Theodore Holmes Bullock

Department of Neurosciences, University of California, San Diego, La Jolla, California 92093-0201

Running title: Future of research on electroreception

Correspondence:

T. H. Bullock
Dept Neurosciences 0201
UCSD
La Jolla, CA 92093-0201
USA

Phone: 619-534-3637

Fax: 619-534-3919

E-mail: tbullock@ucsd.edu

Summary
Besides the rounding out of presently active areas, six are selected for predictions of marked advance. (1) Most discoveries will be in cellular componentry and molecular mechanisms for one or another class of receptors or central pathways. (2) More major taxa will be found with electroreceptive species, possibly birds, reptiles or invertebrates, representing independent evolutionary "inventions". (3) Electric organs with weak and episodic electric discharges will be found in new taxa; first, among siluriforms. (4) New examples are expected, like lampreys, where synchronized muscle action potentials add up to voltages in the range of weakly electric fish. Some of these will look like intermediates in the evolution of electric organs. (5) Ethological significance will be found for a variety of known physiological features. Exs.: uranoscopids, skates and weakly electric catfish with episodic electric discharges of unknown role; electroreceptive ability of some of the diverse group having Lorenzinian-type ampullae (besides elasmobranchs) including lampreys, chimaeras, lungfish, sturgeons, paddlefish, and salamanders; gymnotiform and mormyrid detection of capacitive component of impedance. (6) The organization of some higher functions in the cerebellum and forebrain will gradually come to light.

For centuries interest in electric fish has been concentrated on the electric organs and production of the strong discharges in either high voltage or high current species. In recent decades interest has turned to the sensory reception, functions of weak discharges and central processing of electric information. At present more than a score of laboratories in a dozen or so countries are actively investigating the anatomy, physiology, pharmacology, molecular neurobiology, behavior and field biology of electric fish, strong and weak, as well as fish, amphibians and mammals that are electroreceptive but lack electric organs. The other papers in this volume manifest the range and level of sophistication of the current state of knowledge. It is the aim of this contribution both to predict and to influence some of the future directions of research by pointing to opportunities with potential significance for general neurobiology, not only in electroreception but also in the "sensorimotor" control and production of electric discharges.

A. Most of the action in future research will doubtless be in the realms of cellular componentry, molecular and pharmacological mechanisms in each of the classes of sense organs and in the central pathways. Most of these will be germane to general problems of neurobiology, for many of which these animals are especially favorable material.

I will say no more about this active front. Instead, I will hazard predictions and highlight opportunities in several other broad domains.

B. Starting with the evolution of electroreception, I touch only upon its distribution, predicting the discovery of more taxa with electric organs and with electroreception, a sense modality which, more clearly than any other has been independently invented in evolution more than three times. At least two of these three times it evolved with three classes of sensory receptors in the same animal together with corresponding central pathways, not necessarily homologous in the different taxa.

Among the candidates for future discovery of electroreception, wading birds that probe in the mud are obvious possibilities. So are aquatic reptiles. Among mammals, so far only the monotremes have given convincing evidence of possessing this sense modality (Pettigrew, this volume). One of the largely aquatic insectivores, the star-nosed mole, has been a candidate but, so far, the negative results are more convincing than the positive claims. Other species ought to be examined, using quasi-natural electrical stimuli. Ideally this should be done behaviorally. A very close second best is physiological and recording averaged evoked potentials in the midbrain is usually the simplest indicator. If electroreception is present, it is almost certain to be evident in the first preparation.

Very telling is the dramatic story of the discovery of electroreception in one subfamily of notopterid teleosts, though absent in its sister subfamily and in other families of the order, Osteoglossiformes (Bullock and Northcutt, 1982). This was convincing because actual brain responses to physiological stimuli simulating normal signals were recorded in the one subfamily and not in others. This finding opened up the possibility that electroreception might turn up anywhere among the hundreds of fish families, especially teleosts. It is not necessarily an ordinal character, as it appears to be in Mormyriformes, Gymnotiformes and Siluriformes and it will not necessarily be homologous to previously known examples.

