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Evidence for a direct effect of androgens upon electroreceptor tuning

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Summary

  1. 1.

    Tuberous electroreceptors of individual wave type weakly electric fish are tuned to the fundamental frequency of that fish's electric organ discharge (EOD). EOD frequency and receptor best frequency (BF) are both lowered following systemic injection of 5-α-dihydrotestosterone (DHT). A previous study (Meyer et al. 1984) showed that the effect of DHT on the EOD generating circuitry was independent of an ongoing EOD and suggested that its effect on electroreceptor tuning was indirect, possibly mediated by the electric field. We have continued these studies to determine the factors which influence electroreceptor tuning.

  2. 2.

    Baseline recordings of EOD frequency, receptor oscillations, and single afferent tuning curves were taken. After fish were electrically silenced by spinal cord transection they were injected daily with either DHT or saline or were implanted with either DHT-filled or empty silastic capsules.

  3. 3.

    As previously reported, the EOD frequency (determined from pacemaker nucleus recordings) was lowered in DHT-treated, transected fish and increased in control fish.

  4. 4.

    Similarly, receptor tuning was lowered in the DHT-treated, silenced fish. Oscillation frequencies decreased in both treated and control groups, but significantly more in the hormone group. Single afferent best frequencies were lowered in both DHT groups and raised in their respective control groups.

  5. 5.

    In another series of experiments exogenous electric fields capable of driving receptors in a 1-to-1 phase-locked manner were placed around silenced fish. We were unable to elicit any shift in pacemaker frequency or electroreceptor tuning regardless of stimulus field geometry.

  6. 6.

    Four transected fish were injected with DHT and placed in exogenous electric fields of higher frequency than their original EOD. Even in the presence of a higher frequency electric field, DHT lowered EOD frequency and afferent BF.

  7. 7.

    We conclude that androgens produce effects both on the EOD generating circuitry, probably at the level of the pacemaker nucleus, and on electroreceptors, probably, ultimately, on receptor cell membrane conductances. These effects occur in parallel allowing the two parameters to remain well matched. In contrast to former predictions, exogenous electric fields alone appear unable to shift receptor tuning.

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Abbreviations

EOD :

electric organ discharge

ΔEODp :

normalized change in electric organ discharge frequency

BF :

best frequency

ΔBFp :

normalized change in best frequency

OSC :

receptor oscillation frequency

ΔOSCp :

normalized change in receptor oscillation frequency

DHT :

5-α-dihydrotestosterone

References

  • Bass AH, Hopkins CD (1983) Hormonal control of sexual differentiation: changes in electric organ discharge waveform. Science 220:971–974

    Google Scholar 

  • Bass AH, Hopkins CD (1984) Shifts in frequency tuning of electroreceptors in androgen-treated mormyrid fish. J Comp Physiol A 155:713–724

    Google Scholar 

  • Bass AH, Hopkins CD (1985) Hormonal control of sex differences in the electric organ discharge (EOD) of mormyrid fishes. J Comp Physiol A 156:587–604

    Google Scholar 

  • Bass AH, Volman SF (1985) Steroid-induced changes in action potential waveforms of an electric organ. Neurosci Abstr 11:159

    Google Scholar 

  • Bass A, Segil N, Kelley D (1984) A steroid sensitive electromotor pathway in mormyrid fish: electric organ morphology, androgen receptor biochemistry and steroid autoradiography. Neurosci Abstr 10:927

    Google Scholar 

  • Bastian J (1977) Variations in the frequency response of electroreceptors dependent on receptor location in weakly electric fish (Gymnotoidei) with a pulse discharge. J Comp Physiol 121:53–64

    Google Scholar 

  • Bennett MVL (1967) Mechanisms of electroreceptors. In: Cahn P (ed) Lateral line detectors. Univ Indiana Press, Bloomington, pp 313–393

    Google Scholar 

  • Bennett MVL (1971) Electric organs. In: Hoar WS, Randall LDJ (eds) Fish physiology, vol 2. Academic Press, New York, pp 347–491

    Google Scholar 

  • Ellis MM (1913) The gymnotid eels of tropical America. Mem Carnegie Museum 6:109–204

    Google Scholar 

  • Enger PS, Szabo T (1968) Effects of temperature on discharge rate of the electric organ of some gymnotoids. Comp Biochem Physiol 27:625–627

    Google Scholar 

  • Fettiplace R, Crawford AC (1978) The coding of sound pressure and frequency in cochlear hair cells of the terrapin. Proc R Soc London B 203:209–218

    Google Scholar 

  • Fostier A, Jalabert B, Billard R, Breton B, Zohar Y (1983) The gonadal steroids. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol IXa. Academic Press, New York, pp 277–372

    Google Scholar 

  • Hagedorn M, Carr CE (1985) Single electrocytes produce a sexually dimorphic signal in South American electric fish,Hypopomus occidentalis (Gymnotiformes, Hypopomidae). J Comp Physiol A 156:511–523

