Sleep and sensorimotor integration during early vocal learning in a songbird

Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours(1-4). During sleep, brain regions are reactivated(5,6), and specific patterns of neural activity are replayed(7-10), consistent with patterns observed in previous waking behaviour. Birdsong learning is a paradigmatic model system for skill learning(11-14). Song development in juvenile zebra finches (Taeniopygia guttata) is characterized by sleep-dependent circadian fluctuations in singing behaviour, with immediate post-sleep deterioration in song structure followed by recovery later in the day(15). In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurons in the robust nucleus of the arcopallium (RA) carries information about daytime singing(16). 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 neurons 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 preceding the onset of practice associated with vocal learning. We hypothesize that night-time bursting induces adaptive changes in premotor networks during sleep as part of vocal learning. By this hypothesis, adaptive changes driven by replay of sensory information at night and by evaluation of sensory feedback during the day interact to produce the complex circadian patterns seen early in vocal development.