What about invertebrates? There has been no concerted effort to look for electroreception among these phyla, that I know of. Once upon a time we dismissed all the smaller invertebrates as unlikely to be electroreceptive because the theory of how fish must do it depended on their size and their high skin resistance. Now we know that this sense modality can be useful, as in mormyrids, even when it is 20,000 times less sensitive than ordinary rays, so we would not be surprised if an arthropod or mollusc or even an annelid turned up with it. "It" has to mean evidence that the species uses naturally available electric stimuli in its normal behavior and excludes senses that, like hearing, may use an electric step in the chain of transducing events. B.U. Budelmann and I did a few experiments on the cuttlefish, Sepia, recording from 4 or 5 places in the brain of intact, unanesthetized animals while imposing large, quasi-uniform fields across the body - without observing any averaged evoked potentials. But a negative finding is quite inconclusive and I wouldn't count the cephalopods out as yet.

So much for my predictions on the distribution of electroreception among the taxa.

C. Electroreception is one thing, electric organs are another. They do not always go together. I predict new species will continue to be found that generate and use feeble electric organ discharges - first of all among the thirty-some families of siluriforms, all of whom are believed to be electroreceptive but only a few electrogenerative. Baron and coworkers (Baron, 1996a, b; Baron and Morshnev, 1998) have recently reported several Ethiopean species and at least one family to add to the previously known catfishes (Clarias, Synodontis, Hagedorn et al. 1990; Baron 1994b, Baron et al. 1994) that discharge weak electric pulses in short bursts after many hours of silence, with suggestive evidence of a social communicative function.

D. It has amazed me that there are not, so far, intermediate cases between weak electric organs and ordinary muscle bundles either with a tendency for nerve endings to prefer the same side of the muscle fibers or for a single motor unit to be very large or several motor units to fire in synchrony. We would notice such cases by the larger than usual muscle action potentials in extracellular recordings. Single, large muscle potentials synchronous with respiration were reported for lampreys by Kleerekoper and Sibakin (1956, 1957). They even suggested that these "spike potentials" function with electroreception - before that term had been invented or any case of it was known. They inferred this from observations which they believed to show aid in prey detection. This unique claim, besides calling for confirmation and extension with behavioral experiments, points to the opportunity to look for other taxa that generate useful electric signals without electric organs. Ordinary gilling as well as fin movements and body bends are associated with action potentials that sound like a "swish" in the audio-monitor - coming from many asynchronous motor units. There might be a species here and there that synchronizes them, as lampreys seem to do. We may find candidate stages in the evolution of electric organs, in ordinary muscle.

E. Turning back to the ethological domain of known weakly electric fish, it seems that we are on the verge of learning the function of the weak and occasional electric organ discharges in the rays and catfish that have them - probably in communication for reproductive or other social roles - judging from early hints in the work of Mikhailenko (1971) and now Baron (1994a; Baron et al., 1994). More puzzling and ripe for new behavioral work in tanks is the functional role of the moderately weak electric organ discharge burst of the "star-gazers" - marine teleosts of the family Uranoscopidae. We were told by Pickens and McFarland back in the 1964 that they discharge apparently simultaneously with the act of prey capture - seemingly too late to help in timing the mouth-gaping capture. Some workers question whether the very modest current, shorted by sea water, could effectively disorient a small prey fish. The case is ripe for new work and the fish are common along many coasts. Even for the well studied mormyrids and weakly electric gymnotiforms, only recently has good evidence begun to appear that the system is used in locating food - small, living prey

It is not yet known definitely what normal objects are discriminated with the use of the demonstrated ability to estimate the capacitative component of impedance. We reported (Scheich et al., 1973) that 0.001 microFarads of capacity in parallel with the water around the fish altered the response of T unit receptors markedly. Presumably the brain, with a whole population of receptor units could detect much less than this - which puts it in the range of capacitative impedance of smallish pieces of tissue. Walter Heiligenberg's first exposure to the tropics was a short expedition he and I made to the Rio Negro in Brazil in 1977 to investigate this but the main result was that he fell in love with the tropics.

F. All these mysteries I predict will be solved in the near future, as well as many new details of the brainstem circuitry and dynamics for analyzing electrosensory input and formulating electromotor output. This will amplify the understanding of the already relatively well-known system - a system more nearly understood in respect to certain normal behaviors, from receptors to effectors, through second order, third order and more than a dozen successive orders of neurons, than perhaps any other in neuroethology.

