Evolution of electroreception

!l\5

50 19) reveal trophic efli:cts similar to those described here, and other experimental studies show that misoriented dendrites form in response to a change in cell position or synaptic input. A case in point is the patterning of cortical neurons in the reeler mutant mouse a. On the other hand, neurons isolated from many or all of their normal inputs in cell cultures produce dendrite-like processes which may resemble in vivo configurations~-L This shows that synaptic interactions are not necessary for dendrites to form. Evidently there are determinants of dendritic growth which are intrinsic to developing neurons, and the cell's cytoskeletal apparatus appears to play a key role 2°. How such intrinsic organization and environmental influences, such as synaptic input, interact to produce normal patterning provides a challenging topic for future research.

t'ct,rt~,,,, /~J,';.:

Evolution of electroreception T. H. Bullock, R. G. Northcutt and D. A. Bodznick Recent evidence s h o w s that the t a x o n o m i c distribution o f electroreception i,~ greater than was p r e v i o u s l y thought. This k n o w l e d g e p e r m i t s n e w speculation a b o u t the evolution o f this sense, a topic alreaclv discussed in l i m i w d aspects by L i s s m a n .s a n d H o p k i n s ~4.

Electroreceptive fish have at least one set of sense organs specialized for the detection and measurement of feeble, electric fields in the water around the fish, plus specialized brain structures that process this information and organize the appropriate response. The sensitivity of the receptors varies widely. Voltage gradient is preferred to curReading list rent density as a measure of sensitivity, * I Banker, G. A. and Cowan, W. M. 1,,1977)Brain and in the water, the receptor threshold (as Res. 126, 397-425 distinct from behavioral threshold) can 2 Bodian. D. (1937)J. Comp. Neurol. 68, 117-159 range from < 1/.tV cm -~ to as high as 2 mV 3 Caviness, Jr., V. S. and Rakic, P. (1978) Annu. cm -1. The lowest threshold values come Rev. Neurosci. i. 297-326 4 Eaton, R. C., Farley. R. D., Kimmel. C. B. and from salt water elasmobranchs (sharks, skates and rays) most of which lack specialSchabtach, E. (1977)J. Neurobiol. 8, 151-172 5 Faber, D. and Kom, H. (1978) in Neurobiology ized electric organs whereas the highest of the Mauthner Cell (Faber, D. and Kom. H.. threshold values come from freshwater eds). pp. 47-131, Raven Press, New York teleosts with electric organs where special 6 Goodnmn, C. S., Bate, M. and Spitzer, N, C. relatively insensitive receptors monitor the (1981)J. Neurosci. 1.94-.102 7 Hendelman. W. J. and AggerwaL A. S. 1,19801 fish's own discharges. Thresholds of other sets of electroreceptors, even in freshwater J. Comp. Neurol. 193. 1063-1079 electric fish, are generally less than 100 8 Jacoby, J. (1979)Neurosci. Abstr. 5, 165 9 Kimmel, C. B. and Eaton. R. C, (1976) inSim- /~V cm ' and in non-electric fish less than pier Networks and Behavior (Fentress, J. C , 10/xV cm . Marine, non-electric electroed.), pp. 186-202. Sinaar. Sunderland, Ma~ receptive fish attain higher sensitivity than sachusetts freshwater fish. 10 Kimrnel, C. B., Eaton, R. C. and Powell. S. L. ( 1980)J. Comp. Physiol. 140, 343-350 Methods of testing for electroreception 11 Kimmel, C. B. and Model, P. G. (1978) in Well-studied behavior gives the lowest Neurobiology of the Mauthner Cell (Faber, D. and Kom, H.. eds), pp." 183-220, Raven Press, thresholds. Salt-water rays, after operant New York training, show statistically significant 12 Kimmel, C. B., Schabtach, E. and Kimmel, R J. orientation responses to fields of 0,005 p.V (1977) Dev. Biol. 55,244-259 c m 1. Freshwater electric fish show a kind 13 Kimmel,C. B., Sessions,S. K. and Kimmel,R J. (1979) Proc. Natl Acad. Sci. U.S.A. 76, of social behavior called the jamming avoidance response with fields of 0.5/zV cm ' 4691-4694 without training8 (see also T I N S , August 14 Kimmel,C. B., Session, S. K. and Kimmel. R. J. (1980)J. Comp. Neurol. t98, 101-120 1981, pp. 205-210). Reliable uncon15 Model. P. G. (1980)Neurosci. Abstr. 6. 251 ditioned responses are rare, however, so 16 Murphey, R. K., Mendenhall, B., Palka, J. and that behavioral methods are not suited for a Edwards. J. S. (1975)J. Comp. Neurol. 159, wide-ranging survey of diverse taxa. At the 407-418 17 Nakajima, Y. (1974) J. Comp. Neurol. 156, opposite extreme, electxophysiological searches for single sensitive units in the 375-402 18 Nordlander,R. H. and Singer,M. ( 19781J. Comp. nerve, ganglia or brain are also unsuitable Neurol. I80, 349-373 for such a survey since only a tiny propor19 Rakic, P. and Sidman, R. (1973)J. (bmp. tion of neurons can he sampled. Neurol. 152, 133-t62 For these reasons, the most convenient 20 Solomon. F. (t980) Cell 21, 333338 21 Zonoli, S. J. (1978) in Neurobiology of the • Mernbrane channel theory, emphasizes the transMauthner Cell (Faber, D. and Korn. H., edsL membrane voltage sensitivity. Voltage gradient gives pp. 13-45, Raven Press, New York less spreadof thresholdvalueswith watersof different conduetivitiesthan does current density. The electroCharles B. Kimmel is at the Department of Biology, receptive tish acts a.s a voltmeter in drawing very University of Oregon, Eugene, OR 97403, U.S.A. littlecurrent, comparedt~ the waterthe fish occupies.

