ELECTRIC FISHES November 7, 1968 CONTENTS I. INTRODUCTION ....................................................... II. ELECTRIC ORG.ANS ......................... i......... o................. 2 @lorphology ................. ......................................... 2 Electrophysiology ............................................. 47 III. NAVIGATION AND DETECTION WITH ELECTRIC FIELDS ................ IV. REFERENCES .......................................................... 14 I. INTRODUCTION There are seven families of marine and fresh-water fish capable of deliver ing appreciable voltages outside their bodies. For example, the giant electric ray (Torpedo nobiliana) can electrocute a large fish with its pulses of 50 amperes at 50 to 60 volts. Thouch much smaller, the African catfish (MalaDterurus) pro- 2 duces as much as 350 volts, and the electric eel Electrophorous) of the Amazon and other South American rivers puts out more than 500 volts. In contrast, there are weakly electric'fishes-which generate from a few tenths to several volts, but even these species exceed the hiahest output of other animals which produce minute electrical currents in their nervous, muscular, and glandular tissue. 2 "There now seems to be no doubt about the-survival value of the peculiar capability of the electric fishes. For the powerfully electric species it ser- ves ob-vious offensive and defensive functions, and recent work has shown that in the weakly electric ones it serves as part of a sensory guidance system for navigation in murkey waters and for the detection of predators and prey. The advantag2es, in fact, are such that natural selection brought about the develop- ment of electric organs quite independently in almost every one of the families" (Grundfest, 1960a, pp. 115-116). In several cases, different physiological so- lutions were developed for the generation of electrical energy and the shaping and timing of the electric pulses. "Animal electricity" was first studied in 2 electric fishes, and throughout the 19th Century these animals were the center of research on electrophysiology. As far back as 1791 Galvani suggested that there was a kinship between the elec- tricity'of "torpedo and cognate animals" and the "animal electricity" that he be- lieved he had observed in muscles and nerves. A dispute arose between Galvani and Volta wherein the latte2r thought that Galvani had demonstrated "metallicts electricity by the contact of two dissimilar metallic surfaces rather than ani- mal electricity. This was correct in that Galvani's frog nerve-muscle prepara- tions were merely more sensiti've detectors of electricity than any instruments available at that time. But "Volta was wron- in denying the existance of ani- mal electricity. In 2trying to prove his contention that the electric fish con- tained some sort of generator Volta discovered the electrochemical battery, or igalvanic' cell. The 'voltaic pile' of cells in series he called 'an artifi-cial electric'organ' which he thought 'victoriously demonstrated' his argument" (Grundfest, 1960a, p. 117). At the present time, work-on electric fish 6 offers some potentially very useful leads to the solution of the problems of synaptic transmission such as the induction by tlie-nerve impulse of the chemical mechanism that underlies the relay of the impulse from one nerve to the next and from the rlerve cell to muscle or gland tissue. II. ELECTRIC ORGANS Morpholoay 0 Electric organs are derived from muscle and consist of an array of cells called electroplaques. These component cells may be stacked in columns like a roll o'f coins along each side of the body, running longitu2dinally and parallel with the spinal column. The eel is an example of this type and has some 6,000 to 7,000 electroplaqi4es in each column, with 70 columns in the organs on each side of its body. -In the adult eel they make up about 40 percent of the bulk -of the body. In contrast, the columns in the electric ray are arranged verti- cally, i.e. at right 2angles to the spine, formina a large'compact electric organ in each of the animal's wings. A third pattern is found in the African catfish, in which the organ is in the form of a mantle of tissue just below the skin,. surrounding the entire body from gills to the tail. The bilateral electric or- gans of several species are shown in Figure 1. Each electroplaque is a thin wafer-like cell whose two surfaces diff2er markedly. In most species, one surface-is innervated directly by a dense net- work of nerve terminals or indirectly through one or several stalks which emerge from one of the electroplaque surfaces (Figures 2 and 3). But in almost all cases only one surface of the cells is innervated. The opposite side has a number of deep folds and convolutions to increase its total area. All of the electr2oplaques in one species are oriented in the same