G. Much more difficult to anticipate, however, is the progress we will make in some other areas. An example is the functional organization of the forebrain - including its pallium, striatum, and limbic divisions. This relatively neglected area might not only round out our picture of the neural basis of some electric behaviors, well studied up to the 'tweenbrain. With that background and the use of stimuli in several other sense modaliies, the electric fish cerebrum should be a good place to elucidate general questions about the physiology of higher centers in advanced teleosts. Ancestral fish invented the forebrain; how their modern descendants organize and use it should give needed perspective on the vastly more studied mammalian forebrain.

I am thinking of questions such as these. Are the various sense modalities - visual, auditory, lateral line, tactile, proprioceptive, olfactory, electric, etc. and the highest motor centers represented in segregated areas - as in mammals, or is there a primitive, multimodal, convergent, perhaps sensorimotor pallium? If they are even partly segregated, are there multiple areas for a given modality, as in mammals, and are they distinct not only in location but in dynamic properties or best stimuli?

Actually we have the beginnings of some information in a study by Prechtl et al. (1998) - who collaborated in the laboratory of the late Walter Heiligenberg - on the cerebral pallium of Gnathonemus, based on evoked potentials and multiunit spike responses at many loci and depths by multiple semimicroelectrodes and multiple modalities of physiological stimulation. They found an astonishing degree of segregation of the four modalities - vision, audition, electroreception and lateral line mechanoreception. The best represented is sound reception and it is in fact subdivided into two physiologically distinct areas - not surprising, since some mormyrids are considered to be acoustically relatively advanced fishes.

We don't yet, however, have answers to further questions such as whether any of these areas - the visual, the auditory, the electroreceptive or the lateral line mechanreceptive areas - map some aspect of the sensory world, like visual space or acoustic frequency or body surface or object distance or relative movement. We have little idea whether there are feature sensitive neurons with complex or ethologically significant best stimuli.

As yet we cannot say whether there is some form of modular organization, in fish, like the minicolumns and the full columns of the mammalian cortex.

We do not know whether there is anything like the plasticity of the mammalian cortical maps, based on the animal's recent experience. Bell and his coworkers (this volume) have shown us how recent experience can change the responses of some brainstem corollary discharge neurons, within minutes, and we have to wonder whether this is reflected in the forebrain.

Even in mammals, where effort has been concentrated, we do not know the actual tranforms of information processing in neuronal assemblages of the thalamus or striatum or cerebellum. Is it possible that the brains of fish might be more readily decoded so that we can discern the transforms? So far, aside from some examples in the brainstem of electric fish, where we think we know roughly what's happening, this field is still quite virgin.

There are other opportunities for research on electric or electroreceptive fish and higher central organization with broad evolutionary significance. What is the degree of modulating influence upon some standard response when you activate or silence the locus coeruleus and its noradrenergic system that sends axons all over the forebrain and cerebellum? What is the influence of the raphe nuclei and its serotonergic system; the basal forebrain and its cholinergic system; the homolog of the substantia nigra-ventral tegmental dopaminergic system? Have these systems evolved a great deal - as the hippocampus has and the cerebellum supposedly has not? Higher functions include intermodulation of responses to a standard stimulus when delivered on a background of different brain states, such as arousal, sleep-like quiescence, directed attention or expectation.

We do not yet know what differences the fish might show in so-called cognitive responses of the forebrain compared with the well known mammalian slow wave responses to expected stimuli and to "oddball" stimuli, as an example. Are there only quantitative or also qualitative differences in functional properties correlated with the great differences in architecture. One thinks of the relative paucity of intrinsic, pallio-pallial connections compared to the mammalian cortico-cortical connections that Van Essen counted a few years ago - some 780 in number (counting a connection from area A to B as one and area B to A as another), out of a possible 3,500 or so (Mountcastle, 1995)? Is the relative paucity that I presume will be documented in the number of reciprocal connections with lower centers great enough to regard as qualitative? The same question may be posed for the relative absence of laminar-specific connections and laminar-specific current sources and sinks? These are only examples of a probably large class of differences yet to be examined. Another class is defined by functional states, including those due to our stimulation and those arising with tasks that the animal innately performs or is trained to perform. How much do we know about differences among major taxa in modulator-specific influences or in the distribution of activity-dependent changes, as in fMRI (functional magnetic resonance imaging) and measures of vascular circulation changes with brain state?

