convergent designs for electrogenesis and...

Convergent designs for electrogenesis

Carl D Hopkins

and electroreception

Cornell University, Ithaca, USA

New- and old-world tropical electric fish lack a common electrical ancestor,

suggesting that the mechanisms of signal generation and recognition evolved

independently in the two groups. Recent research on convergent designs for

electrogenesis and electroreception has focused on the structure of electric

organs, the neural circuitry controlling the pacemaker driving the electric

organ, and the neural circuitry underlying time coding of electric waveforms.

Current Opinion in Neurobiology 1995, 5:769-777

Introduction

Ethologists and neuroethologists have been fascinated

by electric fish and by the evolution of an entirely

novel electrosensory modality ever since Hans Lissmann’s

discovery of ‘weak electrogenesis’ in the monnyriform

fishes of Africa in 1951 [l] and his subsequent discovery

of active electrolocation (the sensing of objects in the

environment as distortions in the electric field generated

by a fish’s own electric organ discharge) [2,3]. We

now know that the electric sense is used for electrical

communication [4-6,7”], for passive electrical sensing

of prey [8], and for active electrolocation [9,10].

Electric fish provide a good model system in neuro-

ethology for several reasons: there are many species

to compare in new- and old--world groups; electric

behavior is novel and inherently fascinating; the modality

is convenient to work with physiologically; and there

are many parallels between the electric sense and

audition Ill]. This review focuses on recent research

that examines convergent designs for electrogenesis and

electroreception in new- and old-world fresh-water

tropic.11 fish.

Phylolgeny and electrogenesis

Key to any comparative neurobiological study is a good

comprehension of the phylogenetic relationship between

the organisnu in question, and the recent explosive

growth of cladistics coillbined with new molecular

techniques has had a clear ilnpact on the field of

neuroethology. It is now clear that the two main

group:; of fresh-water electric fish, the Mornlyriformes

(Osteoglossomorpha, Teleostei) from Africa and the

Gymnotiformes (Ostariophysi, Teleostei) from South

America, are distantly related but do not share a common

electrogenic or electroreceptive ancestor 12,121; however,

each of these two groups has a sister group of fish

that has arnpullary electroreceptors but no electric

organs [4,12]. In spite of the phylogenetic distance,

both the mormyrifornls and gynmotifornls include

wave- and pulse-discharging species. I3oth groups have

pulse-discharging species that generate complex electric

organ discharge (EOD) waveforms. They also both have

three types of electroreceptors with distinct functions

and separate pathways, and both use their electric organs

for electrolocation and communication.

The parallels between the two groups run even deeper

when looking at the cellular basis for behavior. Several

new studies [15-191 have explored the mechanisms

of electrogcnesis, particularly the production of con-

plcx EOD waveforms. As an electric discharge is

an electrostatic field and not a propagating wave,

EOD waveforms are unaffected by echo, reverberation,

refraction, reflection or any other phenomenon affecting

propagating waves (such as sound) [ 131.

Gymnotiform electric organs

Dut how does the electric organ generate something

more complex than a simple, biphasic, spike-like

discharge that one would expect from the sequential

activation of the caudal and the rostra1 faces of

simple electrocytes [14]! Some of the South American

gynmotiforms, such as Gyrtmtrrs rrlmpo, can generate

a triphasic EOD by firing a subset of electrocytes

slightly out of phase with the rest of the population

[l&19]. Electrocytes near the head have a specialized

Abbreviations

AMPA-cc-amino-3-hydroxy--5-methyl-4-isoxazole proprionic acid; BCA nucleus-bulbar command-associated nucleus;

ELa--exterolateralis pars anterior: ELL-Glectrosensory lateral line lobe; ELvxterolateralis pars posterior; EOD-electric organ discharge; CABA--y-aminobutyric acid; ICL-inner cellular layer; ITD-interaural time difference; MRN-medullary relay nucleus:

NMDA-N-methyl-D-aspartate; PPn-pre-pacemaker nucleus; PPn-c-‘chirp’ part of the diencephalic PPn; PPn-g--gradual frequency shift region of the PPn; SPPn-sub-lemniscal PPn.

0 Current Biology Ltd ISSN 0959-4388 769

770 Neural control

(b) EOD waveform

(iii)

~

(0

(ii) 04

Fig. 1. Complex EOD waveforms generated by a South American electric fish. (a) The gymnotiform Gymnotus carapo generates (b) a complex EOD waveform with four components: (i) an early gradual

head negativity, (ii) a strong head-negative peak, (iii) a head-positive peak, and (iv) a head-negative peak. The head-positive peak (iii) re-

sults from the synchronous discharge of the posterior faces of the majority of the electrocytes in tubes 2, 3 and 4 of cells in the elec-

tric organ, which receive innervation from the anterior or posterior electromotor nerves. The final head negativity (iv) arises from the inward current through the anterior faces of these same elec-

trocytes, which have become depolarized by the passive current flow through them from the posterior face. Early head negativity (i) is caused by inward current through the anterior faces of the electrocytes in tube 1; these are innervated on the anterior side from

nerves with a shorter conduction time to the electric organ. These specialized electrocytes generate a local head-negative discharge, which precedes the’main EOD in the tail. Adapted from 1151.

the typical posterior

pathway from the

rostra1 faces of the

head negative; this

in the tail, which

anterior innervation in addition to

one, plus a shorter conduction

pacemaker. This ensures that the

electrocytes fire first, making the

occurs before the electric organ

is caudally innervated, goes head-positive and then

negative again (Fig. 1) [15]. An elegant series of recent

papers details the complexity of the electric organs in

Gyrrrnot~s carapo and the patterns of innervation and

motor control [15-191. Other gymnotiforms, such as

Stcatqcnys elegans, Hypopygus lepk4rus and Rhanrphichthys

achieve multi-phased EODs using electrocytes located in

accessory electric organs on the underside of the head

[14], in addition to the main organ in the tail.

