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The Journal of Neuroscience, June 1, 2003, 23(11):4717-4725

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Corollary Discharge Inhibition of Ascending Auditory Neurons in the Stridulating Cricket

James F. A. Poulet and Berthold Hedwig

Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom

Acoustically communicating animals are able to process external acoustic stimuli despite generating intense sounds during vocalization. We have examined how the crickets' ascending auditory pathway copes with self-generated, intense auditory signals (chirps) during singing (stridulation). We made intracellular recordings from two identified ascending auditory interneurons, ascending neuron 1 (AN1) and ascending neuron 2 (AN2), during pharmacologically elicited sonorous (two-winged), silent (one-winged), and fictive (isolated CNS) stridulation.

During sonorous chirps, AN1 responded with bursts of spikes, whereas AN2 was inhibited and rarely spiked. Low-amplitude hyperpolarizing potentials were recorded in AN1 and AN2 during silent chirps. The potentials were also present during fictive chirps. Therefore, they were the result of a centrally generated corollary discharge from the stridulatory motor network. The spiking response of AN1 and AN2 to acoustic stimuli was inhibited during silent and fictive chirps. The maximum period of inhibition occurred in phase with the maximum spiking response to self-generated sound in a sonorously stridulating cricket. In some experiments (30%) depolarizing potentials were recorded during silent chirps. Reafferent feedback elicited by wing movement was probably responsible for the depolarizing potentials.

In addition, two other sources of inhibition were present in AN1: (1) IPSPs were elicited by stimulation with 12.5 kHz stimuli and (2) a long-lasting hyperpolarization followed spiking responses to 4.5 kHz stimuli. The hyperpolarization desensitized the response of AN1 to subsequent quieter stimuli. Therefore, the corollary discharge will reduce desensitization by suppressing the response of AN1 to self-generated sounds.

Key words: corollary discharge; efference copy; stridulation; presynaptic inhibition; postsynaptic inhibition; ascending neuron 1; ascending neuron 2

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Received Dec. 6, 2002; revised Feb. 3, 2003; accepted Feb. 21, 2003.

This article has been cited by other articles:

				H. M. ter Hofstede and J. H. Fullard The neuroethology of song cessation in response to gleaning bat calls in two species of katydids, Neoconocephalus ensiger and Amblycorypha oblongifolia J. Exp. Biol., August 1, 2008; 211(15): 2431 - 2441. [Abstract] [Full Text] [PDF]

				J. F. A. Poulet and B. Hedwig The Cellular Basis of a Corollary Discharge Science, January 27, 2006; 311(5760): 518 - 522. [Abstract] [Full Text] [PDF]

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