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

TL;DR

Zebra finches respond more strongly to familiar calls, and their brain activity shows stronger and longer responses to these calls, helping them communicate effectively in social groups.

Contribution

This study reveals how social familiarity modulates neural activity in a vocal premotor nucleus to enhance specific vocal responses in zebra finches.

Findings

HVC interneurons show stronger and more sustained responses to familiar calls compared to unfamiliar ones.

Vocal response rates and consistency correlate with elevated neural firing rates and prolonged activity in HVC interneurons.

Birds respond faster and more precisely to familiar calls, indicating a link between neural activity and behavioral output.

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.

Vocal interactions frequently occur in social groups where the ability to quickly identify and respond to specific individuals is crucial. Zebra finches, known for their highly social nature and vocal behavior, serve as an excellent model for exploring this process. In this study, we investigated how a vocal control region in the bird’s forebrain is affected by the vocalizations of a familiar partner versus an unfamiliar bird, and how this distinction influences the bird’s vocal responses. We designed a behavioral test in which zebra finches respond differently to familiar versus unfamiliar call playbacks. The birds responded faster, more often, and with greater timing precision to calls from known partners. To uncover the neural correlate of this effect, we recorded the activity of a premotor brain area called HVC as birds listened to playbacks of familiar and unfamiliar calls. We discovered that HVC neurons, particularly the inhibitory interneurons, showed stronger and more sustained responses to familiar calls. Furthermore, the intensity of these neural responses was a reliable predictor of how quickly and consistently the birds replied in the behavioral test. Our findings reveal how socially meaningful sounds can shape premotor activity to guide context-specific communication within dynamic social groups.

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