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This article provides an abbreviated account of an unfamiliar sensory system well developed in certain families of fishes and present in simpler form in a few amphibians and mammals. Some species use only the passive form – electroreceptors filter and map the electric fields of extraneous origin, whether biological or nonliving, around or near the animal. Where the system is developed in an active form, it involves an electric organ that generates pulses of current under central control, and an array of specialized sense organs that detect the animal’s own field and central (brain) circuits that analyze these signals with respect to its spatial and temporal structure. In addition to discussing each of these topics we will mention briefly the behavioral uses (such as communication, feeding, and electrolocation, among others), the developmental history, evolution, and special aspects.
A species of catfish common in African fresh waters which can deliver a strong jolt, as well as a Mediterranean species of ray they called Torpedo, presumably because it can induce torpor, were known to the ancients. Very soon after 1492, South American electric eels were brought back to Europe and their high voltage discharges were familiar. They figured in classical experiments and controversies about animal electricity in the 18th century. Not until the 1940s was it realized that many smaller relatives of the electric eel, common in neotropical fresh waters also discharge electric organs, although feebly – usually peaking at a few millivolts measured on the skin, out of water, in one or a few thousandth of a second pulses, several times every second, night and day, continuously. Studies of the mechanisms of production, control and use of the strong electric organ discharges (EOD) were already well along when the weakly electric fish added questions of reception, brain analysis, use, function, development, and evolution. These rapidly expanding fields of research have been reviewed in two books: Bullock and Heiligenberg (1986), updated in Bullock, Hopkins, Popper and Fay (2005). The following is a condensed and selective summary.
Diversity is conspicuous in the temporal pattern of electric organ discharges (EOD). Some species are called “pulse fish” because the EODs iterate at a low and irregular repetition rate (intervals several to many times the duration of the single pulse). Others are “wave fish” because the intervals are brief and regular (equal to or little longer than discharge duration) – reaching regularities higher than any other known biological rhythms. Each discharge is commanded by a special brain nucleus that receives and integrates multiple inputs and is usually relayed through one or more synapses in the brain stem and again in the spinal cord, besides the last junction between efferent axon and electrocyte. The regularity of the EODs can be controlled by the brain and routinely shows a very small variation. It is not yet clear what situations or states of the brain are associated with higher or lower regularity or what selective advantage such extremely low variation confers. Presumably this advantage lies in the domain of detecting or assessing objects that distort the instantaneous electric field of the EOD – the signal analyzed by the electroreceptive system.
A landmark in neuroethology, the science that seeks to explain behavior in terms of neural structure and function, is the Jamming Avoidance Response (JAR), a simple behavior observed in wave species when two or more individuals are within range of each other and have EOD frequencies close to each other. Unless there is a large difference in size, each fish will, quite reliably shift its EOD frequency in the direction to increase the difference in frequency – interpreted as an avoidance of being mutually jammed. This behavior means that each fish is solving the problem of recognizing which part of the mixed electric fields in the water coming from its own EOD and which part is from other fish. Some ingenious experiments demonstrated that they do not utilize information in the brain that commands each EOD train but depend on analysis of the sensory feedback.
A speculation of possible interest to electrochemistry is that there might be patterns of texture in the electrochemical fields, close to the bottom or to objects past which water is flowing, that electrosensitive fish can detect and characterize as useful signs of the features of the solid surfaces. One class of experiments has shown that such fish detect or compute the plane of an invisible (transparent plastic) bottom in order to maintain a prefered tilt or angle between the fish’s vertical axis and the plane of the substratum (the “ventral substrate response”).
A more detailed description of the ontogenetic development and evolution of electric organs is given in the Appendix.
Ontogenetic development The multiple types of electroreceptors are all derived from lateral line receptors which are endowments of all fishes plus aquatic amphibians mediating mechanical senses associated with relative movement of animal and water in a low frequency range 0.1 to 100 Hz. Commonly called water flow and vibration, overlapping with acoustic reception via the inner ear and eighth cranial nerve. The sense cells in both mechano- and electro-receptors are members of a large class of sensory hair cells, although some of the electric sense cells have lost their ciliary “hairs”. We do not know the crucial features that evolved to alter the “adequate” stimulus from a mechanical event to an electrical one, but the change in sensitivity was many orders of magnitude and, in each class of electroreceptor, was tuned to a best frequency that could be many octaves apart. The ontogenetic development in the young animal begins, as for lateral line sense organs in clusters of neuroblasts in the head called lateral line placodes that send their outgrowing central axonal processes in to the brain by one of several cranial nerves, mostly the trigeminal. Their peripheral axons grow into the lateral line nerves to a species-characteristic quite wide distribution over the skin of the developing non-nervous parts of the eventual sense organs. These non-nervous parts plus the sensory “hair” cells that actually detect and transduce the stimulus event into physiological signals that can conduct along the axons, depend on the nerve growing in from the distant neuron to steer, trigger, and control the placement, orientation, tuning, and sensitivity that develops.
