Feed-forward inhibition fine-tunes response timing in auditory-vocal interactions

Abstract

The ability to regulate vocal timing is a fundamental aspect of communicative interactions for many species, including conversational speech among humans, yet little is known about the neural circuitry that regulates the input-dependent timing of vocal replies. Exploring this topic in the zebra finch premotor area HVC, we identify feed-forward inhibition as a key regulator of vocal response timing. Based on a spiking network model informed by behavioral and electrophysiological data from communicating zebra finches, we predicted that two different patterns of inhibition regulate vocal-motor responses. In one scenario, the strength of production-related premotor inhibition translates into plasticity in vocal response delays. In the other scenario, fast transient interneuron activity in response to auditory input results in the suppression of call production while a call is heard, thereby reducing acoustic overlap between callers. Extracellular recordings in HVC during the listening phase confirm the presence of auditory-evoked response patterns in putative inhibitory interneurons, along with corresponding signatures of auditory-evoked activity suppression. The proposed model provides a parsimonious framework to explain how auditory-vocal transformations can give rise to vocal turn-taking and highlights multiple roles of local inhibition for behavioral modulation at different time scales.