way. In addition to the main organ, an accessory electric organ is present in the electric ray. The electroplaques of this organ have a different orientation, i.e.,.they are in- nervated on their dorsal rather than their ventral surfaces. The surface of the electroplaques innervated and other aspects of their structure in a number of electric fish are summarized 8in Table 1. . . ......... .. --------------- a c 'Figure 1. The electric organ arrangement in various electric fishes. The electric eel (a) has three organs (stippled area at top left): large main 2 organ, smaller organ of Sachs behind it and organ of Hunter immediately under- neath. Main organ and organ of Hunter appear.in cross section below. Arrow indicates direction of current flow in body of fish during electric discharge. In Mormyrus (b) organ is situated near tail. Organ of MalaDterurus (e) forms a mantle just under skin of fish. Electric skate (d) has organ in tail. 8 Electric ray (e) has a kidney-shaped organ in each wing. Cross-sectional view shows columns of electroplaques in organs. The direction of the dis- charge (arrow) is perpendicular to the broad surface of ray. (After Grund- fest, 1960a) Figure 1 continued on next'page. rt Cb jl' /eACCESSORY ORGAN M IN ORGAN STALK PENETRATING STALK C- (7, V C7, MULTIPLE STALK b swim IA6DtR 2 NER'IE ELECTROPLAGU Figure 2 Details of electric organ of electric rays (a), morriyrids (b) and elec- tric eel (c) are shown. Electroplaque columns are vertical in body of the ray (top right). Nerve terminals (colored branching at top left) directly innervate column. Crania2l nerves (heavy colored lines at right) connect organs with elec- tric lobes (solid colored area) of brain.-. iecently discovered accessory organ is found only in ray genus 'illarcint. Among different mormyrid species electro- plaques are indirectly innervated via three types of stalk. As in some other fishes, uninnerval-ed membranes of electroplaques in main organ of eel are con- 5 voluted. (After Crundfest, 1960a). foci Vogul main argon accessary argon (a) (b) spinal ca2rd resiral swim ladder caudal lnnervaled fcce (d) Figure 3. Sariples of organ and electroplaque structure. (a) Column of electro- plaques in series array, representing essentially the arrangement in the torpe- dine electric fishes and in Astr26scoDus. (b) Dorsal view of innervation which applies to Torpedo and main orcan of Narcine; innervation is by individual nerve fibers to ventral surface of each electrodlaque entering four different points of the periphery and supplying a limited area of the surface. In 'Astro- Scopus and the accessory organ of Narcine innervation is on the rostral surface, and nerve supply is more complicated. Fig2ure also applies to Torpedo, except that accessory organ is absent. (c) Diagrammatic view of series and parallel. arrays of electroplaques in the electric eel. A somewhat similar series-parallel- arrancement occurs in other electric fish in which one surface is innervated. In R-ala innervation is on rostral surfaces. (d) The mormyrid electroplaques are innervated on one or several stalk processes whic6h form from branches that arise in the caudal surface of each electroplaque. In some, branches penetrate through the electroplaque body and innell'Tiation is then ahead of the electroplaque. In Malapterurus there is only a single stalk which arises from the center of the caudal face of the electroplaque. (After Crundfest, 1960b). Table 1. Anatomy of electroplaque in several electric fish. (After Grundfest, 196C Diniensions No. of Species - Ori.-iti Inner. %\o. in 2 colunins 7 (muscle) vatioti' Orientation R-C D-V hI-Lt colufiins per side Torpedo rwbiliana Branciiial v D-V 8 mill 10 u 8 niiii 1000 1000 2 Narrine brosiliensis Alain or-an Branchial v D-V 4 mm 10,u 4 mm Soo 400 0 Accessory organ Brancliiil D 2 Oblique 4mm 20 a 4mm 200 10 Raia clarala Skeletal R R-C .200 12 Astroscopus y-graccum Ocular D D-V 10 mm 50 u 10 mm 200 20 Electrophorus etectricus Skeletal - c R-C 200 u I mm IS mm 6000 75 Eigenniannia virescens Skeletal 2 c R-C 2mm 200 200 Is 5 Slernopygus elegaru Skeletal c R-C I mm 60 60 IS Gymnolus carapo Skeletal 11 and C R-C 20018 Soo 2 Soo 80 4 Slernarchu.s albifrons R-C Gnatlione.