Social familiarity strengthens neural and vocal responses to conspecific calls in zebra finches.

Abstract

Across animals, dyadic vocal interactions often occur within complex acoustic environments containing numerous signalers. The influence of socially relevant acoustic signals on the neural circuits controlling interactive vocal behavior remains poorly understood. We examined this issue in zebra finches, highly social songbirds that maintain nearly continuous vocal contact through the exchange of short innate calls. We developed a behavioral paradigm that elicits differential responses to familiar and unfamiliar vocal partners, enabling the prediction of social context based on individual birds' response patterns. We then used high-density Neuropixels probes to record neural activity within a vocal premotor nucleus in the songbird forebrain, while birds listened to familiar and unfamiliar contact calls. We found that the activity of putative projection neurons and interneurons in this vocal premotor nucleus was modulated by the familiarity of heard calls, with interneurons exhibiting stronger responses to familiar calls. Furthermore, we found that measures of vocal responsiveness correlated with neural response parameters during listening. Specifically, we observed that increased vocal response rates, rapidity, and temporal consistency for familiar call playbacks were correlated with elevated mean and peak firing rates, as well as prolonged activity, in HVC interneurons. These results demonstrate how socially salient auditory information can affect a forebrain premotor circuit to maintain the specificity of vocal interactions within complex and dynamic social environments.