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