crook .!\on 0:’ Schroeder r/ ~1.~’ and cell “a cross” of Ramon 1 Cajal.5x The very elongated soma is locatcd throughout the length of SGC and gives rise to LUO thick\ polar dendrites. The basal dendritic shaft arhorircs in a horizontal fashion at the SACjSGC border: whereas the apical shaft ascends, giving r15c to ;I dendritic tier in SGC and a more superficial one at the SFGS/SO border. The axon originate> from the apical trunk high in SGC and turns down towards SAC. Another large fusiform cell has its efferent axon originating from the basal pole of the soma (Fig. IOA), and possesses a thick, nodous and wider apical arbor at the SOjSM border than the fusiform with the shepherd’s crook axon. This neuron has combined characteristics of Types Ilb and XI of Meek and Schellart.50 The axon is not shown in the drawings of these authors. Horizontal

cells of stratum griseum centrale

Type “a” horizontal cell has a rounded soma, giving rise to one or two sparsely spinous dendrites which ramify only sporadically in the horizontal plane of SGC (Fig. 11). The axon arises from the soma and appears to course within the plane of one of its dendrites. Ram6n y Cajal’s’* horizontal cell (Fig. 164, cell “d”), Vanegas et a1.69(Fig. 7) and Meek and Schellart’s’” Type V, seem comparable to the Gymnotid variety. Type “b” small horizontal cell has an octopus-shaped soma and fairly spinous confined dendritic field at different levels of SGC. After a short trajectory, the axon bifurcates into two small slightly beaded branchlets. These are probably small interneurons of SGC (Fig. 11C and D). Stratum

album centrule

The SAC is chiefly a fibrous layer containing scattered large multipolar cells, a few medium-sized multipolars, and a small number of pyriform cells displaced from SPV. According to the preferential orientation of the dendrites, the large multipolar cells of SAC, can be divided in: (ai and aii) Cells with a chiefly horizontal dendritic spread (Fig. 12A,B). (b) Cells with a predominantly horizontal arbor, and one vertically oriented dendrite (Fig. 13). (c and d) Cells with a substantial vertical dendritic component, in addition to the major horizontal tree (Fig. 14A,B and C). Some of these cells can be found displaced upwards to deep SGC. (a,) This cell has a widespread dendritic field in deep SGC. The soma has a peculiar flask shape, and gives rise to a descending dendrite with a characteristic widening before it bifurcates in SAC. These dendrites have a nodous sinuous contour and are non-spinous. The axon was impregnated for a short distance ascending in SGC (Fig. 12A).

SFGS

MID

SGC

\

DEEP

SGC

mid SGC

\, SAC

SPV

A

(a, ) This dcndritic a fa\

cell generates

tree at the XC.

branches

reaching

drltes are moderately

an extensive

SAC interface. down

to SW.

(Fig.

12B).

A

similar

only for ;I short

cc11 type

described for both. teleost (Schroeder cell

“b”)

and

Thcsc den-

spinous. An axon arises from

the cell body and could bo fotlowcd distance

horixon(al and also has

amphibian

tcctum

(bl This large multipolar dendritic

and Marc

Sharma.“”

Discussion).

istic of this neuron

(Fig.

13) has ;I

processes. and a wide and deep SGC.

An importanl

is that in addition

character-

it posscs~s ;I

we have only been able to

this process to the IPLiSFGS

border.

The

in SAC.

13: Vanegas

Fig.

rccentt!

1’1trl..“’ Fig!. I2 c’t (I/..“’

and teavcs ~hc It‘ctum

collaterals

al‘tcr

Th~j

ccl1

type has been described in other teteos;ts (Komcskic

intraceltut;ir

(L6Gr

of SAC

tietd in SAC

is sparsely spinous.

single ascending dendrite; follow

recurrent

this neuron recording

(c) This multipolar large triangular

round soma with tine hair-like horizontal

off

has been

t-I& 4E).

*hich

axon descends to SPV giving

to scvcral dendrites

or (I/..‘“’ Fig.

has been identiticd

and

filled

ccl1 (Fig.

\4ilh

I-IA)

(!t>~call!

thick

spine laden

reach SO to form

The

horirontul h:i\c

;I

apical

SAC‘ and EC.

ha\ ;I

dendri~c~. Tv.o

dcndritcs

cul-vitincalThe

~XUII

:rp~cal

small hcrI;LItb arranged L~IW gi\c

branchcs in mid Xc‘.

wictc

h> (\ec

sparseI> spinou\ cell hod! giving 1-1s~‘

tufts: rhesc tuft? arc nodosc and ont! nous.

dye”’

7).

sparhcly

\p~-

oft‘ spinou\

Two ba\al dcndritc\

asccnding ;~sccncis

courxc to

S
through \\hc‘t-c if

I-. S4\

c

and 1.. MAIJH

Fig.

SAC

t I. (A and R) Horizontal cells of WC. Bar for both liguresr 25 pm. (C and D) Flask-shaped cells of SGC

Bar in (C): 2Spm.

forms a loop and then descends to exit the tectum. This cell corresponds to Type XIII, of Meek and Schellart,‘” and Ram6n y CajaI’s” ceil with thick protoplasmic expansions (Fig. 145b). A fairly similar cell has an ovoid soma with irregular lumpy contour. A variation of the triangular multipolar, has a large candelabra shape dendritic tree; the basilar dendrites are very spinous, while the shorter branches have a nodose appearance. The longer ascending dendrites bifurcate at SFGS (Fig. 14B). (d) Another large multipolar cell (Fig. 14C) gives rise to two or three widely spreading horizontal dendrites with wavy nodose appearance. From these dendritic trunks a series of vertically oriented branches take off, which break up into delicately nodose tufts at the SFGS/SO border. The axon leaves the ventral aspect of the soma and descends into SAC. This cell type has been described by Ram& y Caja15* (Fig. 145a), and by Meek and Schellart% as Type XIII cell.