Heterogeneous electric organs, accessory electric organs

and simple electric organs are more interesting when

viewed in the light of phylogeny. Alves-Games et

al. [20*] used mitochondrial DNA to construct a

phylogeny for the gymnotiform electric fish of South

America to re-examine relationships among the pulse

gymnotiforms (Fig. 2). Pulse discharges appear to

have arisen independently in the families Gymnotidae

(Gymwotus) and Electrophoridae (Electrophoms), and

then again in the Hypopomidae/Rhamphichthyidae

families. Especially interesting is the apparent clade

composed of the genera Gyttrnorhatrrphichfhys, Rhatrr- phichthys, Hypopyg14s and Stcatqerrys, all of which have

accessory electric organs in addition to the more

typical electric organ located in the long tail. All

the fish in these four genera produce complex EOD

waveforms containing three or even four major peaks

(Fig. lb). By contrast, fish in the genera Bra~hyllypoporrrfrs

(formerly Hypopotwus) and Microstcrnarchus do not appear

to have accessory electric organs, and their EODs are

very simple, being composed of biphasic waveforms.

The revised phylogeny based on molecular data shows

that these complex accessory electric organs may have

had a single common evolutionary origin rather than

multiple unrelated origins, as suggested by the traditional

phylogeny.

EODs

j _ , ~ -1/ Brachyhypopomus

Fig. 2. A recent phylogenetic analysis of the gymnotiform elec . . tric fish of South America derived from analysis of sequences of mitochondrial DNA. This analysis demonstraies a closk relation-

ship between the genera Rhamphichthys, Gymnorhamphichthys, Steatogenys, and Hy~_‘opygus, whereas previous traditional mor- phological studies had placed the last two closer to Brachyhy- popomus and Microsternarchus in a separate family (Hypopomi-

dae; !ight shading). The revised phylogenetic analysis is consistent with the common presence of accessory electric organs in Hypopy- gus, Steatogenys, Cymnorhamphichthys and Rhamphichthys. The

accessory electric organs found on the underside of the head are re- sponsible for generating the early head-negative phase of the EOD (indicated by arrows). Adapted from [20**].

Mormyrid electric organs The 200 species of African mormyrids are well

known for their EOD diversity [5,21] and for gener-

ating monophasic, biphasic, triphasic, inverted tripha-

sic and even four-phase EOD waveforms (Fig. 3).

Recently, Alves-Games and Hopkins (J Alves-Games,

CD Hopkins, unpublished data) generated a partial phylogeny of the A&can mormyriform electric fishes

using mitochondrial DNA, and the phylogeny was

used as a framework to re-examine the evolution of

their complex electrocyte morphology (Fig. 4). The molecular phylogeny suggests that primitive electric

Convergent designs for electrogenesis and electroreception Hopkins 771

(a) Stalkless (b) Non-penetrating stalk, posterior innervation

(c) Penetrating stalk, (d) Inverted (e) Doubly penetrating anterior penetrating and non-penetrating innervation stalk, posterior stalk

innervation

EODs -- &______;,_______+;;o&_____:_

Petrocephalus Brienomyrus

bovei sp. 5 Morm yrops zanclirostris

Pollimyrus isidori

Fig. 3. The electric organs of the mormyriforms are composed of electrocytes oi varying degrees of complexity, depending on the species.

(a) Stalkless electrocytes, found only in Gymnarchus niloticus, are innervated on the posterior side, and only the posterior face fires a spike. The anterior face is deeply convoluted, has a high capacitance, and does not fire a spike. The EOD is a monophasic, head-positive pulse. (b) Non-penetrating stalk electrocytes are found in Petrocephalus, Mormyrus and several other genera, including Brienomyrus; the stalk is innervated on the posterior side. The EOD is biphasic, as the posterior face fires an action potential first, and the anterior face follows.

(c) Penetrating stalk electrocytes have anterior innervation, and are widespread in the genera Marcusenius, Gnathonemus, and Brienomyrus. The EOD is always triphasic, although the initial head negativity may be notireable only on expanded gain (thin line in upper trace). The initial head negativity is caused by the inward-directed current in the stalk, which is directed in the posterior direction when the stalk action potential reaches the point of penetration. The large head positivity is generated by the firing oi the posterior iacc, whereas the final head negativity results from the firing of the anterior face. (d) Inverted penetrating stalk electrocytes have EODs that are correspondingly inverted in polarity; they are iound only in the genus Mormyrops. (e) Doubly penetrating and non-penetrating stalk electrocytes are innervated on the posterior side, and are found in the genera Stomatorhinus and Poollimyrus. The EOD in Pollimyrus isidori has an early head positivity that

precedes the main biphasic pulse and is thought to arise from the anterior-directed current into the stalk on the posterior side oi rhe electroryte, and the posterior-directed flow on the anterior side. The main biphasic disrharge that follows is probably produced hy rhe posterior iace and then anterior face oi the electrocyte itself. Adapted from [Shl with data irom [X*1.

orgasms were stalkless, but then evolved into stalked

and theu penetrating-stalked; however, reversion to

non-penetrating stalks may have occurred several times

in various different genera (Fig. 3).