-nus com- pressiroslris Skeletal c R-C so." 10 mm 5 mm 100 2 2 btorttzvrus rume Skeletal c R-C 50 ;g 10 mm 5 mm 100 2 Gymnarchus niloticus Skeletal c R-C 100 100 100 14 2 140 4 Alatapterurus electricus - c R-C 4011 1 mm I mm 3000 isoo Abbreviations are R. rostral; C, caudal; D, dorsal; and V, ventral. t,%Iedial-l;tteral. Electrophysiology The electroplaques in each--column of an electric organ form a series array, so that the hook-up in series adds the outputs of the cells and builds up the voltage, while the arrangement of columns of electroplaques in parallel2 functions to build up the amperage. "The large area of the organ of the strongly electric fishes is analogous to the large number of plates in a storage battery cell of high current output" (Grundfest, 1967, p. 405). The 2 discharge characteristic$ of electroplaques in several fishes are outlined in Table 2. In the electroplaques of marine ele@tric fish, only the innervated surface of the cell is reactive. Electrogenic activity cannot be evoked by 2 direct elec- trical stimulation, but only by stimulating the nerve or with chemical agents, i.e., the cell is electrically inexcitable. The electroplaque's cell membrane, like that of the nerve or muscle cell, is selectively permeable to potassium . ions 2 but not to sodium ions, so that the higher concentration of the former in- -side the cell membrane and the latter outside the cell creates a resting poten- tial across the membrane , with the inside negative and the outside positive. 2 After a sti'mulus is applied, the permeability of the menbrane changes, permitting the movement of both types of ions (and,-therefore, an electric current) to flow across the men@brane. Generally, only the_innervated membrane of the electroplaque Table 2. Electroplaque dischar-e and response characteristics in several elec- a tric fish. (After Grundfast, 1960 b.) 2 Respon.-e Duration, msec species Discharge 2 Post- kmplitude, Ampti- synaptic VOILS Form Frequency tudc, mv Type* potential Spike 2 Torpedo nobiliana 60 . 'i%lonophasic Repetitive on ',%lax. 80 1 s None excitation ]Vareine bresilienjis Ntain organ 2 30 I%Ionoplinsic Repetitive on ',%lax. so, I 'L%'one excitation Accessory or-an 0.5 ',%Ionophasic Repetitive on I%Iax. 80 I None excitition Baia clarcia .4 Nlonopliasic Repetitive on ',L%Iax. 80 1 25 'None 2 excitation Astroscopur y-@raccum 7 ?tfonaphasic Repetitive on ',%tax. 80 1 5 None excitation 2 Electraphorus c[cciricut 1600 Nlonophasic Repetitive on Nfin. 100 2 2+ 2'+ excitation Eigertmannia cirescens I 2?vfonophasic 250/sec Nlin. 100 2 1 positive direct current Sternopygus ele2gans I Nlonoph3sic SO/sec Niia. 100 2 2 10 positive direct 2 current Gymnolus carapo I Triphasic SO/sec ',%fin. 100 t I.S I Sternarchus albifrons I Diphosic 750/ste ,,% I i n. 100 3 Gnatlionemu.s com- prtssirostris 10 Diphasic Variable I i n. 100 4 0.2 -Alormyras rume 12 Diphasic Variable2 Nlin. 100 4 Gymnarchus nildicus Low ',%Ionophasic 300/sec AlOtaptCrUFUS CICCtriC= 300 %Ionopbasic Repetitive on Alin. 100 4 2 2 excitation *Response types: 1, electrically iiiexcitatile electropl3ques which produce oniv a postsynaptic potential and only on the innervated surface; 2, responses are both postsvnaptic poteiitials and spikes,'prodticed only at in. pervated surfice; 3, opposite. uninneryated surface ali-@o is eicctrica2lly excital;le. producin.- a spike, whereas the innervated surf.-ice develops botli a pestsynaptic potential and a spike; 4, the svnaptic junction is at a distance frotn the inajor surfaces of the electropl-Aque on one or severiil stat'.-s produced by the caudal surface. and both rnajor surfaces produce spikes. is affected. The opposite membrane usually remains inactive, maintaining a ne- gative potential and offerin2a little resistance to the flow of electric current. Inasmuch as current flows from positive to neaative, the orientation of the electroplaque determines the current's direction in the fish. For 2 example,'the innervated surfaces of the eel's electroplaques all face the tail, so that cur- rent flows from tail to head inside the fish and from head to tail in the water 2 to complete the circuit. "The great number of electroplaques in series enables the eel to produce the volta-e 'necessary to overcome the hiah resistance of its fres2hwater environment. The columns in parallel enable it to generate a cur- rent, in brief pulses, of about one anpere, so that even in fresh water the or- gan generates considerable power. The electric rays, living in salt water, show 2 a corresponding adaptation to the lower resistance of this medium. The giant ray Torpedo nobiliana has up to 1,000 eleciroplaques in series, much fewer than the eel, and so generates a lower volta'ge. But it has some 2,0700 columns in parallel in each organ, giving it its extraordinary amperage (Grundfest, 1960a, p. 119). ; The generation of electricity in electroplaque memb@ranes considered as batteries is shown in Figure 4. la lb + UNINNERVATED t-IE?v',B@ANE IELECTRI@@ALLY INEXCITABLE) 2 A 0 INNERVATED MEMBRANE (ELECTRICALLY INEXCITABLE) .2a 2b 2 UNINNERVATED MEH@,BRANE IELECTRICALLY INEXCITABLE) t INNERVATED M@EIVBRANE (ELECTRICALLY EXCITABLE) 3a 2 3b ------------ UNINNERVATED MEMB;IANE I ELECTRICALLY EXCITABLE) J- 2 INNERV@.TEC) MEVBPANE z (ELECTRICALLY EXCITABLE) + Figure 4. The generation of electricity by electric fishes can be explained by comparing electroplaque membranes (shaded areas) to batteries. Restina poten- tials of membrane batteries, 2 ne-ativelv ch rged on inner surface and positively charged on outer, are sho@-m at left. In marine fishes nerve stimulus short-cir- cuits battery of innervated membrane (lb). Magnitude of discharge equals resting potential, and current (broken line) flows through electroplaque, then through external medium. In eel, stimulus reverses polarity of batter8y of electrically III. NAVIGATION AND DETECTION WITH ELECTRIC FIELDS The gymnarchus has a weak electric organ which-is somewhat like the power- ful electric organs of the electric eels and other fishes in that it is derived from muscle tissue. 