ELECTRIC TRANSMITTING ORGANS AND DETECTION PROCESS HYPOTHESES IN ELE- CTRIC FISHES 4 February 1974 Most authors and scholars of electric fishes agree that: 1. The anatomy and physiology of the electric organs of different species are diverse; 2 The diversity amohg species stronoly sugcest that the electric orc,,an-electroreceptor system plays quite different roles in the biology of different species. But what is this role is not known .as of today; 3. Some classification has been made with regard to their transmitting electric oroan as follows: a. low resting frequency, high standard deviation of interval 2 lengths and respondino- to different kinds of stimuli with a many-fold increase in frequency and amplitude of the sional (for example, Gnathonemus petersii)., b. medium restin- frequency, medium standard deviation of interval lengths, responding to some stimuli with a several- fold increase in frequency (for example, Gymnotus carap6o),' C. medium frequency with little or no change in the repetition rate of the siernal, but with the possibility to stop completely the discharge (for example,, Gyi-nnarclius niloticus), d. hi-h restin- frequency with low standard deviation, respondin- r.,> CP to a few special stimuli with small shifts in repetition rate of the signal (for example, Sternarclius albifrons), e. species with no known response to stimuli with chanae in 2 CD the repetition rate of the signal. 4. The discharge of the electric organ has been found to be commanded from a pacemaker center in the medulla, in most species studied until now. (See Fio,. 1.) This train of impulses seems to be re- layed 1:1 in a nucleus in the medulla and again in the electro2motor neurons in the spinal cord to be passed through the spinal nerves to the electric transmittino, organ. Some electric fishes have a very elaborate array of electroreceptors. All electric fishes have other sensory receptors mostly part of the lateralis line system like: temperature receptors, mechanical receptors and water- displacement receptors. These sensory receptors are located2 in the dermis. There are other sensory receptors non-related to the lateralis line like: acoustical receptors., chemical receptors,, olfactory receptors., taste receptors and in some electric fishes optical receptors (vision)' not to mention equilibrium and stabilizincr receptors. All these sensory receptors, electric and nonelectric, may work separately or in accordance in a hybrid cross correlation information 2system used in social interaction, feeding, swimming and navicration, in offense or defense. Because of the multiplicity of use the sensory system is very com- .plicated usin- neuronal preprocessin-s and discriminating filterin- systems,, delay-lines, etc. is Some electric fishes use p, sive and/or ,tctive object detection systems. Th0ere .ire some marine and fresh-iv,,iter fishes which do not have any electric traiismittin- or,-an, but have ,in electroreceptor system. (Marine sh,,irks lil:c: 2 c 4 ELECTR'C- 0 itr.Ati 'PA 2 4Af.!,j - f SIPE) Fig. 1. Connection between the pacemaker in the brain, the relay nuclei, the electromotor neurons, the electric transmittin- or-an and the electrore- t=k t:l 0 ceptors in electric fishes. 3 Neo- ,-,iprion brevirostris, Scilliorhinus canicula, a catfish: Plotosus or the eel An@,milla an@,uilla and freshwater fishes like Clarias.) A classification of electroreceptors can be made from the followincr r> criteria: 1. Autorhytmic2. This means that they emit a very low amplitude signal from less than one to a few millivolts. Depending on the particular receptor class it can have a. low repetition rate (less than 100). a medium repetition rate (from 100 to 500) or a high repetition rate (from 500 to 3000), 2. Nonautorhytmic. 2 or we can divide them in: 3. Synchronous. This means that they respond to the transmittina =P organ in case of a stimulus with a nerve transmission spike rate synchronized to the electric oraan. 4. Nonsynchronous. Another classification could be used as: 2 5. Ampullary organs similar to or identical with the Lorenzini amnulla which has a canal lined with a very hiah resistance membr ne filled with a jelly and communicatincr to an ampulla with sensory orcrans.-- The jelly can be high, medium or low con- ductive and accordingly beincr acid, neutral or basic. There are many kinds of 2sensory cell formation classes. 6. Tuberous or mormyromasts, mostly not directly connected to the surface of the skin. Every mormyromast may have one, two or more sensory cells separately innervated and respondin- each to different amplitudes (levels) of stimuli. Maybe a more adequate classification would be one talcincr into account the 3stimuli to which these electroreceptors respond such as: 4 a. Conductivity: conductinc,r or nonconductin,- objects, the level of responi@e-bein- more or less proportional to their conductivity factor; b. Direction: response of the sensory cells bein- conditioned to 0 the fact that an object is directed toward or away from the fish; 2 c. Form: sharp ed-es will stimulate some receptors, others will be stimulated by round or rounded objects; d. Movement: the chanae in position or form of an object will pro- duce a m@@dulation of the autorhytmic impulses of some receptors and will be sensed by the fish; e. Smoothness or Rouchness of objects could also constitute a criter2ia of stimuli classification; f. Chemicals in the water may affect the electric receptors and their response., we have proof for this. Finally codina- can be a classification criteria. -Lissman and Machin. proposed a 1. "Pulse-frequency-modulation" (like in Gymnarchus niloticus); Watanabe and Bullock proposed a 2 2. "Pulse-phase modulation" (like in Eicenmannia virescens); Szabo and HaaiNvara analyzed and sua,,crested three other kinds of codino-s: 3. "Number cocl,:n-- mechanism" (like in gymnotidsas: Hypopomus artedi), 4. "Probability codin- mechanism" (like in gymotids as: Stern-,irchiis t> 8 albifrons)., 5. "Latency codin(r mechanism" (like in mormyrids as: Gnathoiiei-lius petersii). 5 Accordin- to the first hypothesis "Pulse-frequency modulation" sen- sory information should -be conveyed by the frequency of the sensory impulses dependent on the pulse of the electric dischar,-es. The second hypothesis "Pulse-phase modulation" the sensory codincr co is the result of time relation (the phase) on the2 sensory impulse followin- the electric organ discharo-e. t), The third hypothesis called the "Number codino- mechanism" supposes t> that the intensity of the electric potential field is coded throuah a single electro- receptor fiber by the number of nerve impulses produced by each electric 2 organ pulse. In the number four hypothesis, called "Probability codina, mechanism, the coding is provided by the probability that each electric orcran impulse might initiate an impulse in the nerve fiber. Finally the fifth hypothesis: "Latency coding mechanism" is explained by the fact that certain mormyrid electroreceptors permit a chanae in latency of impulses of the electric organ relate2d to the intensity of the current flowino- throucrh the receptor. Therefore, the intensity of the potential field can be coded by the time relation betwee.n electric transmittincr organ discharge and sensory impulse, the time ranging being as much as 8 milliseconds. For variations in the superthreshold field intensity this would be the only mech- anism for a sensory organ producing sinale spikes. The place wher2e the latency-shift of the sensory impulse is takina place has not as yet unequivoc- ally explained. It is worth meiitionin(, that there ,tre electroreceptors connected to t> nerve fibers which would not transmit any impulses without a specific stimulus. Otlier electroreceptors are related to ilerve fibers discli.,tr,-in- continuou4sly. t> 6 Some, when presented with stimuli, would increase their electric activity and others would decrease it. The first type of fibers are called phasic fibers, the second type are called tonic fibers. Electroreceptors connected to phasic nerve fibers are called phasic electroreceptors (i.e., tuberous orcrans = mormyromasts); electroreceptors connected to tonic fibers are called tonic electroreceptors6 (i.e., ampullary or,-,ans like the Lorenzini ampulla). 7