I parade these traits of functional differentiation of higher brain centers to suggest a realm of comparative researches and to encourage new effort in a direction that surely promises a rich harvest. I have confined myself to physiology and anatomy and to presently familiar technics and almost certainly do-able experiments. I have not touched on a long list of others, such as brain slices of higher centers, intracellular recording, pharmacological, chemical and molecular approaches.

I believe, as surely as anything I have faith in, that new principles will be found, new emergent organizational insights gained by mining these veins of precious ore. These revelations are sure to change the big picture drastically - not only the picture of how electric fish work and what teleosts with advanced brains can do, but the understanding of mammalian achievement and of the evolutionary biology of complexity. The evolution of complexity has hitherto been discussed with almost no appreciation of the uniqueness of the brain in respect to specific traits that measure complexity.

I am also sure that real appreciation of the complexity of the neuro part of neuroethology will hardly come before we have done a great deal more on the ethology part. Here also, the state of understanding of the evolutionary differences between major taxa and grades of complexity is meager and most studies aim only at adaptive differences between species of about the same grade. Relatively neglected are comparisons between grades for example to estimate the complexity of behavior in semiquantitative ways such as the length of the ethogram, the number of distinct social situations the animal can distinguish, the number of levels and states expressed which in ourselves would be called emotions and the number of learned items, bits or facts that we call knowledge. Certainly, these are hard won and technically challenging goals. But there are plenty of rewards along the way and plenty of good questions that, with proper formulation, should be fundable research projects.

References

Baron, V.D. (1994a). Possible role of electroreception in the behavior of weakly electric fishes. Sensory Systems 8, 217-224.

Baron, V.D. (1994b). African Clarias catfish elicits long-lasting weak electric pulses. Experientia 50, 644-647.

Baron, V.D. and Morshnev, K.S. (1998). About peculiarities of electric organ discharges of two species of synodontid (Mochokidae, Siluriformes). Dokl. Acad. Sci. 361, (1) (in press).

Baron, V.D., Morshnev, K.S., Olshansky, V.M. and Orlov, A.A. (1994). Electric organ discharges of two species of African catfish (Synodontis) during social behaviour. Anim. Behav. 48, 1472-1475.

Baron, V.D., Orlov, A.A. and Golubtsov, A.S. (1996a). African catfishes. A new group of weakly electric fish. Izvestiya RAN. Ser. Biol. No. 1, 106-111. (In Russian)

Baron, V.D., Orlov, A.A. and Golubtsov, A.S. (1996b). Discovery of electric discharges in the African catfish Auchenoglanis occidentalis (Siluriformes: Bagridae). Dokl. Akad. Sci. 349, 565-567. (In Russian)

Bullock, T.H. and Northcutt, R.G. (1982). A new electroreceptive teleost: Xenomystus nigri (Osteoglossiformes: Notopteridae). J. Comp. Physiol. 148:345-352.

Hagedorn, M., Womble, M. and Finger, T.E. (1990). Synodontid catfish, a new group of weakly electric fish. Behavior and anatomy. Brain Behav. Evol. 35, 268-277.

Kleerekoper, H. and Sibakin, K. (1956, 1957). An investigation of the electrical "spike" potentials produced by the sea lamprey (Petromyzon marinus) in the water surrounding the head region. I and II. J. Fish. Res. Board Can. 13, 373-383 and 14, 145-151.

Mikhailenko, N.A. (1971). Biological significance and dynamics of electrical discharges in weak electric fishes of the Black Sea. Zool. Zh. 50, 1347-1352 (in Russian).

Mountcastle, V.B (1995). The evolution of ideas concerning the function of the neocortex. Cerebral Cortex 5, 289-295.

Pickens, P.E. and McFarland, W.N. (1964). Electric discharge and associated behavior in the stargazer. Anim. Behav. 12, 362-367.

Prechtl, J.C., Von Der Emde, G., Wolfart, J., Karamürsel, S., Akoev, G.N., Andrianov, Y.N. and Bullock, T.H. (1998). Sensory processing in the pallium of a mormyrid fish. J. Neurosci. 18: 7381-7393.

Scheich, H., Bullock, T.H. and Hamstra, R.H. Jr. (1973). Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fish, Eigenmannia. J. Neurophysiol. 36, 39-60.