method for testing whether an animal is electroreceptive begins with recording averaged evoked potentials (AEPs) from the brain s,~. These are relatively easy to record from the mid- and hind-brain and are independent of training, motivation and many drugs. They do not involve extensive searching, delicate dissection or the other problems associated with single unit recording. Furthermore, when stimulus-triggered averaging techniques are used, it is possible to detect small responses not immediately apparent against the background electrical activity of the brain (Fig. ! ). In this context, the term evoked potentials includes four kinds of responses ~. (i) Relatively smooth, slow AEPs are the simplest and most readily found, but demand the most controls against artifacts. (ii) 'Hash' is jargon for multiunit spike activity too small to count. It is detected by listening to an audio monitor and leads to slower 35

56

256

256 ms

Fig. I. Potentials evoked in octavolateral area of a ratfish (chimaera, HydrolaguscoUei)by single cycles" of sinusoidal current at the indicated frequencies, as a uniform field, of 8 I~V cm -~, initially head negative; filters, 1-1000 Hz; averages of 32 -64 sweeps; 10 Hz record is so large the gain is reduced by half Lowest trace shows the stimulus for the 10 Hz response and represents 12 gV at the recording amplification. Brain negativity gives downward deflection.

TINS - February

1982

51

POLYPT ERIFORMES

30 orders Mormyrfformes~" Gymnot,formes Sllur,formes

t.

CROSSOPTERYGII ~, \,

\ \,

DIPNEUSTI ~[~, ~

~

\ ' , I : '/

r---

HOLOCEPHALI ",

\'

\

PETROMYZONIFORMES%~

\\\~\\

',

" ",, ,

\

/ /

~

'\

X

/ ~

--

"

TELEOSTEI . HOLOSTEI

(ACTINOPTE,qYGI,)

~ / ~ (CHONDRICHTHYES) ~ (GNATHOSTOMATA) (AGNATHA)

Fig. 2. Major groups of living fishes and the distribution of evidence for electroreception. DN, dorsal octavolateral nucleus," EL. electrosensory lateral line lobe," LA, Lorenzinian ampullae; TA, teleost type of ampullae; TU, tuberous electroreceptors.

