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A corollary discharge maintains auditory sensitivity during sound production

Nature volume 418, pages 872–876 (2002)Cite this article

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.

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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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  1. Department of Zoology, University of Cambridge, Downing Street, CB2 3EJ, Cambridge, UK

    James F. A. Poulet & Berthold Hedwig

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  1. James F. A. Poulet
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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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