Bar in Fig. D: 50pm.

small

ax, axon

Medium -size ~luitip~i~r~qf stratum album centrafe These neurons can have a predol~iIlant vertical orientation (Types e and f), or be (Types g, h. i) confined to the deeper layers. (Type e) This multipolar neuron has a mediumsized soma (Fig. 15B) with a wide dendritic field which is formed by obliquely ascending dendrites, These dendrites give off vertically ascending branches which terminate mostly in SGC, although a few branchlets may reach SO. ‘The dendrites are thin, nodose and sparsely spinous. The axon of this cell was not impregnated. A similar cell type has been described in the frog.4O (Type f) This neuron has an ovoid soma in SAC which gives rise to an axon with collaterals f~lluwing a recurrent trajectory. A thick ascending dendrite reaches the IPL/SFGS border after giving two or three oblique branchlets along its course, while a thinner descending dendrite forms a small field in SAC (Fig. 15A).

The optic tcctum of Gymnotid

IPL

fish a

232

A

SFV

-_

(‘fhpc

g) This

\tcllats

mcdium-siLcd

appearance

nc>n-spinous

hr !nchlets

111;I layered

fashion.

co~~,c‘~ in SAC‘

I)

course

tv;mclllcth.

spheroid

horiconlal

The

c,irr I<\ on1\

lint

(Fig.

dcndritic

mod-

in mid

in Xc‘.

(Fig.

16H).

sonia

gives

to

tvio

horizontal

of

arbor

il

shol-ter

dcndritic

amount

SAC‘

trot

tint

Iong

is confind

was incon--

axon

IK).

ascending

SGC:

presenting

tier\

mid SGC

and descend\ (c) Thi\

~II;I

arc the chicl‘ constituents

of this

p! preform cells arc also present Ior

convcnicncc

thq

Th~~ire arc eight ;1\on5. four

will

;dso

with

ctfercnt

hut

ascending

small

branch&),

with

cells

axons.

hcrc.

two types

do ,iot appear to ha\c an axon and ;I candelabra ccl1 \zh~~ Iv

fine ;IYO~ like

idcntilicd I
with

process

in SAC

~n\cstipators

have not

illustration\

ol’iill the

(;\lnnotitis.

and did not she\+ somatic

pyriform

p11‘~cncc ,II- ;tb~ncc

of

I~K;I~I~~~\. it i\ dltTicu/t ,,u~ matcrI;il

with

cell varieties

dcndritic

spines

in

typIcal

to make exact comparison\

thox

spccics

of other

ol

of tclcosts.

avoids

the

(g) The

(Schrocdcr

\mooth

in

round

~ma


amount

rn~tl WC‘.

Upon

brc,lh\

up into

gi\cs an ascending reaching

;I l’airl~

which

reach ah far branch

Irom

SO.

the

ascending

bifurcation.

rcachcs

~~vcrl;tpping

it\ dcndritic

Another

,o~;I

111 XC‘

.~rboi- In \tipcl-licial (h) The

or

This

dclldritic ‘The

“b”

it

the

in SFGS

emerges

(Fig.

I7A).

type has the dendritic

branch

branch

;IXOII

pyril‘orm narrow

usually

IO the

ha\c Tao

a wide field in mid SGC field

in

reaches

ascends and forms

II y~\c,s ;I collatci-al

cells in SPV.

;i5ccndin~

SFGS.

A

single

SM.

a loop. to IPL.

spine\ othcl-

at M hich point and c~dciccnd-

;i

tclc‘osts

ati

with

rescmblc

SI’V

(i) Thib

Thus 17(‘).

(Schrocdcr

(‘I (I/.“‘)

dendrites.

Sonic

;~~;on;il cells

p>riform

ccl1 of mid an asccndinf

this

and

subl;i\er

forms

uruall)

;I f:tir-ly

brancheh

and

dcndritic

tree in

breaks

l\idc

ramities

horvontal oni’

withln (I+$.

up

cell tape dot\ ,I similar W;I~

not

cell 111

report&

of these

to

p) I-iform partialI>

and Schcll;~t-t.” ~&IS :I \01n;1 ulth

dcndt-Itc MIth almost

the aplcal

I‘rom IPI.

SGC

The

nunibcr

c\crc4ccncc\ and

and (>ti1\ ;i Ii‘M splncs

of S<;(‘

,,riginatcx

;i small

raniification5.

of Meek

L;~I;III

base.

boundary

presenting

one: or tM0 spines.

In

proce\\

;I \cr>

at It\

carrIc5

neuron.

no spine\ in mid KC.

numbcl

Ifoloc~cvrr~r,.v the axon h;i\

has

is indented

;kxon (Fig.

XIV

111011

19).

dcndritc

intrinsic Type

;I\OII

ha> ;I daunt)

niodcr-ate

has an a\on-like

cell of

to this

habc

ccl1

the

raniItic\

In our material.

houquct

ha\c pre\! naptlc cells

and

and at the SO ‘SFGS

to

hroadc\t

ccllh.

ccl1 type‘ in

%I)

\omctimcs

typical

mod-

p> riform

cell of SC;{‘

(Fig.

ascending

as-

piLc> otl

the

the

111

the

I7D) with

Fig.

QI~;I

shaft

p>r~form

comparable

;I confined

appear

of

a plexus

a wider

;I dcndritic

shaft

point

forms

pyriform

and forms

lacks

Iramilications,

rclaticcly

J

arbor of this

bvith

v+hile ;I

which

near

whcrc

into

branchlcts

border.

axon

of qncs

deep and

dendritic

of spiny

and

.I short

and onlv

formtng

arbor.

pyr-Iform

which

for

bundle.

SPV

among

SF<;S.

been idcntitied

The

layer\. tylx

1na1n dcndritic ,Incl

this

dendrite

SAC

but

The

IPL

\arict>

11’1.

IPL.

\vidu arbor

dendrite SAC.

as the SFGS:SO

cntcrs

in SPV.

profundum.

01 \pines in SPV.