searching for the next two categories. (iii) Multiunit spikes are large enough to discriminate from the background and (iv) single unit spikes are the most difficult responses to find but also the least equivocal. Standard methods are available for summating stimulus-related responses over repeated trials. Each of these approaches has been useful in identifying electroreceptive fish. Strictly speaking, the failure to find an AEP is not proof of absence of electroreception but with experience it has correlated well with other evidence. If slow AEP responses are found within a reasonable range of sensitivity, such as 0.2 mV cm t one can go on to look for single units in specific brain centers, afferent fibers in the lateral line nerves, sense organs in the skin, and both central and peripheral specialized anatomy. We will show below that specialized central anatomy, once validated physiologically, can itself become a search tool. It is most desirable to have evidence, at least by extension from favorable species, that the sensitivity is relevant to behavior or to naturally available and biologically significant stimuli, in order to justify the term electroreception%

romyzoniformes* are highly electroreceptive 2. In a few preliminary experiments, we have not found electric responses in hagfish (Myxiniformes), but it is premature to list them either way. Our own experiments, together with those published by others v, show that nearly all nonoteleost groups have this sensory modality, i.e. lampreys, sharks, skates and rays, ratfish (chimaeras), lungfish, bichirs and reedfish, sturgeons and paddlefish. All of these groups have a special nucleus in the lateral line area of the medulla, called the dorsal octavolateral nucleus (Fig. 3A). This nucleus receives all the electroreceptive afferents via a dorsal root of the anterior lateral line nerve, and no other inpuP"3. McCormick ~ ° = suggested that a dorsal octavolateral nucleus is a diagnostic sign of the presence of electroreception in non-teleost fish. This suggestion has now been confirmed by our physiological studies 2'25. By finding a dorsal nucleus in "Terminologyfor most taxa follows Nelson'": Ior gymnotiforms we follow Mago ~.

Northcutt ~4could add Crossopterygii to the list of presumptively electroreceptive taxa. Contrary to earlier opinions it now appears that electroreception is not a newly evolved sensory system restricted to a few families of advanced fishes but is as phylogenetically old as the other major vertebrate sensory systems. Only the Holostei ( A r n i a , the bowfin and L e p i s o s t e u s , the gar) lack electroreception among the non-teleost taxa - as judged both by the evoked potential criteria and by the absence of both the dorsal root of the anterior lateral line nerve and the dorsal octavolateral nucleus (Fig. 3B ). We suppose that the immediate ancestors of teleosts, like their relatives, the holosteans, also lacked electroreception. The main reason for this conclusion is that, so far as we know, only a very few teleost orders have this sense modality. Out of some 33 orders of teleosts only three are known to have electroreception: the Siluriformes (catfishes), Gymnotiformes (South American electric fishes) and Mormyriformes (African electric fishes). The first two are related, both being in the superorder Ostariophysi along with nonelectroreceptive groups such as the Cypriniformes. The mormyriforms are very remote from the ostariophysans. Thus, it would appear that this sensory modality has been reinvented at least twice within the teleosts, once or twice within the Ostariophysi and once again in the immediate ancestors of the momayriforms. This is all the more notable since this modality includes two main classes of receptors and a whole hierarchy of brain centers specialized for this input. Latimeria,

Several types of electroreceptor The complete independence of the nonteleost electroreceptive system and that of the teleosts is underlined by basic dissimilarities both peripherally (Table I) and centrally. The hair cells of the non-teleosts are excited by negativity at their outer (cili-

Taxonomic distribution of electroreception Where do we find electroreception among animals? So far, there is reasonable evidence only for fish. Some amphibians may be electroreceptive, but the evidence is still only suggestive 9.'~. Invertebrates have not yet been studied. Fig. 2 shows the groups of living fishes and the presently° known distribution of electroreception2O 22.~. The principal surprise in the newer findings was that lampreys (Pet-

alln

A

B

C

Fig. 3. Variation in the piwine octavolateruli~ area o f the medulla ~een in diagrammatic trans'verse sectlotls o f one side, & pattern seen m lampreys, cartilaginous fishes and primitive hony fishes. B, pattern seen m holosteans and nonelectroreceptive teleosts C, pattern seen in electrorecepti~e silurifi,rm teleosts Abbreviations: alln, anterior lateral line nerve; cc. cerebeUar crest; don, dorsal octavolateral nucleus; dr. dorsal root o f alln: el. electro~ensoo' lateral line lobe: m. magnocellular octaval nucleus: nton. medial octavolateral nucleus; vr. ventral root o f alln; ~"111. ~~ctaval nerl e.

