Sleep and sensorimotor integration during early vocal learning in a songbird

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Abstract
Behavioural studies show that sleep plays a role in learning, and birdsong is a well established model system for the study of learning. It has been proposed that forebrain premotor neuron activity in sleeping adult zebra finches reflects daytime singing episodes. Now Sylvan Shank and Daniel Margoliash demonstrate a surprising role for sleep in establishing the organization of the songbird's brain at the time the bird first starts to learn to sing. In juvenile zebra finches yet to master their song, exposure to an adult 'tutor' song produced profound changes in the premotor neuronal activity during the subsequent sleep session. These changes in night-time activity are echoed in tutor-song-induced changes in singing the next day. In sleeping adult zebra finches, forebrain premotor neuron activity is proposed to reflect daytime singing episodes. This study shows that in juvenile songbirds yet to master their song, auditory exposure to an adult 'tutor' song produced profound changes in the premotor neuronal activity during the subsequent sleep session. These changes in night time activity preceded and reflected tutor-song induced changes in singing the next day. Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours1,2,3,4. During sleep, brain regions are reactivated5,6, and specific patterns of neural activity are replayed7,8,9,10, consistent with patterns observed in previous waking behaviour. Birdsong learning is a paradigmatic model system for skill learning11,12,13,14. 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 day15. In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurons 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 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.