Gn!rle

(.lii)

ccl1 is found album

\trat imi

in

tier’\? in mid

).

dcndritic

SGC

(F:ig.

(‘I trl..“’

~crrucou~ t!17c’ ofp)riform

mid

\vh~ch reaches deep SM.

som;i.

in

The

dcndritic

4

spine\.

(hi

(.II) 7‘h1\

in

111 IPL tree

I7H

till (OI-

hpinous

and another

elTcrcnt

is smooth

sm;111 p!r-ifor-m

dcndritic

not

t1111\ ml-cl>

the

the previous

supcl-ficially

of

in

soma

of yncs

two sparscl\

arboriation

Lnllkc

numhcr

cell type has a smooth it

in the SI‘CiS

smooth

been imprcgnatcd

in SGC.

hranchcs

in tMc>

17(i).

remains

(FIN.

111

branchlct\

has ;I smooth

in SAC

in SAC

dendrite

types.

in

ot- the

haa

spinous

spin!

found

spines.

awn

clthcr

;I loop in IPI

uhlch

It forms arbor-

spiny

(FilJ-.

It hax ;I moderate

deep to

ccnding

horl/ontal

provided

y%nou\

it terminates

cell of SPV

pyrilhrm

or

that

certainty.

pi-~IOLIX

This

type

have yet to

and

tn mid

ramification\

befhrc

deep XC

coursing

erately

intrinsic

SPL

to an aaccnding

or
HYO~ forms

width

The

(f)

plexus

sparscl)

rise

of its

dendrite,

where

SPV.

The

Into

SAC‘.

Sonic

and SG<‘.

be described

thpe\ of pyriform

I!Ix~

lamina.

in SAC

in

spines.

ccl1 is located

spines most

p>ril’orm

distance

cells and pericpcnd~mal

I‘uund

somatic

is only

pike5

and Sf:GS

of SM.

deep half

X3<‘. types of pyiform

soma

and giving

a medium \ arious

It5 dcn-

and axonal

pyriform

its

in S.4C.

and

cell

two

dendrite

type “d”

or

dendrite.

to

pyriform arbor

wIthin

l7B).

SCiC.

((1) The

2

The

origin

and

The

with

SFGS.

The

ramitia

(Fig.

one or

has

dcndritic (Fif.

thpc‘ “c” pi-esents

cell of SAC

ad_iaccnt deep SGC.

plc‘lcl> inlpwgnatcd

The l7E)

has both the dcndritic

at IPL

which

SGC

axon

;I tuft

nodous

branch in mid

The

dcndritc

The

field

SGC.

mild

211 ltlzlgniticant

~tcmmc1.1 \pincs.

recurrent

(c)

asymmetricall\

dendrites

into

111 deep SC;C

long

ing dritic

nndous

SC<‘.

ascending

The

cell has a

delicate

IbA).

breaking

:~~on cour\cs

S:\l . and

to

a semicircular

boat-shaped

\p~nou,

l~~ngcr branch

thicl,cr

which

forming

(Fig.

( f\ pc 11)This

(.I‘hpc

multipolar rise

deep and adjacent

t~eld 111MC‘.

L,I.,IIcI~

giving

IICI-.

01’ thc\c the

17b)

in IPI

\haI‘t bil’urc;itc\.

plant

l‘hc

,i\c)n

\ccondar-> of It\ 0v.n

E. SAS and L. MALEK

SFGS

SFGS SFGS

M SGC

\

&

a

sic

A

sac

:

Fig. 15. (A,B) Medium-sized

Fig. 16. (A,B,C)

SGC

ax

Medium-sized

multipolars

multipolars

of SAC with a preferential axon.

vertical

of SAC with dendrites 50pm. ax, axon.

ramifying

SPV

orientation.

mainly

Bar: 25 pm. ax.

in deep layers.

Bar:

The optic tectum

of Gymnotid

SAC’. The dendritic shaft is fairly smooth through deep SGC. and then it gives spinous branchlets in mid SW‘ and IPL. One tine dendrite ascends to SM and carrlcs a moderate amount of fine long-stemmed spines. The axon originates at IPL; where it gives a few branches and then, it takes a long recurrent cout~se and leaves the tcctum via SPV (Fig. 18A). (b) This projection pyriform cell type (Fig. 18B) has the soma located in SAC. with dendrites ramiI\ins appropriately deep in SAC and SGC, but do not cntcr SFGS. This subtype dots give off local collaterals at the height of the axonal loop in SGC, to IPI. and mid SGC. and terminates by leaving the tcctllm. This ccl1 appears to correspond to Type XV 01‘ Rlcck and Schcllart.” (by) .4 Lariant of type b pyriform cell (Fig. 18C) has dcntlritic branches reaching SFGS, and its axon hranchcs in IPI. and then descends and leaves the tcctllnl. (c) Tqpc “c” pyriform has the distinctive characteristic of possessing an axon which originates deeply nca~ the sonu (in SAC) and dots not form a loop in IPL but instead it leaves the tcctum after giving a collateral branch which ascends into deep SGC (Fig. IXDI.

This neuron has ;I soma located in either SPV or SAC’ and ;I wide spreading dcndritic arborization conlined to SAC and SGC. The dendrites are mostly smooth with only occasional spines. A thin process was ohscrvcd. leaving a dendrite and descending to WV. but we arc not completely certain of its axonal nature. .An identical ccl1 was illustrated by Romeskie and Sharmah” (Fig. 4D), and Potter.”

