Journal of comparative physiology

, Volume 133, Issue 4, pp 327–338 | Cite as

Electroreceptors of a weakly electric fish

II. Individually tuned receptor oscillations
  • Terry A. Viancour
Article

Summary

The hypothesis of an active electroreceptor filter, characterized by an underdamped, oscillatory impulse response, was tested indirectly by investigating the pattern of afferent discharges resulting from receptor excitation with electric field pulses. When stimulated with a single, high amplitude, short duration pulse the majority of afferents responded with bursts of two or three spikes having interspike intervals, in individual fish, correlated to the individual's electric organ discharge period, and, more importantly, with the best frequency of the corresponding receptor. Pulses causing current to flow into the receptor from the bath resulted in shorter response latencies and more spikes per burst than pulses of the opposite polarity. The polarity dependent latency shift was also correlated with the best frequency of the receptor and the electric organ discharge repetition rate of an individual, but it was much shorter than expected based on the prediction of a generator potential in the form of a classical underdamped oscillation. Because of this it is concluded that the generator potential oscillations increase in period for successive cycles. This was essentially confirmed by the form of the receptor organ excitability cycle which was measured by using a two pulse stimulus paradigm.

Further confirmation of the existence of an oscillatory generator potential was obtained by recording compound action potentials from the afferent nerve and comparing the single peaked potentials obtained by direct nerve shock with the multipeaked potentials evoked by receptor activity in response to electric field pulses in the water.

The physiological properties of tuberous electroreceptors are nearly the same as the properties of receptors in the phylogenetically related vertebrate auditory system. This leads to the suggestion that the two systems have in common similar physiological mechanisms, and that the oscillatory receptor properties observed for electroreceptors may serve, in the auditory system, as the basis for a proposed second filter.

Keywords

Electric Field Pulse Interspike Interval Compound Action Potential Good Frequency Electric Organ Discharge 

Abbreviations

EOD

electric organ discharge

mn

mean of the distribution

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References

  1. Bastian, J.: Frequency response characteristics of electropreceptors in weakly electric fish (Gymnotoidei) with a pulse discharge. J. Comp. Physiol.112, 165–180 (1976)Google Scholar
  2. Bennett, M.V.L.: Mechanisms of electroreceptors. In: Lateral line detectors. Cahn, P. (ed.), pp. 313–393. Bloomington: University of Indiana Press 1967Google Scholar
  3. Bullock, T.H.: The reliability of neurons. J. Gen. Physiol.55, 563–584 (1970)Google Scholar
  4. Bullock, T.H., Chichibu, S.: Further analysis of sensory coding in electroreceptors of electric fish. Proc. Natl. Acad. Sci. USA54, 422–429 (1965)Google Scholar
  5. Bullock, T.H., Horridge, G.A.: Structure and function in the ner vous systems of invertebrates, Vol. 1, p. 149. San Francisco: Freeman 1965Google Scholar
  6. Evans, E.F.: The effects of hypoxia on the tuning of single cochlear nerve fibres. J. Physiol.238, 65–67 (1973)Google Scholar
  7. Evans, E.F., Klinke, R.: Reversible effects of cyanide and furosemide on the tuning of single cochlear nerve fibers. J. Physiol.242, 129–131 (1974)Google Scholar
  8. Evans, E.F., Wilson, J.P.: Cochlear tuning properties: concurrent basilar membrane and single nerve fiber measurements. Science190, 1218–1221 (1975)Google Scholar
  9. Hagiwara, S., Kusano, K., Negishi, K.: Physiological properties of electroreceptors of some gymnotids. J. Neurophysiol.25, 430–449 (1962)Google Scholar
  10. Hagiwara, S., Morita, H.: Coding mechanisms of electroreceptor fibers in some electric fish. J. Neurophysiol.26, 551–567 (1963)Google Scholar
  11. Hagiwara, S., Szabo, T., Enger, P.S.: Electroreceptor mechanisms in a high-frequency weakly electric fishSternarchus albifrons. J. Neurophysiol.28, 784–799 (1965)Google Scholar
  12. Hall, J.L.: Spatial differentation as an auditory “second filter”: Assessment of a nonlinear model of the basilar membrane. J. Acoust. Soc. Am.61, 520–524 (1977)Google Scholar
  13. Hopkins, C.D.: Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J. Comp. Physiol.111, 171–207 (1976)Google Scholar
  14. Hopkins, C.D., Heiligenberg, W.F.: Evolutionary designs for electric signals and electroreceptors in gymnotoid fishes of Surinam. Behav. Ecol. Sociobiol.3, 113–143 (1978)Google Scholar
  15. Kiang, N.Y.S., Watanabe, T., Thomas, E.C., Clark, L.F.: Discharge patterns of single fibers in the cat's auditory nerve. Cambridge: M.I.T. Press, Res. Monograph 35, 1965Google Scholar
  16. Scheich, H., Bullock, T.H., Hamstra, R.H., Jr.: Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fishEigenmannia. J. Neurophysiol.36, 39–60 (1973)Google Scholar
  17. Suga, N.: Coding in tuberous and ampullary organs of a gymnotid electric fish. J. Comp. Neurol.131, 437–452 (1967)Google Scholar
  18. Szabo, T.: Activity of peripheral and central neurons involved in electroreception. In: Lateral line detectors. Cahn, P. (ed.), pp. 295–311. Bloomington: University of Indiana Press 1967Google Scholar
  19. Viancour, T.A.: Neuronal response autorhythmicity associated with non-mechanical frequency filtering in the electrosense system ofEigenmannia virescens. Neurosci. Abstr.2, 229 (1976)Google Scholar
  20. Viancour, T.A.: Electroreceptors of a weakly electric fish. I: Characterization of tuberous receptor organ tuning. J. Comp. Physiol.133, 317–325 (1979)Google Scholar
  21. Wachtel, A.W., Szamier, R.B.: Special cutaneous receptors of fish: the tuberous organs ofEigenmannia. J. Morphol.119, 51–80 (1966)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • Terry A. Viancour
    • 1
    • 2
  1. 1.Department of Neuroscience A-001University of California, San DiegoUSA
  2. 2.Neurobiology UnitScripps Institution of OceanographyLa JollaUSA

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