Neural Dynamics in the Basal Ganglia Underlying Birdsong Practice and Performance

Abstract

Skilled movements are typically more variable during practice, promoting exploration, yet highly stereotyped during performance, favoring exploitation. How neurons encode and dynamically regulate motor variability across practice and performance states remains unknown. Songbirds sing more variable songs when practicing alone and highly stereotyped songs when performing to a female, providing a powerful system to explore how neural ensembles regulate motor variability. Here, I used this system to identify neural mechanisms underlying practice and performance. First, I used deep brain imaging techniques to demonstrate that spiny neurons (SNs) in the basal ganglia (BG) encode vocal variability during solo practice, and that SN activity is strongly suppressed to enable stereotyped song performance towards a female. Second, I showed that optogenetically inhibiting SNs reduces pitch variability to female-directed levels. Third, I collaborated with Dr. John Pearson’s lab to uncover a coding scheme whereby specific patterns of SN activity map onto distinct spectral variants of syllables during vocal practice. Lastly, I use photometry, anatomical tracing, molecular profiling, and ex vivo physiology to establish that adrenergic signaling in the BG regulates vocal variability by directly suppressing SN activity. I conclude that SN ensembles encode and drive vocal exploration during practice, and the social context-dependent noradrenergic regulation of SN activity enables stereotyped and highly precise vocal performance.