This ccl1 has a fairly similar appearance to that shown by Ramcin y Cajal’” and Vanegas ct trl.,h’ with onI> slight variations. It differs from that shown by Ram& y Cajal 5X in Barhus fhiatilis. in that in Gymnotids the radial process of this ccl1 maintains its hirsute appearance even in the superficial layers. This ccl1 has ;I soma with an irregular contour, located at the Lcntricutar aspect of SPV, and possesses a verticall! ascending process surrounded by a meshwork for-med by fine hairlike processes; some of which are longer than the others and protrude away from the meshwork. This apical process reaches SM where it appL~ars to widen into an end foot upon reaching the peal surface. The cell depicted by Vanegas et al.,69 rcfct-red to as an “epcndymal supporting cell” appears to form a cylindrical shaped radial process Mhich progressively widens along its ascent. without prcscntinp intermittently the longer filamentous appcndagcs observed in our material. .4 summary of Gymnotid tectal cells, the laminar diztllhtttion of their dendrites and axons. and the

fish: a Golgi

‘ii

study

laminar distribution of their known extrinsic is presented in Fig. 19 and Table 3.

afYcrcnt\

DISCUSSIO’V The tectum is generally consider& to ol-ganl/c orienting responses of the eyes and body to scnsorh (predominantly visual) input. In Gymnotid fish ~hc nature of both the sensory input and the motoroutput is different from that of most other teteo\ts. Despite these apparently major difl’crenccs. the tccturn displays a remarkable conservatism in it\ \tt-ucture. The discussion below focuses on rhe cvolutionary. functional and dcvclopmcntal implication\ of tectal morphology in thcsc tish. The dominant sensory input to Lhc tcclum 01’ high-frequency Gymnotids is electroscnsor! rathclthan visual. Whereas the retinal Input is dcnsc onI> in deep SO and adjacent upper third of SF(iS. the toral input is moderate in SAC. nuss~\c in Xi< and still substantial in the lower half of SFGS. Since most tectal neurons have dcndritcs uithin the tc~ral recipient zone we assume that the) can hc dit-ccIt> influenced by electrosensory input. The ImpcJrtancc of this toral input is reflected In the cucctlcnr dc\~clopment of SGC and proliferation of cdl rypc\ 111thl\ layer. The decline in retinal input IS not, hov,c\cr. paralleled by an equivalent decrease in the thickness of the SO and SFGS. These two ta!,ct-\ occupk 1623% of the tectal thickness. whereas in o~h fish with poorly developed vision they con\tittttc bunts 1420% of the tectum.” Perhaps the toral input to SFGS can occupy the synaptic targets nc)t-mall> occupied by the retinal input (see sccrion on dc\elopment). Many different toral cell ry~>ch contrlhutc to the torotectal projection’.““’ and. con\iticring the precise laminar or sublaminar dlstribtrtion or‘ mo\t dendritic bushes in the tcctum. II i\ IiLcl! that different toral neurons project to diytinct lam~nac OI sublaminae of the tectum; a prcccdcnt for the \uhlaminar distribution of tectal afTcrcnt\ c‘\i~bt\ in the Thus the parallel protectum of amphibians.“,‘” cessing of electrosensory input k+hich IKC‘III-\ 111~hc TS’ of Gymnotids is likely to continue 111the Icctum. although with the addition of Lisuat inli>rmaric>n to some of the channels. The motor system of high frcqucnch (is mnot~& i\ also modified with respect to: (a) hod> mo\cmcnt\. (b) cyc movements, and (c) electric organ cIIsch;Irgc\ (a) Gymnotid fish move forward or backuard~ b\ creating the appropriate undulation in the ;ln;lt lin which runs the full length of their hod). This motor pattern is presumably dcrivcd from rhc pr~rn~t~\c body oscillation which gcneratcs s\vimminf 111to\\cl vertebrates.” It differs from the usual \v, 1111 ~;IIWII generator in that the oscillation can pt-occcrl l‘tron~ caudal to rostra1 (during backward swimming). end it is usually uncoupled from osclllation~ 01‘ the. hod\ and tail. This uncoupling is probabtl \crh ~mport;~n~ since bending the body or tail change\ the \h;lpc 01

236

SM

so

SAC SPV

i

ax

SPV

SGC

SAC

SAC SPV

E

s PV

-F

The optic tectum

of Gymnotid

fish: a Golgi

137

study

IPL

SPV

H

I

I-IF. 17. (.A) Type al pyriform of SPV with intrinsic axonal plexus m IPL and SFGS. (B) Type b pyriform with axonal rnmilications in IPL and mid SGC. (C) Type h pyriform ccl1 with presynaptic dendrites. (D) Type f pyrlform has a very extensive horizontal arbor in mid SGC, and an axon (ax) ramifying higher in IPL. (E) Type cc pyriform of SPV with wide dendritic arbor and owrlapping axonal plexus in mid SW’. lnscrt In t E) shows candelabra type pyriform. (F) Type i pyriform with wide dendritic tree and atonal ramllication in IPL and soma In SGC. (G) Type d pyriform in deep SGC. Note axonal loop In IPL. and then descending trajectory of the axon into SAC. Ascending dendrite enters SM. (H) Type e pyriform axon courses horizontally in deep SGC. Dendritic tree has an arbor in SAC and deep SGC and ;I second ramification in SFGS. (I) Type J pyriform dendritic tree confined to deep layers. similar to Type XV of Meek and Schellart. Bar in Fig. 17A-I: 2pm. Bar in (E) insert: 50pm.

the electric organ dipole and can thus influence clectrolocation.~~ Tcctal outflow in Gymnotids must thcrclbre control a very different spinal swim generator. t b) Eye movements have been noted in .!+EHHU/HN/U.but not ,4prc~~~~~us.’ We have recently obscrvctl cyc movements in Apteronotids (Maler. unpubli+cd obscr\ ations). but these were so small that the) \+crc readily seen only under an operating mlcroscopc. These cyc movements were most promincnt when the animal had been treated with stimulator! drups as part of neuropharmacological in\chtigations and WC concur with Bastian’ as to their paucity under normal conditions. Recent work has dcmonstratcd that eye movement commands arc convl~!cd to the tcctum via the stratum marginale.‘“.“ but the SM is well-developed in Aptrronotus despite tbc rcduccd mobility of the eyes: furthermore the Jcvcll>pmcnt of SM in .4ptcwmotus may still be correlated with visual input, since it becomes thinner in the, C:~LIC~~II fourth of the tectum where the retinal

input is also greatly diminished.” We can interpret these facts in two ways. Electrosensory and visual input interact in the Apteronotid tectum and. as Bastian’ has pointed out, eye movements would drastically change the correlation of these maps. Thus the analysis of electrosensory input may need to take into account even the minute eye movements of these fish: note that this explanation dovetails nicely with the reduction of SM in the caudal tectum, a region of poor visual input. Alternatively, it is possible that other neural systems unrelated to eye movements have taken over the torus longitudinal&SM pathway (ii High-frequency Gymnotids can change the frequency of their electric organ discharge during social interactions.” The best studied of these frequency shifts is the jamming avoidance response (JAR)” which shifts the fish’s frequency away from that of a neighboring conspecific. A particular combination of spatial and temporal information from electroreceptors is required to drive the JAR, and