    Google Scholar 

  • Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33:254–265

    Google Scholar 

  • Hopkins CD (1972) Sex differences in electric signalling in an electric fish. Science 176:1035–1037

    Google Scholar 

  • Hopkins CD (1976) Stimulus filtering and electroreceptors in three species of gymnotoid fish. J Comp Physiol 111:171–207

    Google Scholar 

  • Hopkins CD (1980) Evolution of electric communication channels of mormyrids. Behav Ecol Sociobiol 7:1–13

    Google Scholar 

  • Idler DR, Truscott B (1972) Corticosteroids in fish. In: Idler DR (ed) Steroids in nonmammalian vertebrates. Academic Press, New York, pp 127–252

    Google Scholar 

  • Kirschbaum F (1983) Myogenic electric organ precedes the neurogenic organ in apteronotid fish. Naturwissenschaften 70:205

    Google Scholar 

  • Koch C (1984) Cable theory in neurons with active linearized membranes. Biol Cybern 50:15–23

    Google Scholar 

  • Lewis RS, Hudspeth AJ (1983a) Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature 304:538–541

    Google Scholar 

  • Lewis RS, Hudspeth AJ (1983b) Frequency tuning and ionic conductances in hair cells of the bullfrog's sacculus. In: Klinke R, Hartman R (eds) Hearing — Physiological bases and psychophysics. Springer, Berlin Heidelberg New York Tokyo, pp 17–24

    Google Scholar 

  • McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303–1311

    Google Scholar 

  • Meyer JH (1983) Steroid influences upon the discharge frequencies of weakly electric fish. J Comp Physiol 153:29–37

    Google Scholar 

  • Meyer JH (1984) Steroid influences upon discharge frequencies of intact and isolated pacemakers of weakly electric fish. J Comp Physiol A 154:659–668

    Google Scholar 

  • Meyer JH, Zakon HH (1982) Androgens alter the tuning of electroreceptors. Science 217:635–637

    Google Scholar 

  • 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 154:625–631

    Google Scholar 

  • Pfaff DW, McEwen BS (1983) Actions of estrogens and progestins on nerve cells. Science 219:808–814

    Google Scholar 

  • Szabo T (1974) Anatomy of the specialized lateral line organs of electroreception. In: Fessard AE (ed) Electroreceptors and other spezialized receptors in lower vertebrates (Handbook of sensory physiology, vol III/3). Springer, Berlin Heidelberg New York, pp 13–58

    Google Scholar 

  • Viancour T (1979) Electroreceptors of weakly electric fish. II. Individually tuned receptor oscillations. J Comp Physiol 133:327–338

    Google Scholar 

  • Watson D, Bastian J (1979) Frequency response characteristics of electroreceptors in the weakly electric fish,Gymnotus carapo. J Comp Physiol 134:191–202

    Google Scholar 

  • Westby GWM, Kirschbaum F (1981) Sex differences in the electric organ discharge ofEigenmannia virescens and the effect of gonadal maturation. In: Szabo T, Gzeh G (eds) Sensory physiology of lower aquatic vertebrates. Pergammon Press, Oxford, pp 179–194

    Google Scholar 

  • Westby GWM, Kirschbaum F (1982) Sex differences in the waveform of the pulse-type electric fish,Pollimyrus isidori (Mormyridae). J Comp Physiol 145:39–403

    Google Scholar 

  • Wingfield JC, Farner D (1975) The determination of five steroids in avian plasma by radioimmunoassay and competitive protein binding. Steroid 26:311–327

    Google Scholar 

  • Yialamas D, Zakon HH (1984) Tuning of newly generated electroreceptors. Neurosci Abstr 10:193

    Google Scholar 

  • Zakon HH (1984a) Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age. J Comp Neurol 228:557–570

    Google Scholar 

  • Zakon HH (1984b) The ionic basis of the oscillatory receptor potential of tuberous electroreceptors inSternopygus. Neurosci Abstr 10:193

    Google Scholar 

  • Zakon HH, Meyer JH (1983) Plasticity of electroreceptor tuning in the weakly electric fish,Sternopygus dariensis. J Comp Physiol 153:477–487

    Google Scholar 

  • Zipser B, Bennett MVL (1973) Tetrodotoxin resistant electrically excitable responses of receptor cells. Brain Res 62:253–259

    Google Scholar 

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Authors and Affiliations

  1. Scripps Institution of Oceanography, U.C.S.D.A-002, 92093, La Jolla, California, USA

    Clifford H. Keller

  2. Department of Zoology, University of Texas, 78712, Austin, Texas, USA

    Harold H. Zakon & Dorothea Yialamas Sanchez

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  1. Clifford H. Keller
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  2. Harold H. Zakon
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  3. Dorothea Yialamas Sanchez
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Keller, C.H., Zakon, H.H. & Sanchez, D.Y. Evidence for a direct effect of androgens upon electroreceptor tuning. J. Comp. Physiol. 158, 301–310 (1986). https://doi.org/10.1007/BF00603614

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  • DOI: https://doi.org/10.1007/BF00603614

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