52

I1\3

ary) pole, (depolarization of the apical membrane) whereas hair cells of teleost ampullae are excited by positivity at the outer pole (depolarization of the basal membrane). There are also differences in the ciliary appendages, judging from the few well-studied examples. For example, in elasmobranchs the hair cells of Lorenzinian ampullae have a kinocilium but no microvilli, whereas those of teleost ampullae, as in gymnotiforms, have microvilli but no kinocilium. In addition, the equivalent of a dorsal octavolateral nucleus, which in the non-teleost receives the ampullary input, is not found in teleosts. Instead, the three orders of bony fish that have evolved electrosensory systems have each developed a new octavolateral nucleus called the electrosensory lateral line lobe (ELLL) entirely devoted to the electroreceptor input (Fig. 3 C): this nucleus is called by some authors the posterior lateral line lobe. The use of the same name for all three orders does not necessarily imply that these structures are homologous. Despite the numerous differences which highlight the separate evolution of electro-

reception within the teleosts, the degree of convergence is striking'. For example, their convergent microscopic appearance gives the ampullary organs their common name 7~7. Functionally they are similar in having their best sensitivity at very low frequency stimuli (maximum sensitivity between ca. 0.3 and 30 Hz). This probably means that they are adapted for the detection of electric fields other than those produced by the fish's own electric organ. These could include fields of biological origin such as those produced by prey fish, social partners, or even the fish itself, as well as slowly changing and I)(2 fields of geophysical origin. The latter will generally be converted into low frequencies at the receptor by the fish's movements. A further remarkable stage in the evolution of electroreception was the emergence of a new class of receptor called the tuberous organs and the corresponding distinct brain centers. Tuberous organs, named, like ampullary organs, for the histological appearance of the early examples to be examined, are found in all the gymnotiforms and mormyriforms, and only in

/'et,~.,:,, /~:.~_

these two orders Actuall3. the ruberou, organs are quite heterogeneous and like the ampullary categor b embrace independently invented, convergently evolved ,trgans m two taxa that are far apart in relationship ~ :~" Besides a few microscopic characteristic~ of the organ and of the hair cells, tuberous receptors have in common a sensitivity to high frequency stimuli. They are apparently specialized to detect rite electric fields produced by electric organ discharges (EODs) of the same fish and ol others, especially those ~,1 orespecifics"' ~~ ~:*~;'',,.2~. Their rllaximunl sensitivity', depending on the species and upon the individual and even the part of the body surface in which they lie, is at frequencies somewhere between 70 and 3000 Hz. i.e. they are usually sharply tuned.

Subclasses of tuberous receptor In each family of gymnotiform and mormyriform fish there are at least two subclasses of tuberous receptor, distinguished either by the way in which they normally encode intensity changes in the EOD field, or by the physiological intensity

T A B L E 1. Summary of the varieties of electroreceptors and their brain centers Ampullary s3,stems Taxa

Organ

Majority of non-teleost fishes: Petromyzoniformes Hoiocephali Elasmobranchii Dipneusti Chondrostei Polypteriformes Crossopterygii

Minority of teleost fishe~: Siluriformes Gynmotifonnes Mormynformex

I oren:rinian ampullae

Teleost ampullae fmay be heterogeneous)

Hair cells

Tuberous systems Gymnotitbmles Gymnotidae Eleetrophondae Hypopomidae Rlaamphichth} alac

No kanocihum With micmvilh

Polarity

Cathode excite~

Anode excites

Afferent fiber coding type

F

F

First nucleus in medulla

Dorsal nucleus

ELLL ( portion ol medial nucleus)

Midbrain center

TS, lateral half

"FS, lateral third

Sternopygidae Apteronotidae

Tuberous r Tuberous I Tuberous type I type I type n

In epithelium, facing lumen With kinocilinm No microvilli

Momwriformes Mormyridae

Tuberous type 11

Knollenorgan

I G}mnarch dae

Mormyromast

G) mna~homast

ty'pe I

Gymnarchoma~ type It

Protruding into lumen, attached by narrow base, specialized accesmD cells No kinocilimn Mlcrovilli cover flee surface

Mierovilli cover; complex acessory cells

Two type s. with and ~ifuout mierovilh: con> plex innervation

Long micrc~ dli at bottom of invagination

D slow

S

ELLL (

porhon of medial nucleus)

Two types: short microvllh II~ the invaginatton

Anode excites M

B

Ihst

slo~ EI.LL (

T fast

P

K

slow

fast

portion of r~tial nucleus)