Electric skates

A similar story emerges from R recent investigntiou of

the morphology of electrocytes in 63 of the -200

known species of electric skates (&joi&i), which

demonstrate R diversity of electrocyte types, including

cup-shaped, modified cup-shaped, intermediate-shaped,

and disk-shaped [22*]. Th ese different electrocytcs

generate J phylogeny fully cmlsistcnt with phylogcnics

derived iron1 other characteristics [23]. Much remains to

be learned, howcvcr, about the functional significance

of sk.~te electric discharges. Indeed, only a few species

have ever been recorded electrically, even though they

appear to have fully functional electric organs in their

tails: in some species, the EOD is important in social

com~~lunicatio~~ 1241; in others. where the discharges are

species specific, EODs mny be used for species and sex

recognition (13 Bratton, personal coiiiniuilicatioii).

Until recently. only one type of catfish, ~Vlalap~cn4nrs

cktriws, was known to be elcctrogenic; however, in

19’90, Hagedorn ct al. [25] described very weak electric

discharges in several spccics of Syrmdorrrir catfish (family

Mochokidnc). This ycnr there were additional reports

of siulilar electric discharges in ccvernl other Afiiicnn

catfish, including tmro nlore species of- Syrr&rrti.\- and

oue of Cltni~x. Baron nnd colleagues [26*,27*] report

1 (t20 ins duration, 150 pV ci~i~l electric signals from

Clarios catfish during ngouistic cncouuters. The authors

suggest that these discharge\ arc not mere artiiacts of

muscle activity, but that they sc’rvt‘ as socinl signals,

which x-c‘ detected by nmpullnry clcctroreccptors. Thex

ut’w studies raise the interestiug pos&ility of a rclativclv

uncsplored world of very wcnk (i.e. pV cu-1 instead of

nlV cm-l), very low frequency (i.e. less than 50 Hz peak

spectral energy) electric discharges being used iu social

internctions nmoug cntfish, which hnvc traditionnlly been

viewed ns electrically silent.

772 Neural control

\

Fig. 4. Partial phylogeny of the mormyriform electric fish from Africa, derived from analysis of mitochondrial DNA sequences, revealing a progressive evolution of complexity of the electrocytes in the electric organ. The osteoglossomorphs, Pantodon and Notopter~s, are inc ludcd for outgroup comparisons. Gyrnnnrchus niloticus is the most antestral mormyriform, with tlosest affinity to P,~nfodon and Notoptcru, JIKI

it has a simple electric organ, with no stalk. Petrocephalus is the most primltlve of the Mormyridae from this analysis and the osteology. It\ electric organ is composed of simple, non-penetrating stalk electrocytes and the EOD is correspondingly hiphasic (see Fig. 3). Most of thtx remaining species on the chart have electrocytes with penetrating stalks with corresponding triphasic EODs, except for two of the tlricwmyrur, which have apparently reverted to non-penetrating stalks. Adapted from (J Alves-Comes, CD Hopkins, unpublished data).

Neural control of electric discharges

Orle of the most active nrcas of electrogenesis resenrch

has been the elucidation of central control mechanisms

for the patterns of electric discharges used in n variety

of behavioral functions such as social communication

(including threats, retreats, courtship nnd alarm), novelty

responses, general alcrtillg responses, and the jnmnling

avoidance response. Much of the work in this nrcn

began with the pioneering efforts of the late Wnltcr

Heiligenberg to study the neural circuitry behind

the jnmming avoidance response iI1 the gymlotiform

E@wrrrartrricl (reviewed in [ 101). Heiligenberg wanted

to determine how electrosensory inputs are cm&ted

into motor commands to accelerate or decelerate the

nlcdullary pnccmaker; however, work in this field during

the past 10 years has led to nn understanding of 3 far more con~plec list of electromotor behaviors,

including social signals. Severnl rcccnt papers outline the

complex mture of the connections illvolvcd ill thcsc

behaviors (J Alves-Games, CD Hopkin\. uupublisbcd

data; [ 10,28”,2c,“,3(t37.n8”,3’)]).

It is known that in the context of social bchnvior.

gyninotiforms and monnyriti,nns nlodulnte the output

of their electric organs in 3 variety of ways [ 5.0.7”. 101. For example, during courtship, mnlc I:‘[ycrrmlrrrrii1.

who normally produce R 3O(t500 Hz steady ~vnvc

discharge, generate brief (l(~100 111s) ‘intcrruptlon~‘ of

the discharge, which nppenr to stimulntc thr fcn~alc

to approach 2nd ~pam [-Co,4 I]. hth ~lnlec .IIK~

fen&s also make brief ‘interruptions’ or ‘chirps’ .I\

threats [40,42]. Subordinate lii,qcvrlrrrurrrria clcvntc their

EOD frequency by less than 20 Hz in ‘long rim’

(lasting for seconds) [40]. Finally, fcmnlr fish \vill often genernte slow up-ml&down wnrbling Illodulations


of their EOD frequency by lO-20Hz, which may

last for seconds or minutes during courtship and

egg laying [41]. The pulse-discharging fish from the

Bra~/ryllypclpc,,rlf~~ genus generate several displays: brief

silences (interruptions) for threat signals; long silences

as alarm signals; partial, or ‘noisy silences accompanied

by ‘hissing’ background discharges of unknown function;

and a rich range of frequency modulations during social

behavior, including sudden increases in EOD frequency

followed by decreases; and ‘chirps’ [35,40,43]. With a

decade of work including horseradish peroxidase studies,

intracellular recording, glutamate iontophoresis, im-

munocytochenlistry, pharmacological investigation and

electron microscopy, man)- of these display patterns nlny

be described in terms of neural circuitr)

Electric

organ

Brzchyhypopomus

Frequency rises

Electric organ

Fig. 5. Summary of pacemaker cell control in two species of gymnotiforms that illustrates separate pathways for controlling different electrical behaviors, inc-luding frequency rises and falls in the jamming avoidance response (JAK), chirps and Interruptions. Although there are similarities between Eigenmnnnia and Bra<-hy- hypopomu\, the GABA system in Br,7rhyhy~opon,us wems to he absent in Eigenmnnnia. Adapted from [44].

