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----------·~ -~----- ON THE NATURE OF ELECTROSENSING IN THE FISH \ • ' \ lI August 1971 I i ABSTRACT An evaluative review of the electrosensing literature was carried out with the intention of determining the nature of the electrosensing mechanism and its sensitivity. It was found that the biological data base was weak. It was, however, in the development of a mathematical model and mathematical use~ analyses of the sense mechanism and its function. In the course of the analyses, we suggest a working hypothesis on the nature of the sense mechanism. We also collapse the various sensor coding schemes that have been proposed into one scheme. The function of the mathematical model of the sensor that was developed was explored with the use of a computer. The fishes' function at the system level was also considered and possible._mechanisms defined. ii TABLE OF CONTENTS ABSTRACT ........................................................ INTRODUCTION l NATURE OF THE BIOLOGICAL SYSTEM •••••••••••••••••••••••••••••••••••••• 2 ..................................................... Generator Organ 3 Receptor Organ . ..••. ~ . . . . . • • . . . . . . . . . • . • . . . . . . • . . . . • . • . • . . . . • . • . . . • . . 7 Gymnotid receptors. Mormyrid receptors. 8ystem Function, Measurement Technique & Sensitivity •••••••••••••••••• ll Electrophysiological & behavioral techniques. Size of tank required for valid experimental data. POSSIBLE RECEPTOR MECHANISM AND NEURAL CODING ••••••••••••••••••••••••• l7 Mechanism. Coding. MODEL: DEVELOPMENT, FUNCTION, AND SENSITIVITY •••••••••••••••••••••••• 27 Receptor Level ...•.•.•.••.•••.•.••....•••..••••..•••••••••••••.••.•.• 28 Development. Function. Sensitivity. System Level . ......................................................•... 54 .............. CONCLUSIONS •••••••••••••••••••••••.•••••••••••••••••• 55. . ..................................... . REFERENCES ••••••••••••••• • ••• 58 .APPEND IX • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • •• • • • • • • • • • • • • • • • • • • • 61 1. INTRODUCTION It has only been a short time since certain fish were identified as having a previously unknown sensing system, an el.ectrosensing system. It was observed that these fish apparently detect and classify objects that enter into and perturb a weak electrical. field that the fish itself gener ates. With further investigation it was found that this The image displays a stylized depiction of a vault door on the left, with a glowing blue light emanating from its interior. To the right of the vault, text is presented in a stylized font, stating "THE BLACK VAULT". Below this title, in white text, is information about the document's origin from an online database of declassified government documents. It specifies that the record is part of the MKULTRA/Mind Control Collection, comprising over 20,000 declassified pages from the Central Intelligence Agency (CIA). Finally, a yellow URL is provided for free download and online access. time since certain fish were identified as having a previously unknown sensing system, an el.ectrosensing system. It was observed that these fish apparently detect and classify objects that enter into and perturb a weak electrical. field that the fish itself gener ates. With further investigation it was found that this sense is more generally found among fishes than was first thought. Data also appeared indicating that some fish, such as the shark and goldfish, use a passive el.ectrosensing system in that the fish does not seem to generate its own electrical. field. Rather, it seems·to detect electrical. signals, possibly muscle potentials, generated by objects coming into its area. Although there is now a fairly substantial. data base, we find that very little can be applied to the development and understanding of sense mechanism and sensitivity. This is due in part to the fact that pioneering data in this area, as it is in most areas, tend to hEVe faults no matter how competent the investigators. Further, the data base contains very little behavioral. data. Thus, there is little information available on system sensi tivity and function. In sum, though there are individual. investigators contributing quite useful. data to the data base, as a whole the data base is weak. Thus, we have undertaken several. tasks which may al.l.ow an assessment of the fishes' el.ectrosensing mechanism and capability, using the data presently available. First, through limited experimental. work with electrical. fields, sen sors, and objects in various size bodies of water we have gathered data which, when taken with the mathematical. analysis, allows us to interpret much of the data now available. This analysis also provides a specification for tank size; - fish location, and attachments, that will yield valid data in fUture studies. Second, we have suggested as a working hypothesis an electrosensor mechanism. This hypothesis is