Abstract
Vocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. The ability to exchange vocalizations in an alternating fashion is also exhibited by other species, including zebra finches. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. Within this circuit, local inhibition precedes premotor neuron activation associated with calling. Blocking inhibition results in faster vocal responses as well as an impaired ability to flexibly avoid overlapping with a partner. These results support a working model in which premotor inhibition regulates context-dependent timing of vocalizations and enables the precise interleaving of vocal signals during turn-taking.
Highlights
Vocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown
To characterize how zebra finches adjust their vocalizations during interactions, we set up a game of chicken—that is to say, a situation with a high potential for temporal conflict in which two birds are likely to call simultaneously
In this study, we examined the neural mechanisms underlying vocal turn-taking in zebra finches and determined that inhibition in the cortical premotor nucleus HVC provides a critical mechanism for regulating interactive vocal timing
Summary
Vocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. 1234567890():,; Spoken conversations often consist of rapid exchanges of vocalizations that are timed to minimize overlapping elements[1] This form of vocal turn-taking involves the ability to precisely control the onsets of utterances and coordinate gaps. To further explore the contribution of single neurons to the generation of calls we carry out intracellular recordings of identified premotor neurons and inhibitory interneurons in HVC during vocal interactions Both cell types display activity at the onset of call production, on average inhibition occurs before excitation. These results support a working model in which inhibition regulates the initiation of vocal production during coordinated interactions
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