Figure 5 gives schematic diagrams of the neural control

mechanisms for two species of gynmotiforms, and

focmes ou the pacemaker nucleus in the medulla, which

is composed of two ~~11 types: so-called pacemaker

cells, which are intrinsic to the uucleus and seem

to generate the rhythm; and relay cells, which were

orlglnally thought to pass ou the pacemaker’s rhythm

to tble spinal cord, but which are now known to be

the site of additional nlodulation. With no input fro111

higher centers, the pacemaker cell fires at a regular

rate, and rlie relay cells and electric organ follow

in a o11e-tc>-one manner. Modulatory inputs derive

from two sources, a pre-pacemaker nucleus (1’1’11) in

the dienccphnlou and a sub-lcnmiscal pre-paccnlnker

nucleus (SPPn) in the midbrain. These pathways were

first identified by retrograde transport from injections

of horseradish peroxidase into the pacemaker, and the

iunctional sub-divisions were studied by highly localized

iontophoretic injections of glutnnlate into the pre-motor

nuclei combined with pharmacological blockers applied

to the pncenlakcr itself 1441.

The 6st acceleration or ‘chirp’ of the EOD frequency,

used in the context of threat behavior and male

courtship in I~rclfllylly~o~~orrlrr~, aud the fast acceleration

and decrease in anlplitude in the homologous ‘chirp’ of

E@vrrrrarrrria cau be produced by a depolarization of the

relay cells from neurons originating in the ‘chirp’ part

of the diencephalic pre-pacemaker nucleus (PPrl-c). The

synaptic inputs onto relay cells are glutamergic and the

receptors are of the AMPA type.

The gradual acceleration of the EOD frequency-

signaling general arousal and correlating with an increase

in motor activity-in Rru~12ylly~~‘I”‘I”‘“lf’L, and the slow

long ti-equency rise given in the context of submission

and the jamming avoidance response in I~iymrrmrrin, can

be generated by excitatory iuput into the pacemaker

cells from the gradual frequency shif? region of the

PPn (PPn-g) in the diencephalon. Again, with honlo-

logous neural pathways, but not necessarily behavioral

contexts, PPn-g inputs activate NMDA receptors on

the pacemaker ccl1 dendrites, causing a depolarization of

pacenlakers and an increase in the EOD rate [36].

nr~r/ly/tyl,c)E,c)rtll~~ can slow its discharge frequency, and

even turn it of’f conlpletely for short or long periods

of time, to hide from predators or unknown stimuli,

or to signal submission to more dominant fish 13.51.

I3ycrrrrrarrrriti shows neither the behavior nor the neural

pathway for stopping. Kawasaki and Hciligenberg [X.5]

found that nr~r/tylrM”‘po”‘rts has a unique inhibitory

pathway (contain+, GABA) t i-on1 the PPn-i nucleus

to the pacemaker. I~r~lfllyllyl)c’l”)f’tl’2‘ cau suddenly shut

off its discharge frequency for a brief period without

slowing the discharge rate before shutting off, and this

is controlled by descending inputs froul the midbrain

SPPn, which terminates on NMDA-type receptors on

the relay cells (38**,45”]. A similar pathway causes the

downward frequency shift of the Jamning avoidauce

response in Eigcwrrr~~rrrric 134]. In Zi&rrrrr~rrrricl, the gradual

deceleration of the EOD frequency in the context of

the jnniiiiing avoidance rcsponsc derives froiii the more

recently discovered Sl’l’n in the nlidbrain, with NMI)A

inputs direct 011 to the relay cell\ in the paceulaker.

A homologous pathway in I~n~r/~y/~y~~o~~or~~~~~ produces

sudden interruptions [X3”].

We know much less about the inputs to the pacelllaker -

cells ior the Ah-mu electric fkh, and little i\ known

about the control of patterm of electric discharges,

where the inter-pulse interval zequmce\ have been

described ethologically as bursts, stops, regularized

pulses, scallops, variable pulses. etc. [7”.21,46]. T’hc

medullary pacemaker of mornlyrids ib composed of a

conunand nucleus connected directly to a medullnry

774 Neural control

relay nucleus (MRN), which is connected to the spinal

electromotor neurons in the spinal cord in a way similar

to the gymnotiforms. A collateral pathway, described

by Bell ef al. [47], sends neurons from the command

nucleus to a lateral bulbar command-associated (RCA)

nucleus, which in turn projects back to the MRN. But

inputs into the command nucleus, described briefly by

Bell cl a/. [47,48], have not been explored in the same

detail as those in gymnotiforms. Mormyrids differ from

gymnotiforms by having a corollary discharge pathway

that synchronizes the electrosensory processing in the

hindbrain electrosensory lateral line lobe (ELL). Recent

studies have focused on the collateral pathway to the

BCA nucleus (the origin of the corollary discharge

[28”,29”]), which plays an important role in gating

electrosensory inputs and the plasticity of electrosensory

processing in the ELL.

In a recent paper, Kawasaki [4Y] demonstrates that

the ancestral mormyriform, Gymarch rlilotinrs, the

only African electric fish with a wave-like discharge,

completely lacks a corollary discharge in the brain,

although it does have a connection between a command

nucleus in the medulla and a lateral relay nucleus, which

may well be homologous to the BCA nucleus described

by Bell rt a/. [47]. Unlike mormyrids, these fish lack a

direct connection between the command nucleus and

the immediately adjacent MRN. In Gyrrrr~arhrs, nothing

is known of the modulatory inputs into the command

nucleus, nor the mechanism of control of discharge

patterns that play a role in conlnlunicatioII.