subject to test and thereby may provide the means for collapsing the current multiple crude categorizations of the re ceptor that is so typical of a new area of investigation. The hypothesis may also provide a basis for analyzing higher interactions in the fishes' nervous system and thereby increase our understanding of the sense. Third, we indicate in the following the linkage among the various neural coding schemes suggested for the fish and show their essential identity. Fourth, we develop a mathematical model of the fish based upon the use able experimental data. The declassified CIA document displays a title in all capital letters, stating "ON THE NATURE OF ELECTROSENSING IN THE FISH," followed by "August 1971." To the bottom right, a handwritten circled number "256" is present. The page contains several small black dots, likely ink splotches or minor printing imperfections, and a few faint, curved lines. No photographs, stamps, forms, diagrams, or other structured data are visible on this page. The digitally rendered page contains the text of an abstract from a document. There are no images, handwritten annotations, stamps, forms, diagrams, tables, or redactions present on the page. The visual content is solely the typed text of the abstract, with the title "ABSTRACT" centered above the main body of text. fishes' nervous system and thereby increase our understanding of the sense. Third, we indicate in the following the linkage among the various neural coding schemes suggested for the fish and show their essential identity. Fourth, we develop a mathematical model of the fish based upon the use able experimental data. A set of equations describing function is developed on the model. These equations are linked to available experimental data. The mathematical model is analysed by a computer to ascertain the sensitivity requirements of the fish at the receptor and to determine the effects of mani pulating a number of variables. These variables include fish size, object size, object electrical characteristics, object distance from the fish, direction and angle of the object from the fishes' axis, etc.· We briefly discuss the fishes' function at the systems level and close with our conclusions concerning the electric sense. NATURE OF THE BIOLOGICAL SYSTEM Both marine and fresh water species of strongly and weakly electric fish have evolved. Strongly electric fish are defined as those that dis charge their electric generating organs reactively to stun prey or resist capture. Weakly electric fish are defined as those that detect and classify objects by the object perturbing the electrical field formed by the electric 3 generating organ Yhich normally emits a continuous pattern of pulses. The electric field so set up is not strong enough to stun other fish. There are numerous of weakly electric freshwater fish but s~ecies most can be classified as either gymnotids which are South American in origin or mormyrids Yhich are common in Africa. The two groups have many similarities and some differences in physical structure and in the function of their elec trical field generating organs and receptor organs. Other weakly electric fish include Gymnarchus, an African fish, probably related to the mormyrids, and sternarchid, a South American fish that is probably related to the Gymnotids. Generator Organ An understanding of the structure and function of the electrical field generator organ is of importance in understanding receptor function. Thus, generator function Yill be considered first. The cells of the generating organ are referred to in the literature as electroplaques, electroplax, electroplates, or electrocytes. We shall follow Bennett(l970) and use the term electrocytes. The electrocytes are derived from the mesoderm (Szabo,_ 1966),the same type of embryonic tissue as muscle except in the South American family Sternarchidae. The origin of the electrocytes The image displays a page from a document, featuring a "TABLE OF CONTENTS". The content is presented in a structured list format with chapter titles and corresponding page numbers. There are no photographs, diagrams, forms, handwritten annotations, or official stamps visible on this page. The text is predominantly black typewriter font, with a specific page number "ii" in the upper right corner. The document appears to be a standard table of contents, lacking any visual elements that would indicate experimental procedures, equipment, or facilities. organ are referred to in the literature as electroplaques, electroplax, electroplates, or electrocytes. We shall follow Bennett(l970) and use the term electrocytes. The electrocytes are derived from the mesoderm (Szabo,_ 1966),the same type of embryonic tissue as muscle except in the South American family Sternarchidae. The origin of the electrocytes of the sternarchids is the same embryonic tissue from which the neural system is derived, the ectoderm (Steinbach, 1970). Electrocytes of mesodermal origin are typically disc shaped, but may also be drum shaped or tubular. Electrocytes of ectodermal origin are U shaped processes from the spinal cord. The electrocytes of the gymnotid, Hypopomus, are between 300-500 in diameter and about 200 The ~ ~thick. electrocytes of Sternopygus on the other hand are rod-shaped and much longer ... -·------.