23X

E. SAS and 1.. MALFK

C

B

SPV D

SAC

\,

8, ‘\ ,, :,*I, ’

SPV

‘1’,i)

)

4 sc

IPL

a

s PV

Fig. 18. Pyriform cells with efferent axons. (A) Type a projection type pyriform cell with axon collaterals in SFGS and an axon (ax) leaving via SPV. (B) This type b pyrifonn cell seems like a Type XV pyriform cell of Meek and Schellart with a dendritic tree confined to deep SGC, and an axonal loop in IPL with collaterals in mid SGC and an efferent axon via SPV. (C) Type bi pyriform with dendritic tree reaching SFGS, and an axon forming a loop and giving collaterals in IPL and then leaving the tectum. (D) Type c pyriform cell has an axon in SAC. which leaves the tectum after giving a collateral to deep SGC.

both anatomicaPE and physiologica13,29 studies have shown that the TS is essential for the temporal comparisons underlying the JAR. It now appears that this information is conveyed to the tectum which contains cells with the information needed to drive the JAR.29 Heiligenberg has speculated that the JAR may require the tectum because the JAR has evolved from an orienting response. Whether this is the case or not, these results imply that Gymnotid tectal circuitry is carrying out transformations unique to high-frequency Gymnotid fish. Comparatiw

aspects of‘ tectal organization

Despite the different sensory and motor abilities of Gymnotid fish, their tectal neurons are generally similar to those of other teleosts; the similarities and differences will be discussed below. Stratum marginale. Although this layer is almost devoid of neuronal somata, two cell types are found in Gymnotids, and were described only in two other

species of teleosts,58,60 and in the skate, Ruja.” The axons of these interneurons perhaps constitute the presynaptic elements in flattened vesicles reported in Holocentrus.3’ Stratum opticum. The horizontal cells of this layer (Type III of Meek and Schellartso) have similar morphology as those identified in other teleosts 36.50.60.64.69

Stratum fibrosum et griseum super@iale. Pyramidal cells (Type I of Meek and Schellartso) are the major neuronal type of SFGS, and there appear to be various subtypes, not shown in other teleosts. The horizontal and bipolar cells of SFGS are similar to those of other teleosts, but noticeably few in number. In most teleosts (with the exception of Holocentrus) pyramidal cells are mostly found deep in SFGS; in Apteronotus they form clusters at the SOjSFGS boundary and are individually spaced in mid and deep SFGS. Perhaps this corresponds to the segregation of retinal afferents to SFGS. The optic

Round cell of SO Flask shape cell of SO displaced pyramids of SFGS

Horizontal cells of SFGS types a,b Bipolars of SFGS Pyramids of SFGS

Bipolar types: a,b,c,d,e Fusiforms of SGC Horizontal of SGC Aspinous pyramid of SGC Cell of SGC with ascending axon Pyriform types: aii,di,i Pyriform type “a” with efferent axon Candelabra type pyriform Large multipolar type “a” Medium-sized multipolar types: a,b,c,d

SFGS

SGC

Round Glioform

Cell types

so

Lamina

of dendritic branches

Candelabra type pyriform Large multipolar types: a,b,c,d Medium-sized multipolar types: a.b,c.d,e Bipolars of SFGS Horizontal of SFGS Medium multipolars of SAC