Temporal coding and electrosensory circuitry in

the brain

Along with the auditory systems of barn owls and

echolocating bats, the electrosensory systems of electric

fish have been neuroethological favorites for exploring

time coding and time comparison. In a recent review,

Carr [ll] compares the mechanism by which the owl

gains sensitivity to interaural time differences (ITDs),

and a similar mechanism by which E@wrrraru/ia senses regional phase differences in electric stimulus waveforms

(differential phase). Both systems rely upon neural delays

combined with coincidence detectors to produce a

narrowly tuned differential phase or ITD sensitivity, and

both show extreme specializations for reducing temporal

jitter and high-speed conduction, up to the point of

phase comparison. The time-coding pathway in the

gymnotiform &ycnrrranrlia is shown in Figure 6a.

Recent studies of time coding among the African

electric fish have demonstrated at least two convergent

pathways for decoding temporal information among

the mormyriforms: one for detecting the duration of

pulse waveforms among mormyrids (Fig. 6b) (S Amagai,

personal communication; S Amagai, MA Friedman,

CD Hopkins, unpublished data; [50,51,52j) and one

for detecting differential phase in Gyrr~rzardrrtr (Fig. 6~)

[5P]. From behavioral studies, we know that temporal

cues are important in recognizing pulse duration, and

mormyrids often have species- and sex-specific EOD

waveforms [13,21,54]. EOD waveforms are encoded

as a pattern of two to three spikes by the Knollenor-

gan receptors, with spike timing determined by the

waveform of the stimulus. Different parts of the body

surface respond to one phase of the stimulus or to a 180” phase-shifted EOD [13]. The Knollenorgan receptor

afferents converge on large diameter spherical cells in

the nucleus of the ELL [SO], where the cells project

bilaterally to the midbrain nucleus exterolateralis pars

anterior (ELa). Here, timing information from ditf^ercnt

parts of the body surf&e is compared. The inputs

terminate on the two cell types in the ELa: a large cell

intrinsic to the nucleus, and a small cell projecting from

the ELa to the adjacent nucleus, the exterolateralis pars

posterior (ELp). Large cells are GABA-ergic, and their

terminals are on the cell bodies of the small cells [ 511.

Recently, Amagai cl (II. (S Amagai, personal colll-

munication; S Amagai, MA Friedman, CD Hopkins,

unpublished data; [52]) have recorded from a&rents

arriving in the ELa, from large cells in the ELa, and

from cells in the ELp that receive inputs from the

small cells. It has not yet been possible to record t&m

the small cells, so it is unknown how they respond to

waveforms of different duration. Amagai rt a/. (S Amagai,

MA Friedman, CD Hopkins, unpublished data) suggest

that the presence of GABA in the large cells changes the

flmction of the ELa from a delay-line coincidence model

to a delay-line blanking model in which throughput to

the ELp is inhibited if the duration of the pulse is greater

than a given minimum. Thus, there may be direct input

from afTerents to small cells, which becomes inhibited if

preceded by a minimal delay by an input from a large

cell f^rom another part of the body surf&e. Amagai ct cl/.

(S Amagai, MA Friedman, CD Hopkins, unpublished

data) suggest an anatomical arrangement within the ELa

that could map stimulus duration onto position within

the nucleus. At the next higher level in the time-coding

pathway, Amagai (S Amagai, personal conlnlullication)

finds cells that are tuned to specific stimulus durations,

and are thus excellent candidate cells designed to respond

to specific EOD waveforms used for species recognition.

III a very recent study of Gyrrrr~arhs. Kawasaki and (iuo

[We] found cells in the hindbrain that are tuned to

differential phase, and that probably play a vital role

in the phase component of the jamming avoidance

response. The authors recorded from primary ‘S’-type

electroreceptors, which phase lock to the 400 Hz EC)D

stimulus. to show that the primary afS:rents terminate

directly on giant cells in the ELL, as well as sending

terminals up into the inner cellular layer (I(:L) of the

ELL medial zone. Intracellular fills that cross to the

opposite side of the ELL show both ipsilateral .md

contralateral projections from the giant cells into the

ICL. It is here that the authors recorded from cells in the

ICL that are sensitive to differential phase in the o&r of


(a) Eigenmannia

Delay

Electro- t

Phase A t

Phase B receptor

T-receptor

(b) Brienom yrus

Delay --__

,l

-------------~ Phase A

u fl Electrotonic synapse 0 Giant cell 0 Large cell

---o Inhibitory synapse 0 Spherical cell 0 Small cell

(c) Gymnarchus

Phase A - Phase B

4

S-receptor

Fig. 6. Time-coding pathways in the gyrnnotiform Eigenrnannia compared with those in the mormyrids, Brienonlvros ancl Gymnxc-bus. (a) In Eigerxmannin, the time-coding elcctroreceptor (T receptor) projects to spherical cells in the ELL. The spherical cell3 send axon, to the midbrain torus layer VI where they terminate on the distal dendrites of small tells, and on the somata oi giant cells. Giant cells send large axons to distant small c-ell targets. Small cells presumably act as coincident detectors, and fire only when the phase oi the stimolu3 in body region A (phase A), differs from the phase of the stimulus in body region B (phase B), by a precise time difference. (b) The Hrierromyrus time-coding pathway bcglns in the periphery wtih the Knollenorgan receptor, and leads to the spherical c-ells in the nucleus of the ELL (nELLI In the hindbrain. These giant cells project bilaterally to the ELa oi the midbrain where they terminate on large and small cells with elcctrotonic synapses. The large cells, whir-h are CABA-ergic, terminate on small cells within the nucleus. Rather than being coin<-idenc-c detectors, the small cells appear to be selectively blanked, depending on the delay oi the inhibitory input iron1 the large cells. (c) The Gyrnnnrchus time- c-(ding pathway resembles the Knollenorgan pathway only remotely. The S-receptor, which is phase-locked to the EOD \timulus, sends large axons to terminate on giant cells in the ELL, but collaterals alsu terminate In the ICL oi the ELL where differential phase-sensitive tells are found. Giant tells also send axons to tonverge on the same tell layer, and although the circuit is unknown, the cells in the ICL appear to be acting; as coincident detectors. Temporal analysis is accomplished entirely in the hindbraln In Cymnarch~. D,lta irorn (S Amagai, personal tomnlun,tJtion; S Amagal, MA Friedman, CD Hopkins, unpublished data; 151 ,52,5$‘*,57]).