- -------_ ... _ ....... ...... ------·----------.. - ... .. ---· ----- .~J··-----.,~ ~--. ~·· -~··------ --···---~--------- -·-·-·-·----------~ --~--------------~---- - 4 than those of Hypopomus. They are about 1-2 mm in the anterior posterior direction and 200 ~ in diameter. These cells are packed together tightly with little extracellular space, whereas the electrocytes of Hypopomus .. are separated by a considerable amount of extracellular space. The electrocytes are "stacked" in columns in the rear portion of the fish's body to form the electric generating organ. For example, the electric organ of Gnathonemus, a mormyrid, is located just in front of the tail fin and extends forward less than 1/5 of the fish's body length. Gymnarchus' electric generating organ extends from the tail fin to nearly the midpoint. The generating organs of the gymnotid Gymnotus, and of Sternarchus extend further from the tail fin almost to the back of the head. The weakly electric freshwater fish can be categorized in terms of patterns of discharge: those with variable frequency and those with con- stant frequency. Constant frequency fish are defined as those that discharge their electric generating organs at a virtually constant rate even w~en strongly stimulated by an experimenter. Some of these are Eigenmannia, Sternopygus, and the sternarchids. These differences are not absolute, how- ever, and there are species di~ferences in basic rate. The generating organ of the mormyrid Gnathonemus for example, is reported (Bennett, 1970) to dis- charge at frequencies of 30-100 pulses per second (pps). Gyrnnarchus is re- ported to discharge at a frequency of about 250 pps; Gymnotus has a frequency rate of 40-60 pps; Eigenmannia emits pulses at a This page contains a typed document with a header that reads "INTRODUCTION" followed by a single page number "1" on the right. The text discusses electrosensing systems in fish. There are no photographs, handwritten annotations, official stamps, diagrams, tables, or redactions visible on this page. The content is purely textual information presented in a standard document format. The generating organ of the mormyrid Gnathonemus for example, is reported (Bennett, 1970) to dis- charge at frequencies of 30-100 pulses per second (pps). Gyrnnarchus is re- ported to discharge at a frequency of about 250 pps; Gymnotus has a frequency rate of 40-60 pps; Eigenmannia emits pulses at a rate of 250-400 pps; Sterno- pygus fires at 60-100 pps; Steatogenys emits pulses at 40-60 pps; and Hypo 1 porous at 2-20 pps (Hagiwara and Morita, 1963). Sternarchids discharge at 1. Each type of fish has a waveform that is specific to itself. Therefore, although Gymnotus and Steatogenys have the same frequencies, their wave forms.are different. These differences in waveform may be functions of the experimenters' competence in engineering. -------------- - 5 rates of 600-2000 pulses per second (Erskine, Howe & Weed, 1966). Fish that are reported to emit at variable frequency generally increase discharge the~r rate markedly when stimulated. Fish that exhibit this characteristic are the mormyrids (Mandriota, et al, 1965), Hypopomus, Steatogenys, and Gymnotus (Larimer and McDonald, 1968). It should be noted that constant frequency fish do varJ their frequency under certain circumstances. These circumstances include the presence of another signal with frequency close to the fishes'. For example, Eigenmannia which has an organ discharge rate of 400 pps shifts its frequency 10 to 20 pps when confronted with a 400 pps signal (Larimer & McDonald, 1968). In this context, also, is the observation that Gymnarchus temporarily ceases its discharge entirely when presented with a signal mimick 2 ing another Gymnarchus or when startled (Bennett,l970). The mechanisms for controlling electric organ output are in the med- ullary portion of the brain and appear to be similar among weakly electric fish. A small group of cells in the medulla are autoactive and fire syn- chronously, apparently acting as a pacemaker. Their discharge appears to trigger another group of cells in the medulla commonly referred to as med- ullary "relays". Axons from the medullary relay cells descend as part of the spinal cord to synapse on spinal relay neurons. These in turn communi- cate the signal to the electrocytes. The electrocytes of the electric gen- erating organ fire synchronously because of one or more compensatory mechan- isms in the relay pathway from the pacemaker cells. One mechanism is vari- ation in length of the pathway to the electrocytes. The axons to the more distant electrqcytes extend in the straightest possible electrocytes of the electric gen- erating organ fire synchronously because of one or more compensatory mechan- isms in the relay pathway from the pacemaker cells. One mechanism is vari- ation in length of the pathway to the electrocytes. The axons to the more distant electrqcytes extend in the straightest possible line but those to the less distant electrocytes follow a circuitous pattern. A second means of maintaining synchronization involve a delay line mechanism whereby the pathways to the electrocytes differ in conduction velocities. 