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Journal of Comparative Physiology A

, Volume 161, Issue 3, pp 417–430 | Cite as

Coordination of EOD frequency and pulse duration in a weakly electric wave fish: the influence of androgens

  • Alice Mills
  • Harold H. Zakon
Article

Summary

  1. 1.

    The electric organ discharge (EOD) of wave-type weakly electric fish is generated as an extremely regular series of electric organ pulses. Measurements of pulse duration and EOD frequency were made in the speciesSternopygus andEigenmannia. Pulse duration is highly inversely correlated with EOD frequency in a population of fish, so that the EOD waveform remains quasisinusoidal over the species range of EOD frequencies. This places most of the energy of the EOD within the fundamental harmonic to which the electroreceptors are most sensitive.

     
  2. 2.

    Treatment with the anesthetic MS-222 transiently lowers EOD frequency, but does not change pulse duration. This demonstrates that pulse duration is independent of immediate EOD frequency and, therefore, of the medullary pacemaker nucleus (PMN).

     
  3. 3.

    InSternopygus, small monophasic potentials could be recorded outside the tails of curarized fish. These were of constant duration and shape across all fish regardless of the fish's EOD frequency. The location along the body where this potential reversed polarity was close to, although not identical with, the isopotential line for the EOD pulse. These potentials were partially blocked by the curare. They probably represent the summed psps of the synchronously-firing electrocytes. This result supports the hypothesis that differences in EOD waveform, specifically pulse duration, arise from electrocyte membrane events following the psp (postsynaptic potential).

     
  4. 4.

    Implantation ofSternopygus with 5-α-dihydrotestosterone (DHT) in silastic capsules results in decreased EOD frequencies, as previously reported for this species (Meyer and Zakon 1982; Meyer 1983). In addition, corresponding significant increases in EOD pulse duration occurred (a mean increase of about 1.3 ms or 24%). No changes were measured in controls implanted with empty capsules. The maximum decrease in EOD frequency and increase in pulse duration plateau at different times, suggesting that they are the result of different processes. After removal of the hormone capsules, EOD frequency and pulse duration reverted to baseline levels within a few weeks.

     
  5. 5.

    These results demonstrate a degree of coordination between the PMN and the electric organ not previously recognized. It is likely that androgens play a role in this process. If, as proposed, the electrocyte membrane properties determine the characteristics of the waveform, then the androgen must act on both the PMN and the electrocytes to keep EOD frequency and pulse duration in register.

     

Keywords

Androgen Pulse Duration Electric Organ Electric Organ Discharge Electric Organ Discharge Frequency 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

