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A corollary discharge maintains auditory sensitivity during sound production

Abstract

Speaking and singing present the auditory system of the caller with two fundamental problems: discriminating between self-generated and external auditory signals and preventing desensitization. In humans1 and many other vertebrates2,3,4,5,6,7, auditory neurons in the brain are inhibited during vocalization but little is known about the nature of the inhibition. Here we show, using intracellular recordings of auditory neurons in the singing cricket, that presynaptic inhibition of auditory afferents and postsynaptic inhibition of an identified auditory interneuron occur in phase with the song pattern. Presynaptic and postsynaptic inhibition persist in a fictively singing, isolated cricket central nervous system and are therefore the result of a corollary discharge from the singing motor network. Mimicking inhibition in the interneuron by injecting hyperpolarizing current suppresses its spiking response to a 100-dB sound pressure level (SPL) acoustic stimulus and maintains its response to subsequent, quieter stimuli. Inhibition by the corollary discharge reduces the neural response to self-generated sound and protects the cricket's auditory pathway from self-induced desensitization.

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Figure 1: Responses of ON1 during singing.
Figure 2: Presynaptic inhibition of auditory afferents during singing.
Figure 3: Testing the efficacy of inhibition during silent singing.
Figure 4: Inhibition of ON1 during acoustic stimulation prevents subsequent desensitization.

References

  1. Creutzfeldt, O., Ojemann, G. & Lettich, E. Neuronal activity in the human temporal lobe II. Responses to the subjects own voice. Exp. Brain Res. 77, 476–489 (1989)

    Article  CAS  Google Scholar 

  2. Suga, N. & Schlegel, P. Neural attenuation of responses to emitted sounds in echolocating bats. Science 177, 82–84 (1972)

    Article  ADS  CAS  Google Scholar 

  3. Suga, N. & Shimozawa, T. Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science 183, 1211–1213 (1974)

    Article  ADS  CAS  Google Scholar 

  4. Schuller, G. Vocalization influences auditory processing in collicular neurons of the CF-FM bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 132, 39–46 (1979)

    Article  Google Scholar 

  5. McCasland, J. S. & Konishi, M. Interaction between auditory and motor activities in an avian song control nucleus. Proc. Natl Acad. Sci. USA 78, 7815–7819 (1981)

    Article  ADS  CAS  Google Scholar 

  6. Müller-Preuss, P. & Ploog, D. Inhibition of auditory cortical neurons during phonation. Brain Res. 215, 61–76 (1981)

    Article  Google Scholar 

  7. Metzner, W. A possible neuronal basis for Doppler-shift compensation in echo-locating horseshoe bats. Nature 341, 529–532 (1989)

    Article  ADS  CAS  Google Scholar 

  8. Nocke, H. Physiological aspects of sound communication in crickets (Gryllus campestris L.). J. Comp. Physiol. A 80, 141–162 (1972)

    Article  Google Scholar 

  9. Michel, K. Das Tympanalorgan von Gryllus bimaculatus DeGeer (Saltatoria, Gryllidae). Z. Morph. Tiere 77, 285–315 (1974)

    Article  Google Scholar 

  10. Schildberger, K., Wohlers, D. W. & Huber, F. in Cricket Behaviour and Neurobiology (eds Huber, F., Moore, T. E. & Loher, T. E.) 423–458 (Cornell Univ. Press, Ithaca/London, 1989)

    Google Scholar 

  11. Jones, M. D. R. & Dambach, M. Response to sound in crickets without tympanal organs (Gryllus campestris L.). J. Comp. Physiol. A 87, 89–98 (1973)

    Article  Google Scholar 

  12. Suga, N. & Jen, P. Peripheral control of acoustic signals in the auditory system of echolocating bats. J. Exp. Biol. 62, 277–311 (1975)