2. If a passive electric sense is more common than is thought, this could be a protective reaction. A number of investigators have measured the voltage output of the generating organ. Hypopomus is reported to generate a voltage of 8 volts peak to peak when electrodes are placed on the head and tail with the fish more or less out of the water. The same fish in water is reported to generate a voltage of from 10 to 200 millivolts. The in-water measurements were taken with two stainless steel electrodes, one placed in front of the fish and one placed behind the fish. The distance between the electrodes was not given nor was the distance between the electrodes and the fish given. In general, we find that inadequate information is given in the reports of voltage measurements of the electric organ output. Based upon the inadequate information that is reported on voltage measurements and upon measurements that we have made in water, we would suggest ignoring the measurements reported in the literature. In measure ments in our laboratory simulating the reported data, we found that the water acts as a very high distributive resistance. When an oscilloscope is used in the typically reported fashion to measure the fishes' voltage output the input impedence of the scope is being placed in parallel with the resistance of the water. Even when a high input impedence scope is used, there is a loading effect upon the circuit. Thus, we believe, based upon our measurements and the reported investigations, that the investigators have been inadvertently loading down the fish's electric field generator through the use of their measuring devices. We can summarize the salient points by saying that these fish generate a pulsed electrical field in the water. The generator is located in the posterior portion of the body. The generator components have their outputs synchronized by a clock. In some This document page is primarily composed of typed text, presenting a scientific or technical discussion. There are no photographs, handwritten annotations, official stamps, forms, diagrams, schematics, organizational charts, tables, or redacted content visible on this page. The visual appearance is solely that of neatly typed paragraph-style text, suggesting a report or research paper. The document page is a black and white scan of typed text. There is a single digit "3" in the top right corner, possibly a page number. The text is arranged in paragraphs, with a heading "Generator Organ" set apart. There are no images, handwritten annotations, stamps, forms, diagrams, tables, or redactions visible on this page. The content appears to be scientific or technical in nature, discussing electrical fields, fish species, and biological tissues. generator through the use of their measuring devices. We can summarize the salient points by saying that these fish generate a pulsed electrical field in the water. The generator is located in the posterior portion of the body. The generator components have their outputs synchronized by a clock. In some species the clock is more or less invarient, in others it varies, in part, as a function of external events. The reason -------------~·--~---~ - 7 for this difference among species is unknown. The voltage output of the generator and the effective range of the field are unknown due inadequate t~ measurement technique. Receptor Orga..t'l The weakly electric freshwater fish are reported to have both active and passive sensory systems. The active system primarily detects disturb- ances in the fish generated E field. The passive system is primarily sensi- tive to energy provided by extrinsic sources. We are not so sure that the data really indicates two such systems in the same fish, but we shall follow the convention for the time being. There is better evidence that there are a number of fish, such as sharks and gold fish, that have good passive electrosensing systems but no active system. These latter fish and passive systems are not considered, as such, in this paper. Gymnotid receptors. There are two basic types of electroreceptor organs reported in the literature. The differences may be more apparent than real terms of function. i~ The ampullary organs are believed to be the passive system sensors. -- They consist of cells that maintain a continuous rhythmic background firing (low rate spontaneous impulses from the receptor to the brain). Thus, they are referred to as tonic receptors. This