tnicrosecolids. AS yet, the inputs to the IC:L cells have Ilot

been dctcrGted, but it is known that these cells do not

rupond to absolute phase diffcrcnccs as do E@rtrrrurrri~I

cells. Instead, they ndapt to steady-state shitis in phase

differences over a range ofcevernl hundred trticroceconds,

yet cSontirntc to show sensitivity to snull shifts in phncc, tn

the order of nCcroseconds, nt?cr a period of ndnptntion.

Whnt is striking about the rcsttlts in Gyr,rtr&rttz is the

t&t th,~t the diKerentin1 phnsc conipnrisons arc nude in

the hindbrain, not in the niidbraitt, nnd that there ij J

con~~~ti.s\ural pathway ti,r tinte coding itt (Gyrrtrr&ttrx

thnt is not huttd in niornivrids. However, there is Jtttost

cotnplrte sitnilarity in the cotttputntional algorithtn for

the .jaliinting avoidance response between Cyrrtrrtirrlrtrs

xx1 E(qururtrrlrricr. even though the two species evolved

electric orgntis nnd electroreccptors indeperidctitl~.

Conclusions

The cotttparntivc neuroethological work on electric fish

provides an excellent exatiiple of convergent evolution:

not sitnply th:tt electric fish evolved electric organs

jcvernl tinies over, but that the mechanistns of generating couples dischnrges converge on dif&x-ent solutions to

the snnlc probletn. Not only did electric comtnunication

evolve sepnmtcl~ in several groups. but there xe

also parallels in the rhythtn control nicchnttisnis in

paceniakcr. Not only are time codes important in

the independently evolved groups. but the sensory

processing of temporal cues has converged on similar

cotnputntional nlgorithtns. These studies deniottstrate

that electric fish continue to provide &tile ground

for cotiipnmtivc studies, and the evolurionnry process

776 Neural control

continues to provide surprises for the researcher willing

to do comparative studies.

Acknowledgements

I thank Matthew Friedman and Gamy Harned for help with

the figures and for fruitful discursions during the pnqxw~~tion of

this review. Supported by grant #MHZ37972 from the Ndtional

Institute of Mental Health.

References and recommended reading

Papers of particular interest, published within the annual period of

review, have been highlighted as:

. of special interest

. . of outstanding interest

1. Lissmann HW: Continuous electric signals from the tail of a fish, Cymnarchus doticus Cuv. Nature 1951, 167:201-202.

2. Lissmann HW: On the function and evolution of electric organs in fish. J Exp Biol 1958, 35:156-l 91.

3. Lissmann HW, Machin KE: The mechanisms of object location in Cymnarchus niloficus and similar fish. / Exp Viol 1958, 35:457-486.

4. Bullock TH, Heiligenberg W (Eds): Electroreception. In Wiley

Series In Neurobiology. New York: John Wiley & Sons Inc.;

1986.

5. Hopkins CD: Neuroethology of electric communication. Annu

Rev Neurosci 1988, 11:497-535.

6. Kramer B: Electrocommunication in teleost fishes: behavior and experiments. In Zoophysiology, vol 29. Berlin: Springer-Verlag;

1990.

7. Moller P: Electric fishes: history and behavior. In Fish and . . Fisheries Series. Edited by Pitcher TJ. London: Chapman & Hall;

1995.

A broad survey of electric fish behaviors, including early hlstoncal

references.

8.

9.

10.

11.

12.

13.

14.

15.

16.

Hopkins CD: Neuroethology of electrolocation. ! Camp f’hysiol [AI 1993, 173:689-695.

Hopkins CD: Behavioral analysis of sensory function: active and passive electrolocation. J Camp f’hys,o/ [A/ 1993, 173:688.

Helligenberg W: Neural nets in electric fish. In Compvtafiona/ Neurosr~ence Series. Edited by Sejnowskl TJ, Poggio TA.

Camhridge, Massachusetts: MIT Press; 1991.

Carr C: Processing of temporal information in the brain. Annv Kev Neurosri 1993, 16:223-243.

Finger TE, Bell CC, Carr CE: Comparisons among electroreceptive teleosts. Why are electrosensory systems so similar? In Elertroreception. Edited by Bullock TH, Helligenherg W New York: John Wiley & Sons Inc.; 1986:465-481.

Hopkins CD: Temporal structure of non-propagated electric communication signals. Brain Eehav Eva/ 1986, 28:43%59.

Bennett MVL: Electric organs. In Fish Physiology. Edited

by Hoar W, Randall DJ. New York: Academic Pre\\;

lY71:347-491.

Maradar 0: Motor control of waveform generation in Cymnotus carapo. 1 Camp Physfol [A] 1993, 173:728-729.

Caputi A, Macadar 0, Trujillo-Cen6z 0: Waveform generation of the electric organ discharge in Cymnotus carapo. III. Analysis of the fish body as an electric source. / Camp Physiol /A/ 1989, 165.361-370.

