A Corollary Discharge Mechanism Modulates Central Auditory Processing in Singing Crickets

Abstract

Crickets communicate using loud (100 dB SPL) sound signals that could adversely affect their own auditory system. To examine how they cope with this self-generated acoustic stimulation, intracellular recordings were made from auditory afferent neurons and an identified auditory interneuron—the Omega 1 neuron (ON1)—during pharmacologically elicited singing (stridulation). During sonorous stridulation, the auditory afferents and ON1 responded with bursts of spikes to the crickets' own song. When the crickets were stridulating silently, after one wing had been removed, only a few spikes were recorded in the afferents and ON1. Primary afferent depolarizations (PADs) occurred in the terminals of the auditory afferents, and inhibitory postsynaptic potentials (IPSPs) were apparent in ON1. The PADs and IPSPs were composed of many summed, small-amplitude potentials that occurred at a rate of about 230 Hz. The PADs and the IPSPs started during the closing wing movement and peaked in amplitude during the subsequent opening wing movement. As a consequence, during silent stridulation, ON1's response to acoustic stimuli was maximally inhibited during wing opening. Inhibition coincides with the time when ON1 would otherwise be most strongly excited by self-generated sounds in a sonorously stridulating cricket. The PADs and the IPSPs persisted in fictively stridulating crickets whose ventral nerve cord had been isolated from muscles and sense organs. This strongly suggests that the inhibition of the auditory pathway is the result of a corollary discharge from the stridulation motor network. The central inhibition was mimicked by hyperpolarizing current injection into ON1 while it was responding to a 100 dB SPL sound pulse. This suppressed its spiking response to the acoustic stimulus and maintained its response to subsequent, quieter stimuli. The corollary discharge therefore prevents auditory desensitization in stridulating crickets and allows the animals to respond to external acoustic signals during the production of calling song.