background firing appears to be unrelated to electric organ discharge. The background firing shifts smoothly to a higher or lower rate in response to the electrical sources moving into the fish's range. The response to a brief stimulus, for example, is acceleration followed by deceleration. The acceleration phase can outlast the stimulus and according to Bennett (1970) there is accomodation to maintained stimuli. These receptors are sensitive to low frequency electrical fields and to changes in a DC field. - 8 Their response to an applied current is a monotonic increase. The active system sensors are called tuberous organs. They are more rapidly adapting than tonic receptor5. They are sensitive to relatively high frequency stimuli and are insensitive to frequency electrical fields and to changes in a DC field. - 8 Their response to an applied current is a monotonic increase. The active system sensors are called tuberous organs. They are more rapidly adapting than tonic receptor5. They are sensitive to relatively high frequency stimuli and are insensitive to applied DC. Their firing is related to electric organ discharge in that they respond with a train of pulses to each electric organ discharge. Thus, they are referred to as phasic receptors~ As seen on the skin, the ampullary and tuberous organs differ. They also differ in appearance from mechanoreceptors, i.e., canal organs and free neuromasts. The tuberous organ appears on the skin surface as a single small pore, even though it has no opening. The ampullary organs appear as a group of small pores. As an indication of the number of recept ors found on a fish, it can be noted that Lissmann and Mullinger (1968) found that there were 2,000 ampullary and tuberous organs on a 6 em. long Steato genys. Most receptors, about 95 percent, are phasic receptors according to Lissmann and Mullinger (1968). In considering the fine structure of the receptor organs, it can be noted that the ampullary has the appearance of a flask with a narrow o~gan duct (5-20 ~ in diameter) leading from the skin surface to a cavity (30- 40 ~ in diameter) that is located 100-500 ~ within the skin. Embedded in the cavity wall with only a small surface exposed are the sensing cells of the organ. These sensing cells are 10-15 in diameter with each organ ~ containing two to eight of them. Some microvilli 0.8 ~ long are irregularly distributed on the exposed surface of the sensing cells. Filling the duct and cavity is a jelly-like substance with no known function. All sense cells in one organ feed their signals to the same nerve fiber. The nerve myeli~ated is unmyelinated within the organ, having lost its myelin sheath and dividing before entering tlw or;"ll.n. A .....~ ~---MICROVILLI ;n-.~+----REC EPTO R H----SUPPORTING ctLLS l...I...Wl±:!::~'-----N ERVE Fl BE R-----'~::lJ.,;~ r...----LOOSE EPITHELIAL CELLS ~~~~~~\\t~--.~OVERING CELLS LAVER OF' CAPSULE B -Ht---RCCCPTOR cru. rH~-HrtH---Mf"Vt. TERMINAL MI£.~:J.pW'M~~~fH-----5UPPORTIN<Z CELL '--.f.A-....1-A+J--+-~~'L---NERVE F' I BE R SURFACE RECEPTOR CELL SUBSTANCE CELL c BASEMENT MEMBRANE ~~~SUBSEHSORY PLATFORM ~_w~ A---HERVE BASEMENT MEMBRANE D Fig.l a) Schematir. drawing of the two types of ampulla of gymno tids, b) Schematic drawing The image displays a typewritten document with handwritten annotations. A large number "4" is present at the top right, possibly a page number, and a small number "1" is underlined and placed to the left of a numbered list item "1." The document itself appears to be a scientific or technical report, discussing fish and their electric organs, with technical terms like "electrocytes," "Gnathonemus," "Gymnotus," and frequencies in "pps." There are no photographs, diagrams, stamps, or evidence of experimental procedures visible on this page. The text is the primary and sole content of the image. The image is a scanned page of a declassified document containing the number "5" in the top right corner, indicating it is page 5 of a larger document. The page is filled with printed text, arranged in paragraphs describing electric fish. There are no photographs, handwritten annotations, official stamps, forms, diagrams, schematics, tables, or redactions visible on the page. The content is purely textual, with the exception of the page number. There is no visual evidence of experimental procedures, equipment, or facilities. EPITHELIAL CELLS ~~~~~~\\t~--.~OVERING CELLS LAVER OF' CAPSULE B -Ht---RCCCPTOR cru. rH~-HrtH---Mf"Vt. TERMINAL MI£.~:J.pW'M~~~fH-----5UPPORTIN<Z CELL '--.f.A-....1-A+J--+-~~'L---NERVE F' I BE R SURFACE RECEPTOR CELL SUBSTANCE CELL c BASEMENT MEMBRANE ~~~SUBSEHSORY PLATFORM ~_w~ A---HERVE BASEMENT MEMBRANE D Fig.l a) Schematir. drawing of the two types of ampulla of gymno tids, b) Schematic drawing of the tuberous organ of the gymnotid, c) Schematic drawing of the mormyromast of the mormyrid, d) Sche matic drawing of the tuberous organ of the mormyrid. 