Evolution Electric organs are known in some species of skates (rajoid elasmobranchs) and electric rays (torpinoids), without clear indication whether there was only one or more than one independent “invention”. The EOD of skates is weak and probably mainly functions in communication between members of the same species, for example in reproductive behavior. The EOD of Torpedo is high in current but low in voltage and, whatever else it does, certainly contributes to catching prey fish by disorienting their swimming. Electric organs are known in a number of bony fish, including several species and maybe whole families of catfishes (Siluriformes) including one with a strong EOD (Malapterurus), the others being weak, presumably social communicating systems; probably all of the New World knife fishes (Gymnotiformes) which includes the classical, high voltage, low current electric eel (Electrophorus), all species of the African order of Mormyriformes (elephant nose and many others); one family of stargazers (Astroscopidae) with EODs of very moderate strength and quite unknown function. It seems likely that evolution has discovered how to make and make use of electric organs at least five times, independently and possibly more – an outstanding case of parallel evolution, possibly exceeded however by the number of plesiomorphic features independently invented for electroreception. Diversity on the motor side includes a variety of forms of innervation of the electrocytes in mormyrids, where these cells have stalks that in some species penetrate the flat disk-like electrocyte and receive motor nerve endings at a circumscribed part of the stalk. Studies of the mitochondrial DNA sequencing of many species permit conclusions about which form of innervation was primitive and which was derived and agree very well with phylogeny based on anatomical characters (Alves-Gomes and Hopkins, 1996).
With such high sensitivity it becomes difficult to guess what the world must look like to such an animal, especially what the sources of noise might be, that interfere with detection of significant signals or limit the resolution. One such factor must be lightning, since it has been shown to cause millisecond pulses in natural water bodies, up to hundreds of miles distance (Hopkins, 1973) overlapping in duration and form the EOD pulses of many species of weakly electric fish. As in the case of the Jamming Avoidance Response (JAR), it may well be that brain processing which compares the afference from different parts of the body surface enables the fish to distinguish such far field sources from the reafference of its own EOD. The fish are demonstrably able to use high frequency dependent small differences in impedance but it is still not known just what discriminations these fish make, based on complex impedance, for example among aquatic plants.
A speculation of possible interest to electrochemistry is that there might be patterns of texture in the electrochemical fields, close to the bottom or to objects past which water is flowing, that electrosensitive fish can detect and characterize as useful signs of the features of the solid surfaces. One class of experiments has shown that such fish detect or compute the plane of an invisible (transparent plastic) bottom in order to maintain a prefered tilt or angle between the fish’s vertical axis and the plane of the substratum (the “ventral substrate response” akin to the dorsal light reaction, Meyer, 1976).
For many years, there was no special reason to believe that there must be a novel modality for electrosense until it was discovered that many species have a very low voltage EOD, and more convincingly when Lissmann (1958) demonstrated that one of these feeble electric fish can learn to distinguish objects – such as two porous ceramic filters one containing a 6 mm diameter glass rod and the other a 4 mm rod, invisible through the walls of the filter and hence differing only in electrical impedance, via the active ongoing EOD and sense organs that measure the local strength of the electrical field at different parts of the fish’s body surface. The relevant signals are therefore in gradients of hundredths of a microvolt/cm (Machin and Lissmann, 1958, 1960). Even higher sensitivity has been measured, repeatedly, by directly applied electrical pulses in the sea water around some skates and sharks, via their passive electrical receptors; 0.005 microvolts/cm at the peak of a one Hz wave can elicit feeding or orienting behavior (Kalmijn, 2000). Differences between species can be large; one factor being the salinity of the normal habitat. Fresh water forms are generally much less sensitive than sea water animals, perhaps correlated with the greater attenuation of available signals in the high conductivity of sea water.