17. Lorenzo D, Velluti JC, Macadar 0. Electrophysiological properties of abdominal electrocytes in the weakly electric fish Cymnofus carapo. / Comp Physiol [A] 1988, 162:141-144

18. Lorenzo D, Sierra F, Silva A, Macadar 0: Spinal mechanisms of electric organ discharge synchronization in Gymnotus carapo. / Comp f’hysiol [A] 1990, 167:447-45X.

19. Macadar 0, Lorenzo D, Vcllut~ JC: Waveform generation of the electric organ discharge in Gymnotus carapo. II. Electrophysiological properties of single electrocytes. / Cornp Physiol (A/ 1989, 165:353-360.

LO. Alves-Games J, Ort; C, Haygood M, Helllgcnberg W: . . Phylogenetic analysis of the South American electric fishes

(order gymnotiformes) and the evolution of their electrogenic systems: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data. Mel Biol Evol lY?5,

12:298-318. This paper suggests a new phylogeny ior gymnotlform elettnc tl\he\

based on sequence data from mitochondrial DNA. The sample ~nc lude\

19 genera and all six iamilies, with six catfish selected ior out-group

comparison. Someofthe results are ronslstent with earlier morphologic al

studies, but this new paper revises relatIonshIps between Eigmrnanni,~

and Stemopygus (by separating Sfcmopygus as an independent groupJ,

and between Hypopomidae and Rhamphichthyidae.

21. Hopkins CD: Behavior of mormyridae. In Elecfrorewpfwn.

Edited by Bullock TH, Heiligenherg WF. New York. John Wiley

X Sons; 1986:527-576.

22. Jacob BA, McEachran JD, Lyons PL: Electric organs in skates: . variation and phylogenetic significance (Chondrichthyes:

Rajoidei). 1 Morphol 1994, 221:45-63. Combining a phylogenetic analysis of the Rajold skates wth an analy\l\ oi the morphology of the electric organ shows how cell types 111 elec trlc

organs correspond to phylogenetlc groupings.

23. McEachran JD, Mijake T (Edsl: Phylogenetic interrelationships of skates: a working hypothesis (Chondrichthyes Rajoidei). In

Advances in the Biology, Ecology, Sysremarics and 9arur ol th(,

Fisheries. NOAA TechnIcal Report. Edited by Pratt HL. (;ruber

SH, Tamuchl T (Series editor). 1990, 90:285-X)4.

24. Bratton H, Ayers 1: Observations on the electric organ discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behavior. Environ Hiol fishrs lY87.

20:241-254.

25. Hagedorn M, Womhle M, Finger T: Synodontid catfish: a new group of weakly electric fish. Wra~n Behav Evol 1 YYO.

35~268-277.

26. Baron VII, Morshnev KS, Olshansky VM, Orlov AA: Electric . organ discharges of two species of African catfish (Synodontis)

during social behaviour. Anim Sehav 1994, 48:1472-l 475

Two species of African catfish in the genw Synodonr,s produce elec trI(

discharges during soctal Interactlonc. Pulses are separated by -lOm\ .~nd

are given in bursts oi 5 to 10.

27. Baron VD: African C/arias catfish elicits long-lasting weak . electric pulses. Experenria 1994, 50:644-647.

The African catilsh C/arias garfepinus produces very weak, very low

irequenry electric discharges when InteractIng in social sltuatlon\

28. Bell C, Van der Emde C: Electric organ corollary discharge . . pathways in mormyrid fish. II. The medial juxtalobar nucleus.

/ Comp Physml [Ai 1995, 177:463%480.

This paper descrthes an electrophysiologlcal examlnatlon ot a wc ond

command pathway In mormynd fish. Lesion\ to the luxt,llobar nut let)\

show that this pathway mediates the major sensory eifect\ 11, the

mormyromast zones of the ELL, and IS probably important in prowdlng

prec 1se tlmlng Information to the lobe.

29. Bell C, IIunn K, Hall C. Caputl A: Electric organ corollary . . discharge pathways in mormyrid fish. I. The mesencephalic

command associated nucleus. / Camp Physiol [Ai 1’195,

1771449-462 Explores the phyw)logy oi the mesencephallc command-aswc bated

nucleus In the mormyrld tish and shows that It IS respowhle ior gatlng

Knollenorgan responws 111 the medulla, tor descending exritatlon 01

granule cells in the mormyrornast zone oi the ELL and lor varlou\

other senwry functions. This command pathuay does not appear to lx


Involved in plasticity of electrosensory responses in the mormyromast

zone

30.

31.

32.

33.

34.

35.

36.

37.

38. . .

Dye JC, Meyer JH: Central control of the electric organ discharge in weakly electric fish. In E/ertrorereptio/l. Edited by Bullock TH, Heiligenberg WF. New York: John Wiley & Sons Inc.; lY86:71-102.

Dye J, Heilrgenberg W, Keller CH, Kawasaki M: Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus. Pro<- MU/ Acad Sri USA 1989, 86:8993-8997.

Heilrgenberg W, Keller CH, Metrner W, Kawasakr M: Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish, Figenmannia: detection and processing of electric signals in social communication. / Comp Physd /A/ 1991, 169:151-164.

Kawasaki M, Maler L, Kose C, Helligenberg W: Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. / Cornp Neural 1988, 276:113-131.

Kawasaki M, Heiligenberg W: Individual prepacemaker neurons can modulate the pacemaker cycle of the gymnotiform electric fish, Figenmannia. / Cornp f’hysiol iA/ 198R. 162:13-21.

Kawasaki M, Heiligenherg W: Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopmus. / Camp Physfol /A/

1988. 165:731-741.