Bipolar of SFGS Horizontal of SFGS Bipolar of SGC, type “d” Large fusifonns of SGC Spinous pyramid of SGC Aspinous pyramid of SGC Large multipolar types: c,d Pyriform types: ai,b,d,h Horizontal cells of SFGS, types: a,b Bipolars of SFGS Pyramids of SFGS (optical tier) Pyriform types: a,b,d,g,h Pyriform types: a and bi with efferent Large multipolar type “d” Medium multipolar types: a,b,c,d,e Bipolar of SGC types: a,c,d.e Fusiform of SGC Bipolar types: a,b,c,d,e Fusiforms of SGC Horizontal of SGC Aspinous pyramid of SGC Cell of SGC with ascending axon Pyriform types: ai,aii,b,c,d,e,f,g,i Pyriform type “a” with efferent axon axon

~~~____

2. The constituents

-Round cell of SM 4lioform of SM ---Pyramidal cell of SFGS -Pyriform cell types: b,d -Pyriform type “a” with efferent axon -Cell of SGC with ascending axon Round cell of SO

Origin

Table

Intrinsic

axon

semicircularis

Torus

Pyriform types: aii(IPL),b(mid SGC and IPL), c(mid SGC), d(deep SGC), f(IPL), i(IPL) Pyriforms with efferent axon types: b and bi(IPLa mid SGC), and c(deep SGC) Medium size multipolar types: cd Bipolars of SFGS Pyramidal of SFGS and SO Medium multipolars of SAC

of SGC

Horizontal

axon

b,d

(sparse)

types:

Retina

multipolar

axon

longitudinalis

(very dense)

Extrinsic

Retina Torus semicircularis

Retina

Torus

Origin of axonal terminal fields

Cell of SGC with ascending Bipolars of SGC types: a,d

Medium

Type “b” pyriforms Type “a” pyriform with efferent

Cell of SGC with ascending Horizontal of SO Horizontals of SFGS

of SFGS

cell of SM

Small bipolar

Round

of each lamina

tier

of

the

Ciymnolid

superficial

SF(;S. other

in

tree

SFGS; w”““’ density basilar

input.

cell

sqregatcd

this arbor

OnI!

in Romcskie to terminate

Pyramidal

10 those lrith x+ors

tnisaligned

pyramids

wre

in other

and

(xc

Functtonal

effrren\

axon.

cells OI’SC;~‘.

grcatcr

hpolat-

llletllloncd

bul

pyrll‘~xn~

the bipolat-

WC.

and medium-hi/cd

and there appca~- to he a

()I‘ these cull type\ Prcsumahlq

khan descrthai

fusil’ot-m

;LYO~ (Tbiw same

sho\vn

of Meek

characteristic5

in other

to prc$xt

input

ccl1 of’ XC’

XII

in

tcleosts.

111

thus I-clatc‘s 10 the prcr-

cessing of the larpc clcctrosensor~

the

cells v.tlh

Ill :3/wY~~to/tr.v all tt1c aho\c

tcleo\ts.

crook

cells. I‘u~tlorm multtpola~

domina\c

large

ccntralc

and

Lartctl

The

ccvirrdc

cllhrfrfl

griswm

;~xon. pyramidal

horizontal.

cells are pi-cscnt. multipolars

crook

kctum. I‘unctic~nal

Aspect\).

tbpcs of the stratum

shepherd‘s

15tt h

more l’requcn~ 111

impot-(ant

tcleost5 NC as Ihllous:

ol‘othcr cells \\ith

at-c

Ictc’ost\

01‘ lhcit- apical.

y/.\c111)1 c.c,trtr.trlc trurl .strtrlrrt,l

The neurw-tal

wet-k. IS or in mtd

c:~udalmost

have

I<

111 mod

In our malcrt;tt

relativcl>

may

dendrite

arbor

in IPI.

centers

1;lt-

to reach

tiers. M htle pyramtd\

\entraltnost

implications

ctthcr

are not tnentioncd.

misaligmncnt

allwing

and Sharma’h

aligned

and dtstal basilar

.Strrrfl,tu

dilTcrcnt

Input

one

cells dcpictcd

misaligned

other

only

shown

medialmost.

1hu\

the basilar

forms

SGC.‘”

This

subtypes

tclcosts

usually

limited proximal

the

The deepcl

reach

elcctroscnsor~

In other

and ,,4I,‘)

tiers)

the

,II

rn~d SGC and f’or deep SC;C‘) xcording

the arbor. similar S(;C,‘”

deep

with

iz prcatcst

in .-lptero/to/rr.,.“~,“’

pyxmidal

laminarty

or

correla(cs

which

tn

dcntlrttic

mid

in

this

(electroscnsory

(IPL.

the

ramifies

houndxy tier<

depths to

fish

ccl1 ramitics

the qui\;tlent

“” presumably

01‘ retinal

SO/SFC;S

pyramidal

whereas

to th14 layer.

\btth

shcphcrd’h

and Schcllart’“)

Ci!mnotiJ\.

;I\

hax rh<~

This ccl1 has hecn repclrted

(0 n. ~lrc~h~il;imicua. _” torus sc’illtctt-cLtI.iris.”

and n. i\thmi.“’ .Anothcr with

I‘usii’orm

a deep polar

wrrcspond

cell V.;IS ohscr\cd axon

altering

to the pro.jcction

in (;!mnc~ttd~.

SAC‘. Thih cclt ma> ccl1 Type

YI

of Clcck

and Schcllart‘”

,tnd to ;I SOIIIC‘LLhat s1m11;11ccl1 draa n

by

\+ith

Lcghissa.“:

I‘rotn

the basilar

The

Larious

Gymnntids

XC

bipolar

and

arc tither

hipolar

rostrocaudal the multipolar

shafi

FIN.

estcnt

lot:

in ~11s

cc‘11 01‘

hq the aptcat and one’ tn SO SFCiS

or an a171cal ;~rhot- tn

desccndtng

M;IS obser\cd

cells of’ !X(

prcwn(

GIII hc ground. (~\o~d

located

tn SC;C‘ SAC

and ;I basilar

one c;tsc fhc axon The

1’1 trl.. “” and

The
dendrites

the o(hct-

SO’SM

type\

to the bipolar

(‘I (II.“’ The pcrikary:t

or fusifi>rrn. basilar

cell

bear a rcscmblartcc

01‘ FIN. 3 01‘ Vancgaa Schrocdcr

a\011 ort$nattng

;I descending

5hafi.

are

tn(o SAC’. In

entcrtng l’ound

01‘ [hc lectum;

deep XC’. tn Ihc

and togcthcr

cells. arc the prevalent

ncuromtl

MhOIc htth tcpcs

in the caudalmost Icctum 01‘ lp/~~~~~u~~~~/~.\. The difTcrencc\ \vith hipolar reporrcd in olhcr studtc5 arc.

242

f

SAS and I.. MALIK

the longer vertical extent of the dendritic shafts and the greater diversity of bipolars encountered in our material. In Gymnotids, the multipolar cells of SGC and SAC form a more varied population than those shown in perciform teleost.hY goldfish,5”.h” other teleostean optic tectumjh and squirrelfish.