Sleep replay reveals premotor circuit structure for a skilled behavior

Abstract

Neural circuits often exhibit sequences of activity, but the contribution of local networks to their generation remains unclear. In the zebra finch, song-related premotor sequences within HVC may result from some combination of local connectivity and long-range thalamic inputs from nucleus uvaeformis (Uva). Because lesions to either structure abolish song, we examine "sleep replay" using high-density recording methods to reconstruct precise song-related events. Replay activity persists after the upstream nucleus interfacialis of the nidopallium is lesioned and slows when HVC is cooled, demonstrating that HVC provides temporal structure for these events. To further gauge the importance of intra-HVC connectivity for shaping network dynamics, we lesion Uva during sleep and find that residual replay sequences could span syllable boundaries, supporting a model in which HVC can propagate sequences throughout the duration of the song. Our results highlight the power of studying offline activity to investigate behaviorally relevant circuit organization.