Kawasaki M, Heiligenberg W: Different classes of glutamate receptors and CABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish. / Ncurosc-I 1990, 10.3896-3904.

Rose (;I, Kawasaki M, Helligenberg W: ‘Recognition units’ at the top of a neuronal hierarchy? Prepacemaker neurons in Eigenmannia code the sign of frequency differences unambiguously. / (romp fhysrol [A/ 1988, 162:75Y-772.

Spiro JE. Brose N, Hernemann S, Helllgenberg W: Immunolo- calization of NMDA receptors in the central nervous system of weakly electric fish: functional implications for the modulation of a neuronal oscillator. / Neurocti 1994, 14.6289-6299.

An artlbodv to NMDA receptor< labels the relay cells in the pacemaker-hut not the pacemaker cells themselves--n gyrnnotrtorm tish The rtxrlt\ cupport the physlologlcat tindlngs with NMDA blockers.

39.

40

41.

42.

43

44.

45. . .

Zupanc GKH. Maler L: Evoked chirping in the weakly electric fish Apleronotus leplorhynchus: a quantitative biophysical analysis. Can / Zoo/ 199 3. 71:.?301-2310.

HopkIn\ CD: Electric communication: functions in the social behavior of Eigenmannia virescens. Hehcwour 1974, 50 270.-305.

Hagcdorn M, Herllgenberg W: <:ourl and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Rchab

1985, 33:25&LhS

Hophln\ CD: Electric communication in fish. Am Sri 1974, 62 4Lh~437.

Hagtsdorn M: The ecology, courtship, and mating of gymnotiform electric fish. in Electrorcr eprror?. Edited by Bullock TH. Helllgenherg H. New York: lohn Wiley R Sons tnc; 1986:497~526.

Kawasakr M: Comparative studies on the motor control mechanisms for electric communication in gymnotiform fishes. / C-o!o,np Physiol [A] 1993, 173:726-728.

Kennedy G, Helhgenherg W, Ultrastructural evidence of CABA-ergic inhibition and glutamatergic excitation in the pacemaker nucleus of the gymnotiform electric fish, Hypopomus. / (amp Physrol [A] 1994, 174:267-280.

Using electron microscopy, the authors trace fibers from the prepacemaker in Hy~.‘o~ornus to the pacemaker, and demonstrate the presence oi CABA- and glutamate-immunoreactive synapses on the surface oi pacemaker cells. Only glutamate-irnnlunoreactive synapses are hmd on relay cells.

46. Crawiord J: Sex recognition by electric cues in a sound- producing mormyrid fish, Pollimyrus isidori. Brain Echav Evol

1991, 38.20-38.

47. Bell CC, Libouban S, Sraho T: Neural pathways related to the electric organ discharge command in mormyrid fish. / Camp Neural 1983, 216:327-338.

48. Grant K, Bell CC, Clausse S, Ravallle M: Morphology and physiology of the brainstem nuclei controlling the electric organ discharge in mormyrid fish. / Camp Neural 1986, 245:51 L530.

49. Kawasaki M: The African wave-type electric fish, Gymnarchus . . niloticus, lacks corollary discharge mechanisms for electrosen-

sory gating. / Camp Physiol [A] 1994, 174:133-144. Intracellular recordings tram the pacemaker of Gymnarthus n~lotirus

with single-cell tills demonstrates that Gymnarc-husi has a pacemaker or command cell connected indirectly to a relay cell, but that the pathway runs to a lateral MRN. There is no evidence ot a corollary discharge system in Cymnarthus.

50.

51.

52.

53. . .

Bell CC, Szabo T: Electroreception in mormyrid fish: central anatomy. In E/ectrorecept,on. Edited by Bullock TH, Heiligenberg W. New York: John Wiley & Sons Inc.; 1986:375%4’1.

Mugnaini E, Malet L: Cytology and immunocytochemistry of the nucleus exterolateralis anterior of the mormyrid brain: possible role of CABAergic synapses in temporal analysis. Anat

Embryo/ 1987, 176:313-336.

Arnagai 5: Time coding in the electrosensory system of mormyrid fish [PhD thesis]. Ithac-a. New York. Cornell University; 1993.

Kawasaki M, Cue Y-X: Timing comparison circuitry in the electrosensory lateral line lobe of an African wave-type electric fish, Cymnarchus niloticus. / Ncurosti 1996, in press.

Kecordlngs trorn cells in the ICL ot the ELL I” Gymn~rthus show that there are cells sensitive to phase dliierentes on ditferent parts oi the body suriace. Intracellular recordings demonstrate that afierent fibers converge on the Inputs irom large tells 111 the ELL, and that large cells $cnd collateral\ to the opposrte side tri the ELL. Time comparison appears to take place entirely in the ELL.

54. Hopkrnc C-D, Bass AH: Temporal coding of species recognition signals in an electric fish. Scienct~ 1981, 212:85-87.

55 Hopklns CD: Electric organ discharges and phylogenetic . analysis. tn 4th lnrerna~ional Congrex o/ Neurocthobgy. Edited

by Burror+s M, Matheson T, NeL%,land 1’. Sc huppe H. Cambridge, UK: Ceorg Thrern; 1995:418.

A phylogenetic analysis ot the mormyrldae, with an examination oi the pattern ot evolutlor1 ot electric organ morphology in relation to

phylogeny

56. Bass AH: Species differences in electric organs of mormyrids: substrates for species-typical electric organ discharge waveforms. / (-amp Ncurol 1986. 244:313-3 1:).

57. Carr C-, Herligenherg W, Rose (;. A time-comparison circuit in the electric fish midbrain. I Neurorc-r 1986, 10:3LL7-3246.

convergent designs for electrogenesis and...

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