““ These invcstigators point to two subtypes of large multipolar cells; one with a preferential horizontal spread but possessing one ascending branch to SFGS, and the other with a preferential vertical orientation reaching SO. These two types do not appear to cover all the different varieties of multipolar cells reported in frog4” and birds,5’ each projecting to specific target areas. In other teleosts the medium-sized multipolars are usually represented as having a medium width arbor confined either to the adjacent parts of SGC/SFGS, or to deep SGC and adjacent SAC. In our Golgi material we were able to observe all the projection multipolar cell types corresponding to ganglionic cells of layers 6 and 7 reported by Lizir c’t al. in the frog,J” using the cobalt method. The large multipolar neurons of Gymnotids are oriented as follows: (i) in the horizontal plane; (ii) mainly in the horizontal plane with usually one vertical component (see also section on Functional correlations), (iii) in both horizontal and vertical planes. Within the third group there are variations according to: (a) the layers they contribute via their dendritic branches: (b) the retinorecipient layer they reach via their single or multiple ascending dendrites (SO or SFGS); (c) the characteristic manner of termination in the visuorecipient layers SO and SFGS which may be via a single terminal branch, serial tufts. or bifurcating and spreading horizontally, and (d) the width of the dendritic arbor in SGC and SAC. The large multipolar cell with a horizontally oriented soma greatly resembles the fusiform ganglionic cell projecting rostrally of Liz&r et u/.,~” while the triangular multipolar is similar to Ram6n y Cajal’s.s” Fig. l45b cell. which he describes as a ganglionic cell with thick protoplasmic expansions, possessing an efferent axon. The large ovoid multipolar cell of SAC with a lumpy surface. bears a certain resemblance to the Meek and SchellarP’ Type XIII? cell. and to a ganglion cell of layer 6 in the frog. 4” This cell was shown by the latter authors to project to contralateral rhombencephalic levels via the tecto-bulbo-spinal tract, and respond to small moving objects. Lgzlr cutul.” suggested that the large ganglionic neurons of layer 6 in frog are probably responsible for orienting responses to prey. The multipolar cell of SAC with a round soma displaying filiform appendages, and a chiefly horizontal dendritic orientation, with usually a single ascending dendrite towards more superficial layers, is a projection neuron with an axon leaving the tectum via its deep aspect. A similar cell is present in goldfish,hO and in the frog optic tectum, where it was shown to project to the contralateral rhomben-

cephalon.“’ The only diff‘crencc IS the more tromplctc impregnation of the ascending dendrite in Romcskir: and Sharmn’s”” material, ‘ A large multipolar cell of deep SGC 1> ;! t>p~cal example of a horizontal cell confined to the deep layers. This neuron possesses a wide horizontal dendritic tield in SGC which receives elcctroscnsor\ input, and another small field in the SGCi’SAC’ border. It is comparable to cell “d” in Fig. I46 of Ram6n y CajaP in Barbus.$uu’rttilis. The rest of the multipolar cells have a medium-sized soma and arc more frequent in SGC than in SAC. The multipolar cells of SGC probably correspond to the ganglionic cells of layer 7 in frog. 4” These cells were shown to receive dimming and event detector types of retinal information, and to project to ipsilateral spinal cord.4o Chung et ~1.“’ proposed that these neurons arc probably involved in the escape behavior of the frog, when turning away from a threat. Afferents to the neuropil of SGC were reported from ipsilateral telencaphalon to mid SGC, and from contralateral optic tectum to the SGCjSAC border by Ito c’f trl..” Meek,” and Vanegas and Ito,‘” among others. In birds and frogs, cells of SGC have been reported to contribute to the descending tectofugal pathways,‘?.4os9 thus pointing to the importance of these deep layer cells in the initiation of orienting behavior of the animal in response to multimodal sensory stimuli via these descending tectofugal pathways to premotor areas of the lower brain stem. One cell type of SGC appears to be unique to Ap?cvonotus and Eigenmunniu this is the cell with an ascending axon to SO. A remarkably similar cell type has been identified in birds by Ram6n y Cajal.5” The basilar dendritic arbor of this cell would allow it to sample the electrosensory input to SGC while its ascending axon would permit it to influence the pyramidal cells which receive a dominant retinal input. Interestingly the axonal plexus was asymmetric with respect to the dcndritic arbors. Strutitm

peril~entricularr

This deepest layer of the optic tectum houses the various interneuron and projection types of pyriform cells. In Gymnotids eight main varieties of pyriform cells with intrinsic axons can be distinguished, two types without an apparent axon and four projection types of pyriforms. The dendritic contributions to the various layers arc too diverse to build a classification upon them; but they cannot be disregarded due to their functional implications. In Gymnotids the apical dendrite may have: (a) a single terminal apical arbor; (b) contribute via horizontal or oblique branches to different combinations of two layers, and (c) contribute to almost all the layers. The surface of the apical shaft is either smooth. nodose, spinous in specific laminae, or bears only a sparse amount of spines, according to the pyriform cell type. The somata of some pyriform cells may also bear a small number of spines. No mention of these

morphological tectal

difkrenccs

Tlpcs

clcctroscnsory

Golgi

and

c

the tcctum;

usually

Some recognired

three

as follows:

(I

others

notids.

main

by

patterns

that

as

pyriform

axons

can ramify

is

SFGS:

(b)

in

displaced

and

patterns

have been reported

ctTcrcnL

pyriform

of

the

Equivalent

in the goldfish.‘“.“‘-“”

types

identified

and frogJ”

in

also

are

in

its

clcctroscnsor)

localion

and

iological

studier

that

it

is

system

elcctrocommunication; of the Gymnotid

involved

dem(mstratcd

in

and elcctroscnsory predominantly spond thi\.’

’

pyramidal

The

corrclatcs.

Most

point

that

;I

rctlnal

Input

\+ill

input.

Deep

tcctal

01.

may

~XYI

not

he

moving

found onl!

that

fish’s

similar

\+a

able

till\

IC;ISI

<)I’ Rose

some

and

14A

plrilorm the

\ISLI;II

pyramidal

cases

partially

and

16B.

cell “Type input cc‘lls

type.

When