DHT

5-α-dihydrotestosterone

EOD

electric organ discharge

FFT

Fast Fourier Transform

PMN

medullary pacemaker nucleus

psp

postsynaptic potential

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References

  1. Bass AH (1986a) Electric organs revisited: Evolution of a vertebrate communication and orientation organ. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley, New York, pp 13–70Google Scholar
  2. Bass AH (1986b) Species differences in electric organs of mormyrids: substrates for species-typical electric organ discharge waveforms. J Comp Neurol 244:313–330Google Scholar
  3. Bass AH, Hopkins CD (1983) Hormonal control of sexual differentiation: changes in electric organ discharge waveform. Science 220:971–974Google Scholar
  4. Bass AH, Hopkins CD (1984) Shifts in frequency tuning of electroreceptors in androgen-treated mormyrid fish. J Comp Physiol A 155:713–724Google Scholar
  5. Bass AH, Hopkins CD (1985) Hormonal control of sex differences in the electric organ discharge (EOD) of mormyrid fishes. J Comp Physiol A 156:587–604Google Scholar
  6. Bass AH, Volman SF (1985) Steroid-induced changes in action potential waveform of an electric organ. Soc Neurosci Abstr 11:159Google Scholar
  7. Bass AH, Segil N, Kelley DB (1986) Androgen binding in the brain and electric organ of a mormyrid fish. J Comp Physiol A 159:535–544Google Scholar
  8. Bass AH, Denizot J-P, Marchaterre MA (1986a) Ultrastructural features and hormone-dependent sex differences of mormyrid electric organs. J Comp Neurol 254:511–528Google Scholar
  9. Bastian J (1977) Variations in the frequency response of electroreceptors dependent on receptor location in weakly electric fish (Gymnotoides) with a pulse discharge. J Comp Physiol 121:53–64Google Scholar
  10. Bastian J (1981) Electroreception II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells inApteronotus. J Comp Physiol 144:481–494Google Scholar
  11. Bennett MVL (1961) Modes of operation of electric organs. Ann NY Acad Sci 54:458–509Google Scholar
  12. Bennett MVL (1971) Electric organs. In: Hoar WS, Randall DJ (eds) Fish physiology, vol V. Academic Press, New York, pp 347–491Google Scholar
  13. Bennett MVL, Pappas GD, Gimenez M, Nakajima Y (1967) Physiology and ultrastructure of electrotonic junctions IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol 30:236–300Google Scholar
  14. Blaustein MP, Goldman DE (1966) Competitive action of calcium and procaine on lobster axon: a study of the mechanism of action of certain local anesthetics. J Gen Physiol 49:1043–1063Google Scholar
  15. Bullock TH (1982) Electroreception. Annu Rev Neurosci 5:121–170Google Scholar
  16. Bullock TH, Hamstra RH, Scheich H (1972) The jamming avoidance response of high frequency electric fish. J Comp Physiol 77:1–22Google Scholar
  17. Caldwell J (1976) Behavior, psychic, neuropharmacologic, and physiological aspects: physiological aspects of cocaine usage. In: Mule SJ (ed) Cocaine — chemical, biological, clinical, social, and treatment aspects. CRC Press, Cleveland, pp 188–199Google Scholar
  18. Elekes K, Szabo T (1981) Comparative synaptology of the pacemaker nucleus in the brain of weakly electric fish (Gymnotoidae) In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates. Pergamon Press, New York, pp 225–278Google Scholar
  19. Ellis DB, Szabo T (1980) Identification of different cell types in the command (pacemaker) nucleus of several gymnotiform species by retrograde transport of horseradish peroxidase. Neurosci 5:1917–1929Google Scholar
  20. Enger PS, Szabo T (1968) Effects of temperature on the discharge rates of the electric organ of some gymnotids. Comp Biochem Physiol 27:625–627Google Scholar
  21. Fatt P, Katz B (1951) An analysis of the end-plate potential recorded with an intra-cellular electrode. J Physiol 115:320–370Google Scholar
  22. Fostier A, Jalabert B, Billiard R, Breton B, Zohar Y (1983) The gonadal steroids In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol 9 A. Academic Press, New York, pp 277–372Google Scholar
  23. Frey AH, Eichert ES (1972) The nature of electrosensing in the fish. Biophysics J 12:1326–1358Google Scholar
  24. Gottschalk B (1981) Electrocommunication in gymnotid wave fish: significance of a temporal feature in the electric organ discharge. In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates. Pergamon Press, New York, pp 225–278Google Scholar