    CAS  PubMed  Google Scholar 

  13. Borg, E. & Counter, S. The middle-ear muscles. Sci. Am. 261 (August), 62–68 (1989)

    Google Scholar 

  14. Narins, P. M. Reduction of tympanic membrane displacement during vocalization of the arboreal tree frog, Eleutherodactylus coqui. J. Acoust. Soc. Am. 91, 3551–3557 (1992)

    Article  ADS  CAS  Google Scholar 

  15. Hennig, R. M. et al. Auditory threshold change in singing cicadas. J. Exp. Biol. 187, 45–55 (1994)

    CAS  PubMed  Google Scholar 

  16. Poulet, J. F. A. & Hedwig, B. Tympanic membrane oscillations and auditory receptor activity in the stridulating cricket Gryllus bimaculatus. J. Exp. Biol. 204, 1281–1293 (2001)

    CAS  PubMed  Google Scholar 

  17. Clarac, F. & Cattaert, D. Invertebrate presynaptic inhibition and motor control. Exp. Brain Res. 112, 163–180 (1996)

    Article  CAS  Google Scholar 

  18. Hardt, M. & Watson, A. H. D. Distribution of input and output synapses on the central branches of bushcricket and cricket auditory afferent neurones: immunocytochemical evidence for GABA and glutamate in different populations of presynaptic boutons. J. Comp. Neurol. 403, 281–294 (1999)

    Article  CAS  Google Scholar 

  19. Pollack, G. S. Selective attention in an insect auditory neuron. J. Neurosci. 8, 2635–2639 (1988)

    Article  CAS  Google Scholar 

  20. Sobel, E. C. & Tank, D. W. In vivo Ca2+ dynamics in a cricket auditory neuron: an example of chemical computation. Science 263, 823–826 (1994)

    Article  ADS  CAS  Google Scholar 

  21. Givois, V. & Pollack, G. S. Sensory habituation of auditory receptor neurons: implications for sound localization. J. Exp. Biol. 203, 2529–2537 (2000)

    CAS  PubMed  Google Scholar 

  22. von Holst, E. & Mittelstaedt, H. Das reafferenzprinzip. (Wechselwirkungen zwischen zentralnervensystem und peripherie.). Naturwissenschaften 37, 464–476 (1950)

    Article  ADS  Google Scholar 

  23. Sperry, R. W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psych. 43, 482–489 (1950)

    Article  CAS  Google Scholar 

  24. Zaretsky, M. & Rowell, C. H. F. Saccadic suppression by corollary discharge in the locust. Nature 280, 583–585 (1979)

    Article  ADS  CAS  Google Scholar 

  25. Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981)

    Article  ADS  CAS  Google Scholar 

  26. Guthrie, B. L., Porter, J. D. & Sparks, D. L. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221, 1193–1195 (1983)

    Article  ADS  CAS  Google Scholar 

  27. Sillar, K. T. & Roberts, A. A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331, 262–265 (1988)

    Article  ADS  CAS  Google Scholar 

  28. Bell, C. C. in Comparative Physiology of Sensory Systems (eds Bolis, L., Keynes, R. D. & Maddrell, S. H. P.) 636–647 (Cambridge Univ. Press, Cambridge, 1984)

    Google Scholar 

  29. Hedwig, B. Control of cricket stridulation by a command neuron: efficacy depends on the behavioural state. J. Neurophysiol. 83, 712–722 (2000)

    Article  CAS  Google Scholar 

  30. Knepper, M. & Hedwig, B. NEUROLAB, a PC-program for the processing of neurobiological data. Comp. Methods Programs Biomed. 52, 75–77 (1997)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Burrows, T. Matheson and S. Rogers for comments on the manuscript. This work was supported by a Biotechnology and Biological Sciences Research Council (BBSRC) studentship and grants from the Wellcome Trust and the Royal Society.

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Correspondence to James F. A. Poulet.

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Poulet, J., Hedwig, B. A corollary discharge maintains auditory sensitivity during sound production. Nature 418, 872–876 (2002). https://doi.org/10.1038/nature00919

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