Sleep and sensorimotor integration during early vocal learning in a songbird

Abstract

Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours1-4. During sleep, brain regions are reactivated5,6, and specific patterns of neural activity are replayed7-10, consistent with patterns observed in prior waking behaviour. Birdsong learning is a paradigmatic model system for skill learning11-14. Song development in juvenile zebra finches is characterised by sleep-dependent circadian fluctuations in singing behaviour, with immediate post-sleep deterioration in song structure followed by recovery later in the day15. In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurones in the robust nucleus of the arcopallium (RA) carries information about daytime singing16. Here we show that in juvenile zebra finches, playback during the day of an adult “tutor” song induced profound and tutor song-specific changes in bursting activity of RA neurones during the following night of sleep. The night-time neuronal changes preceded tutor song-induced changes in singing, first observed the following day. Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor song-specific neuronal remodelling. Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity proceeding the onset of practice associated with vocal learning. We hypothesise that night-time bursting induces adaptive changes in premotor networks during sleep as part of vocal learning. By this hypothesis, plastic changes are driven by replay of sensory information at night and evaluation of sensory feedback during the day, with the interaction between the two leading to complex circadian patterns such as are seen early in vocal development.