I

I

central portion

TS enlarged, highly ~trahfied, differentiated ttlsp layer

qSp, layer

] O I

cortical portion TS nloderatel 3, large with several nuclei

nucl. exten~

nuel ]ateralls

t------

lateralis Adequate stimulus and function

Low frequency tuned (0.2-20 Hz) Locating pr% ; geomagnetic fields

Tuned to 200-1000 Hz ace tospeciesand body part Monitors E OD esp. fishN ,iv,,n

Electrolocation

"furledto 70-20~) Hi ace toindividual

High precision timing, esp. in evaluating neighbor

Amplitude estimation in both location and commum-

cation For further detail, see Bullock (IO82) TS

toms semlcircalari,: El 1 I

electroreceptixe lateral line Io~'

Tared to 500-3000 Hz aec to species and pan

E.O.D of other fish; electrocommuulcatmn

Amplitude ot o w n E.OD.; eleet~oloeatmn

Tuned m ca 300 Hz

t

T I N S - February 1 982 range and hence the normal role. One subclass in m o r m y r i f o r m s is apparently specialized for detecting other fish at some distance (electrocommunication), another for monitoring small changes in the fish's o w n E O D due to distortion by objects in its field (electrolocation). These subclasses, like the ampullary class, have their o w n brain centers, not only at the medullary (ELLL) level, but also in the midbrain (toms semicircularis), the cerebellum and elsewhere. It is presumed that teleost ampullary and tuberous electroreceptors evolved from mechanoreceptive neuromasts of the lateral line system through a reduction in mechanical sensitivity, a loss of the ciliary processes from the apical surface, and an increase in the electrical sensitivity already present in the basal surfaces. If this is the case we might expect to find a range of intermediate forms that reflect the continuing evolution o f electroreception within orders of the Teleostei. Such intermediates have not been round so far. However, they m a y be rare and our systematic survey too m e a g e r to have discovered such taxa, if they exist. We stated earlier that electroreception is only found in three of the 33 orders of teleosts. H o w intensively other workers have looked for it we d o n ' t k n o w , except that the effort must have varied widely a m o n g orders. W e have looked and failed to find electroreception, with the A E P method, in one or more species of six orders (cypriniforms, anguilliforms, ~ salmoniforms, synbranchiforms, osteoglossiforms* and perciforms). Such negative results, although not definitive, support the presumption that electroreception is exceptional. However, the sample of species and families is too small for such a heterogeneous g r o u p as the teleosts; surprises m a y still turn up.Z}: The octavolateral system o f sensory receptors and brain centers has evolved *Earlier reports from cardiac conditioning studies of high sensitivity (fractional p.V cm ~) in anguilliforms and salmoniforms have not been confirmed but newer cardiac conditioning studies7 have found sensitivity higher ( fractionahnV crn ' ) than for other non-electric fish. Closer study of the lateral line receptors of these orders is needed.

53 special modalities for water movement, vibration, acoustic stimuli, acceleration in each plane, head tilt in each plane, and electric fields o f different kinds. Some of these modalities have been relatively stable for a long time but most have c h a n g e d repeatedly in vertebrate evolution. This promises to be fertile ground for new work including anatomy, physiology, development and behavior.

Reading list 1 Bodznick, D. A, and Northcutt, R. G. (1980) Brain Res. 195,313-322 2 Bodznick, D. A. and Northcutt, R. G. (1981)Science 212.465-467 3 Boord. R. L. and Campbell. C. B. G. ( 1977)Am. Zool. 431-491 4 Bullock, T. H. (1974) in Handbook of Sensory Physiology 111/3 (Fessard, A.. ed.), SpringerVerlag, New York 5 Bullock, T. H (1979) J. Physiol. (Paris) 75, 397-407 6 Bullock, T. H. (1981) Neuroscience 6, 1203-1215 7 Bullock, T. H. (1982)Annu. Rev. Neurosci. 5. 121-170 8 Bullock, T. H., Hamstra, R. H., Jr. and Scheich, H. (1972)J. Comp. Physiol. 77, 1-22 9 Fritzsch, B. Naturwissenschafien (in press) 10 Heiligenberg, W. and Bastian. J. (1980)J. Comp. Physiol. 136. 113-133 11 Heiligenberg, W. and Bastian, J. (1980)Acta Biol. Venez. 10, 187-203 12 Hetherington, T. E. and Wake, M. H, (1979) Zoomorphology 93,209-225 13 Hopkins, C. D. (1976)J. Comp. Physiol. 111. 171-207