Electrosensory receptors have evolved in presumably all elasmobranchs, including the truly fresh water rays, as well as in the sister group of the Holocephala (rat fish and chimaeras) and in one group of the agnathans (cyclostomes), the lampreys or petromyzontids, but not in the hagfishes (myxinoids), which are otherwise more advanced in brain differentiation. Thus electroreception contributes to the argument that these two subdivisions of the cyclostomes are unrelated except through remote common ancestors. The only analog of an electric organ discharge in lampreys is the synchronized muscle action potential accompanying each cycle of respiratory movements and one report would suggest that the lamprey uses this synchronized potential as a form of active electroreception (Kleerekoper 1956). Most elasmobranchs lack any analog of an EOD, as far as we know, but they might well detect distortions of their own standing electric fields due to dc fields from the skin, gills and mucous membranes – like everything living in a conducting medium. The same questions are open for other groups that possess electroreception, but which lack electric organs. This includes the holocephalans, some aquatic salamanders (apodan urodeles), and most of the large and diverse superorder of siluriform teleosts (catfish and others). Several recent discoveries have enlarged the list of catfish that have small electric organs or produce EODs now and then at intervals of many hours – requiring special techniques to capture the episodes for analysis (Baron, 2003). At one stage it seemed that having the central and peripheral specializations for electroreception must be a characteristic of the order and would be found in all families of those orders, an exception has turned up (Notopteridae of the Osteroglossiformes) where one suborder (Xenomystinae) has and another (Notopterinae) lacks the ekectrosense. Also puzzling are the stargazers Astroscopus and Uranoscopus. These live, buried in the sand with only the eyes and lips showing, ready to inhale prey fish by suddenly opening the mouth hence, like the long interval catfish, above, have EODs episodically (when a moving shadow coincides with a tap on the wall of the container, simulating a passing fish, Pickens 1964), but seem to lack electroreception (by the usually reliable test of evoked potentials in the midbrain tectum). The EOD is doubtfully strong enough to disorient a passing prey and doubtfully early enough to give sensory guidance to prey catching.
Since the two orders that display an active electrosense using their own EODs (the Gymnotiformes and the Mormyriformes) are not closely related and many sister groups have no electric sense, it seems probable that their systems have been independently “invented” in evolution. The gymnotiforms are close to the siluriforms and might have shared a common ancestral invention. Just possibly the xenomystine knife fishes inherited an invention of the mormyriforms since they both belong to the osteoglossiforms. As few as two parallel inventions within the teleosts can be argued with parallelisms remarkable in their detail. Outside the teleosts, conceivably one single invention has left its mark in the elasmobranch form of ampullary sense organs and central pathways, in the petromyzontiforms through the elasmobranchs and the chondrostei (sturgeons and paddlefish), dipnoans (lungfish), crossopterygians, and brachiopterygians, to the apodan urodele amphibians. Too little, if any behavioral research has been done on most of these groups toward learning what use they make of the sensory system as a passive sense. Exceptions are the elasmobranchs and the paddle fish. In the former, elegant behavioral physiology (Kalmijn, 1982, 2000) has shown under quasinatural conditions it is used for navigation relative to the earth’s magnetic field as well as to find food fish buried in the sand. In young paddle fish (Polyodon, Acipenseriformes, Chondrostei) it has been shown convincingly that the electric sense guides prey capture even when the prey are small crustaceans about a millimeter long (Daphnia), evoking accurately directed capture of single individuals.
Presently, many of these topics are still very fluid and will disclose new discoveries with further investigation.
afferent: moving or carrying inward or toward a central part. Refers to vessels, nerves, etc. For example, blood vessels carrying blood toward the heart, or nerves conducting signals to the brain. Contrast with efferent.
axon: the threadlike extensions on a neuron, or nerve cell which conducts nerve impulses. A neuron usually has one long axon, which branches only at its termination.
dendrite: a long extension of a neuron with thin, treelike branches. It receives nerve signals and transmits them to the main body of the cell
efferent: moving or carrying outward or away from a central part. Refers to vessels, nerves, etc. For example, blood vessels carrying blood away from the heart or nerves carrying signals from the brain. Contrast with afferent.
electrocyte: cell in an electric organ.
EOD: electric organ discharge.
neuron: a nerve cell; it receives and conducts electrical impulses from the brain. It consists of a cell body, an axon, axon terminals, and dendrites.
nucleus: central part of a living cell.
ontogeny: the developmental history of an organism.
synapse: the junction where a signal is transmitted from the axon of one nerve cell to the dendrite of another nerve cell.
Listings of electrochemistry books, review chapters, proceedings volumes, and full text of some historical publications are also available in the Electrochemistry Science and Technology Information Resource (ESTIR). (http://electrochem.cwru.edu/estir/)
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