'But until recently, no one had found a function for weak electric organs. Now it is known that t'gymnarchus lives in a world totally 2 alien to man: its most important sense is an electric one, different from any we possess't (Lissmann, 1963, p. 359). By means of this sense, it is able to swim with equal facil ity ba'ckward or forward, and to avoid obstacles when they are encountered for'e'or aft. Its movements are made with great precision, and 'it never bumps into the walls of its tank when darting after small fish. 2 The small electric organ of gymnarchus consists of four thin spindles con- taining electroplaques running up each of its sides to a point just beyond the middle of its body. The characteristics of its electric organ discharge vary with the individual and with temperature. For example, specimens may produce voltages of 3 to 7, with a discharge frequency averagin- about 300 cycles per "Durino, each discharge the tip of its tail becomes momentarily nega- second. a tive with respect to the head. The electric current may thus be pictured as s spreading out into the surrounding water in the pattern of lines that describes a dipole field (Figure 5). The exact configuration of the electric field depends on the conductivity of the water and on the distortions introduced in the f2ield by objects with electrical conductivity different from that of the water. In a large volume of water containing no objects the field is symmetrical. When objects are present, the lines of current will converge on those that have better conductivity and diverge from the poor conductors (Figure 6). Such objects alter the distribution of electric potential over the surface of the fish" (Lissmann, 2 1963, 362). If gymnarchus could perceive such changes, it would be able to de- tect objects in its environment.--This it is able to do through skin perforations near its head which lead into tubes filled with a jelly-like substance. Since the jelly is a good conductor, it acts as a lense to focus the lines of electric current which converge from the water into the pores and are led to electric sense 2organs at the base of the tubes. All animals are sensitive to strong electric currents, but their response is to currents many thousands of times stronger than those effective in gymnarchus and gymnotus. The latter can readily learn to locate currents whose density is 5 2 reduced to 2 x 10- VA/cm , as calculated from the response distance to the hor- izonta2l movement of an electrostatic charge outside the aquarium. Even the elec- trostatic charge of a plastic comb elicits a response in gymnarchus. The same fish is able to detect the weak current flow from a horshoe-shaped copper wire when it is closed and dipped just below the surface. It is also possible for this fish to distinguish bptween t'geometrically identical objects with differing electrical 0conductivities. Conversely, it cannot distincuish between dissimilar objects which modify the current distribution in a similar way" (Lissmann and Ifachin, 1958, p. 454). Dischar-e frequencies usually increase at higher temperatures. Figure 5. Electric field of Gymnarchus and location of electric generating or- gans are diagramed. Each electric d@-scharae from organs in rear portion of body makes tail negative with respect to head. Most of the electric sensory @ores or organs are in head region. Undistrubed electric field resembles a dipole field, as shown, but is more complex. The fish res0ponds to changes in the distribution of electric potential over the surface of its body. The conductivity of objects affects distribution of potential. (After Lissmann, 1963.) 7' Figure 6. Objects in electric field of Gymnarchus distort the lines of current flow. The lines diverge from a poor conductor (left) and converge toward a good conductor (right). Sensory pores in the head region detect the effect and inform the fish about the object. (After Liss'mann, 1963). IV. REFERENCES Abe, N. Galvanotropism of the catfish Porasilurus asotus (Linne). Sci. Re P. Tohoku Univ. (d), 1935, 9, 393-406. Altamirano, M., C.W. Coates, and H. Grundfest. Mechanisms of direct and neural excitabil2ity in electroplaques of electric eel. J. Gen. Physiol., 155, 38, 319. Bennett, II.V.L., and H. Grundfest. 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