14 Hopkins, C. D. (1980) Behav. Ecol. Sociobiol. 7, 1-13 15 Hopkins. C. D. ( 1981) Trends NeuroSci. 4, 4-6 16 Hopkins, C. D. ( 1981)Am. Zool. 21, 211-222 17 Kalmijn, A. J. (1974) in Handbook ofSenso O' Physiology IlI/3 (Fessard. A., ed.), SpringerVerlag, New York; and personal communication 18 Lissmann, H. W. (1958) J. Exp. Biol. 35, 156-191 19 Mago-Leccia, F. M. (1978)Acta (ient. Venez. 29. Supl. 1,5-89 20 McCormick, C A. (1978) Doctoral Dissertation, University of Michigan 21 McCormick, C. A. (1981)J. Comp. Neurol. 197, 1-15 22 McCormick. C. A.J. Morphol. (in press) 23 Nelson, J. S. (1976l Fishes of the World, John Wiley and Sons, New York 24 Northcutt. R. G. (1980) Zentralbl. Veterinaermed. Reihe C 9, 289-295 25 Northcutt, R. G., Bodznick, D. A. and Bullock. T. H. (1980)Proc. Int. Union Physiol. Sci. 14. 614; and Bodznick, D. A.. Northcutt. R. G. and Bullock, T. H. (in preparation) 26 Scheich. H. ll977)J. Comp. Physiol. 113, 181-255 27 Szabo. T. (1974) in Handbook of SensoO' Physiology 1HI3 (Fessard. A., ed.). p. 13, Springer-Verlag, New York

T. H. Bullock is at the Neurobiology Unit, Scripps Institution of Oceanography and Department of Neuroscience, School of Medicine. University' of California, San Diego, La Jolla, CA 92093. U.S.A., R. G. Northcutt is at the Division of Biological Sciences. University of Michigan Ann Arbor, MI 48109, U.S.A. and D, A. Bodzntck is at the Department oj Biology, Wesh,van I,'nil'ersi0 Middletown. C1" 0~5457. U.S.A.

Language behavior in stroke patients Cortical v. subcortical lesion sites on CT scans Margaret A. Naeser

In stroke patients with aphasia large differences in hmguage behavior are observed with different left hemisphere lesion sites. The use o f computerized t o m o g r a p h y ( CT) has recently enabled more precise in-vivo analysis o f neuroanatomical lesion sites. In this article sample language behavior and C T scan lesion site patterns are presented f o r two cortical and two new subcortical aphasia syndromes. The combination o f careful assessment o f language behavior a n d detailed inspection o f C T scan lesion sites is contributing toward advances in diagnosis, treatment and prognosis in stroke, ,~Recentl), we ha',e lbund high sensltiviD electro,reception b} AEP in one genus. Xenomystus. but as well as toward a better understanding o f the relationship between language not in another, Notopterus. belonging to the non- behavior and brain structures, both cortical and sabcortical. electric order Osteoglossiformes. The electrosensory The advent of CT scanning in 1973 has including sentence production, comlateral line lobe is found by M. R. Braford and R.G.N. prehension, repetition, reading, writing and to be peculiaril) specialized histologically in greatly enhanced our ability to understand naming. Different lesion sites in the brain Xenomvstus but not in Notopteru~, Osteoglossum. the relationship between different lesion sites in the brain and different forms of will affect these aspects of language in difPantodon or Hiodon. aphasia*8.9, n.l~. The most c o m m o n cause ferent ways. This paper presents sample CT ~Galvmlomxi~, appears not to overlap with elect'oscans and brief descriptions of the abnormal reception, even ,a,ith the special cases of high of aphasia in adults is stroke, e.g. occlusion language for four different types of aphasia threshold electroreception. The most sensitive fish of cerebral vessels. In order for a patient to - two well-known conical aphasia synreportedc' have a first reaction at ca. 5 mV cm a. The be diagnosed as aphasic, he must demonsite of action of galvanotaxis has not been settled. dromes ~a4 and two newer subcortical strate problems in all aspects of language.