jammed

with

the

visual response

intracellular

of SGC

that

It is possible

cells

tcctal

is

units

at to

and SAC‘

and one variety

l7D).

these most

lost their

cells correspond

respectively) to

For

and

objects.

have shown

multipolars (Fig.

The

derived the visual

since dendrite

its

(cattish) useful

charactcri\tlc poldli\h

(\cc‘

PI-L.~uniabl\

b).

stud)

b;1w

and

tkpc

lhis

wilt

In comparing

ol‘thc

tiitTercnccs

pi-cl\c

10 bc

11

01’ nc‘uIona1 Ii;15

~111 oricntln~

in c)thcr

tcIco~I~

\+tilcli

ltik

liiducc

IS

circuitr): disrup(ed location

and loru\

an

compared

tecluni.

tc\cl.

conipatiblc

Mill

hbpcrapparcnl

Iihcl) ttial cmci-y al the

;Znothct-

c~ol\cd

\\lth

the

po\\ihllit!

i\

~1 [ha1 it\ Icct;il

mot-c

\l;iblc

alloy the ~cctum IO used for orlcntalion

this would the circultr! and nicrel~

IO Itic

It is of c‘ouI-5c

11~5

circuilr)

\cnilcIrcul;iris

by the rcmarh.;lhle

in tcctal circuitr\

microscopical

Ihc toral

output

i’lcclrosen~c~r\

l‘rotn

stimuli

the Icctuni

of the torus.“““.’

electron that

that

to

one is struck

conscrvatlzni more

~niphes

I‘hc

d~tl’~_~n~

communicallon)

ha\ e~ol\cJ

respond

11,

I-cllcs.

ol‘Gymnntidz trophy

t>pc

cvc~ltitloii

(personal

that the JAR

I‘uiiclioii

cIcc~romo~oI

ni;i~’

the

;~nd

Rt,mc\klc

pas\ivct\

IO clcaniinc

Hciligenberg

response cell

;I smgle

lllol-ptlolo~~.

ccl1

01‘ this

large

11 111 boLh

II\ original

b> the clcctro\cnsor! altcrin F II\

:I

ltiarure

and ~LIISC Gyninotids

systonis.

and

cell I! p’c i\ cspcc~all~

allo\+\ us to idcntll‘\

and

wan

01’ ;I jammln~

cells

latrc~-

The

I‘urthcr-

for Ihc JAR.“

to the slsn

pyrlform

teleosts~nonelcctrosensory.

orienting

at ;I frcqucncy

restore

ob.jects.

multisensory

f”

may

Bastian’

simultaneous

Helligenbcrg”’

thcsc

large and medium-sired (l;tg

was

interesting

suggcstcd

always

metal

of either

discharge

to moving

01‘

SAC)

input.’

only

;I

clcctrosrnsory

many of these units

sonic

to

We there-

electroreccptors lo

system

oun.

den-

to

Ii).

01 the pa--

to the lcc(tim.

to bc essential

rc\poncl

ascending

physiological

receive

response

and

by visual

organ

In

(clcctrosensory)

can

and the response

or objects

electric

to the fish.5

input

(SGC

clcctroscnsory

rcbponsl\‘cncs~.

basilar

projccl

man!

to

)x1-1\

OCC’LII-\111

analy\l\

and tha(

both

has hecn usurped

functional

coll~‘ag~~c‘s”~ “I h;l\c

one \tagc of this

(Fig.

without

OI- Ic+ than

the animal

appears

;I

M hcthcr

grcatcr

ditl’crcnt

cells

Fig.

tlctcrminc

bctwccn

which

multipolar”’

to

01‘ ;I neighhol-lng

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244

F. SAS and L.

activity.“,“” Competition for synaptic targets is one of several mechanisms which probably operates to ensure a proper topography for this maprR and may in fact be a mechanism generally used during development to organize neuronal connectivity.35,‘h” If two retinas project to one tectum, either naturally or as a consequence of experimental manipulation, the terminals of the two retinas will occupy disjunct patches of the tectum (see for example Refs 4, 21 and 45; or Ref. 16a for a good review). Retinal efferents to the tectum terminate in three dimensions, but developmental studies have concentrated on only two and have generally ignored the third one-tectal depth. The work of Grubergz4 does suggest that under experimental conditions, non-retinal (somatosensory) input might be able to compete with retinal input for synaptic targets. Since the toral input to SFGS occupies patches disjunct from those of the retinal input to this layer, we propose that these two inputs (TS and retina) compete for synaptic targets in SFGS, and that SFGS is well-developed because TS input has replaced the deficient retinal input. A surprising consequence of this hypothesis is that different sensory inputs can “use” the same tectal circuitry (see Discussion above). In lower vertebrates the retina and tectum continue to grow in the adult animal, and the optic fiber terminals must continually shift their sites of termination across the tectum.‘5,5”“,66,67In Gymnotid fish this problem is further compounded by the need to maintain the congruence of the dominant electro-

MAL~K

sensory map with the visual maps.“’ The cicctrosensory system also changes with the animal growth. Up to about 10-12cm body length, the number ot electroreceptors continues to increase,” as does the electrosensory lateral line lobe and TS (Malcr. unpublished observations). This suggests that the torotectal map may also require continual readjustment. After the animal reaches 12 cm body length the number of electroreceptors remains constant.~ ‘? although the animal can continue to grow to ~~11 OVCI 20cm. Therefore, after 12 cm body length the distance between electroreceptors starts increasing;’ il the retina and tectum continue to grow after the fish has reached this body length it might rcquirc other types of synaptic rearrangements to maintam congruence of retina, tectum and the torotectal map. It is fairly simple to partially destroy the Gymnotid electroreceptor ganglion,“’ TS. or retina and it may even be possible to substitute a larger eye toi- the Apteronotus eye (from some species of Eigenttum~icr with large eyes, for example). Apteronotid fish may prove to be an interesting system for the study of synaptic competition and remodeling in the third dimension of the tectum.

Acknowledgements-The authors wish to thank C. E. Carr for some of the Apteronofus Golgi material, W. Heiligenberg and G. Rose for helpful comments on the physiological aspects of this study, B. Goodwin for typing the manuscript and Bill Ellis for photographic assistance. This work was supported by the Medical Research Council of Canada.

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IO October 1985)