  25. Hagedorn M, Carr C (1985) Single electrocytes produce a sexually dimorphic signal in South American electric fishHypopomus occidentalis (Gymnotiformes, Hypopomidae). J Comp Physiol A 156:511–523Google Scholar
  26. Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotid fish. Anim Behav 33:254–265Google Scholar
  27. Heiligenberg W (1977) Principles of electrolocation and jamming avoidance. In: Braitenberg V (ed) Studies of brain function. Springer, Berlin Heidelberg New York, pp 1–65Google Scholar
  28. Hodgkin AL, Huxley AF (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon ofLoligo. J Physiol 116:449–472Google Scholar
  29. Hopkins CD (1972) Sex differences in electric signalling in an electric fish. Science 176:1035–1037Google Scholar
  30. Hopkins CD (1974a) Electric communication in fish. Am Sci 62:426–437Google Scholar
  31. Hopkins CD (1974b) Electric communication in the reproductive behavior ofSternopygus macrurus (Gymnotoidei). Z Tierpsychol 35:518–535Google Scholar
  32. Hopkins CD (1976) Stimulus filtering and electroreception: Tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol 111:171–207Google Scholar
  33. Hopkins CD (1980) Evolution of electric communication channels of mormyrids. Behav Ecol Sociobiol 7:1–13Google Scholar
  34. Hopkins CD, Bass AH (1981) Temporal coding of species recognition signals in an electric fish. Science 212:85–87Google Scholar
  35. Keller CH, Zakon HH, Sanchez DY (1986) Evidence for a direct effect of androgens upon electroreceptor tuning. J Comp Physiol A 158:301–310Google Scholar
  36. Keynes RD, Martins-Ferreira H (1953) Membrane potentials in the electroplates of the electric eel. J Physiol 119:315–351Google Scholar
  37. Mazeaud MM, Mazeaud I, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with a general review. Trans Am Fish Soc 106:201–212Google Scholar
  38. Meyer JH (1983) Steroid influences upon the discharge frequencies of a weakly electric fish. J Comp Physiol 153:29–37Google Scholar
  39. Meyer JH, Zakon HH (1982) Androgens alter the tuning of electroreceptors. Science 217:635–637Google Scholar
  40. Meyer JH, Zakon HH, Heiligenberg W (1984) Steroid influences upon the electrosensory system of weakly electric fish: direct effects upon discharge frequencies with indirect effects upon electroreceptor tuning. J Comp Physiol A 154:625–631Google Scholar
  41. Meyer JH, Leong M, Keller CH (1987) Hormone-induced and ontogenetic changes in electric organ discharge and electroreceptor tuning in the weakly electric fishApterotnotus. J Comp Physiol A 160:385–394Google Scholar
  42. Mills A, Zakon HH (1986) EOD frequency and pulse duration are independently determined but coordinated. Soc Neurosci Abstr 12:313Google Scholar
  43. Nakamura Y, Nakajima S, Grundfest H (1964) Analysis of spike electrogenesis and depolarizing K+ inactivation in electroplaque ofElectrophorus electricus L. J Gen Physiol 49:321–349Google Scholar
  44. Shanes AM (1950) Drug and ion effects in frog muscle. J Gen Physiol 33:729–744Google Scholar
  45. Taylor RE (1959) Effects of procaine on electrical properties of squid axon membrane. Am J Physiol 196(5): 1071–1078Google Scholar
  46. Viancour TA (1979) Electroreceptors of a weakly electric fish. II. Individually tuned receptor oscillations. J Comp Physiol 133:327–338Google Scholar
  47. Westby GWM, Kirschbaum F (1978) Emergence of development of the electric organ discharge in the mormyrid fish,Pollimyrus isidori II. Replacement of the larval by the adult discharge. J Comp Physiol 127:45–59Google Scholar
  48. Westby GWM, Kirschbaum F (1981) Sex differences in the electric organ discharge ofEigenmannia virescens and the effects of gonadal maturation. In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates. Pergamon Press, New York, pp 179–194Google Scholar
  49. Westby GWM, Kirschbaum F (1982) Sex differences in the waveform of the pulse-type electric fishPollimyrus isidori (Mormyridae). J Comp Physiol 145:399–403Google Scholar
  50. Zakon HH (1986) The emergence of tuning in newly generated tuberous electroreceptors. J Neurosci 6:3297–3308Google Scholar
  51. Zakon HH, Meyer JH (1983) Plasticity of electroreceptor tuning in the weakly electric fish,Sternopygus dariensis. J Comp Physiol 153:477–487Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • Alice Mills
    • 1
  • Harold H. Zakon
    • 1
  1. 1.Department of ZoologyThe University of Texas at AustinAustinUSA

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