9 There are a great many clusters of five to fifteen ampullary receptor cells on the head. On the body there are fewer clusters and they tend to be restricted to 3 bands that extend longitudinally along the fish.~ The tuberous organ consists of a bulb shaped invagination of the skin as shown in Fig. lb. The side of the bulb is composed of 10 to 50 layers of flattened cells for a.total thickness of 2-5 The bottom of the bulb ~. is made of supporting cells upon which the numerous sensing cells rest. ~P The sensing cells are 25-30 long and project somewhat like rods into the ~ cavity of the bulb. They are ordered such that the gap between adjacent sensory cells is relatively constant. Each sensory cell is covered on the cavity end with microvilli 0.7 The cavity is filled with a fluid ~long. or possibly jelly-like substance. Loose epithelial-like cells fill much of the cavity above the sensory cells and appear to plug the pore to the surface. The sensory cells feed their signals to a single nerve which, in most cases, loses its myelin sheath where it passes into the tuberous organ. In a small proportion of the tuberous organs the myelin sheath is retained until the nerve fiber enters the sensory cell. The tuberous organs are randomly dis- tributed on the head, where.j;hey are most numerous, and on the anterior half of the body. On the posterior half of the body the tuberous organs are found · in four longitudinal bands. Mormyrid receptors. In Mormyrids, the electroreceptors are referred to as mormyromasts and Knollenorgans (Szabo, 1967). The mormyromast is a two level organ that contains at the surface level sensory cells (type A) similar to the ampullary sensory cells and at the second level sensory cells (type B) similar to the sensory cells of the tuberous organ of the gyrnnotids. TYPes A and B sensory cells are mormyromast is a two level organ that contains at the surface level sensory cells (type A) similar to the ampullary sensory cells and at the second level sensory cells (type B) similar to the sensory cells of the tuberous organ of the gyrnnotids. TYPes A and B sensory cells are always separately innervated. 3. The fish being described is Hypopomus artedi, a species of gymnotid. Details vary slightly from species to species. 10 The type A sensory cells form one or two concentric aureoles at the base of a "jelly sphere" located near the surface of the skin af:! sho'Wil in Fig. lc. In the center of this aureole, a small duct leads to a more deeply situated sensory chamber in the skin within which the type B cells arc located. The inner surface of the duct wall bears tiny microvilli. The duct as well as the lower sensory chamber is filled with a.....m"..lcous substance. Two to five sensory cells occupy the lower sensory chamber. The type B cells with their supporting cell platform though similar to the tuberous organ are smaller. They do not completely fill up the sensory chamber and their free surfaces bear a large number of microvilli. The type B sensory cells in a mormyromast are innervated by a single nerve fiber which splits immediately after penetration through the supporting cells into several to serve the sensory cells. Where the nerve joins br~~ches the type B sensory cell membrane a rod like projection, 0.5 in size, occurs ~ within the sensory cell. Each type A sensory cell is encircled by several accessory cells. The sensory cells their accessory cells are bottle-shaped. The apical or ~~d tip portion of both sensory and accessory cells contact the jelly sphere. The nerve fibers innervating type A cells lose their myelin sheath before entering the receptor organ and pass among the accessory cells to contact the sensory cells. As with type B cells, where the nerve joins the sensory cell, there is a rod present at the sensory cell membrane. The mormyrids also have receptor organs, knollenorgans, which are some what similar to the tuberous organs of the gymnotids. Derbin and Szabo (1968) describe them as being composed of three or four sensory cell complexes one of which is shown in Fig. ld. Each complex is a single sensory cell attached to a highly differentiated supporting platform of cells. The The document is a typed page, likely from a scientific report, detailing voltage measurements of an electric organ in fish. There are no photographs, handwritten annotations, stamps, forms, diagrams, tables, or redactions visible on this page. The content is purely textual, discussing experimental procedures and findings related to the electric fish. what similar to the tuberous organs of the gymnotids. Derbin and Szabo (1968) describe them as being composed of three or four sensory cell complexes one of which is shown in Fig. ld. Each complex is a single sensory cell attached to a highly differentiated supporting platform of cells. The organ is inner vated by single nerve fiber which is derived from a nerve that appears to - 11 serve many sensory cells. The sensory cell lies in and almost completely fills a cavity in the skin at the surface. The wall of the