Motor circuits are required to encode a sensory model for imitative learning

Summary Premotor circuits help generate complex behaviors, including those learned by imitation. Premotor circuits also can be activated during observation of another animal’s behavior, leading to speculation that they also participate in sensory learning important to imitation. Here we tested this idea by focally manipulating the brain activity of juvenile zebra finches, which learn to sing by memorizing and vocally copying the song of an adult tutor. Tutor song-contingent optogenetic or electrical disruption of neural activity in the pupil’s song premotor nucleus HVC prevented song copying, indicating that a premotor structure important to the temporal control of birdsong also helps encode the tutor song. In vivo multiphoton imaging and neural manipulations delineated a pathway and candidate synaptic mechanism through which tutor song information is encoded by premotor circuits. These findings provide evidence that premotor circuits help to encode sensory information about the behavioral model prior to shaping and executing imitative behaviors. The cultural transmission of behavior involves observation of a behavioral model followed by imitation of the observed behavior. How the brain encodes the formative sensory experience provided by the behavioral model remains poorly understood. Although sensory structures are undoubtedly activated during observation of the model, premotor structures that play a role in generating imitative behaviors also can be activated during observation of another animal’s behavior 1–5 . This has led to speculation that premotor circuits may also help to encode sensory information about the model that is important to subsequent behavioral imitation 6–9 . Birdsong is a culturally transmitted vocal behavior with strong parallels to human speech learning, including obligatory auditory experience of a vocal model during a juvenile sensitive period followed by a phase of vocal copying 10–13 . Juvenile male zebra finches first listen to and memorize the song of an adult male tutor during a sensory learning phase (Fig. 1a; ~30–60 days post-hatching (dph)), then engage in vocal practice to emulate this memorized song model during a partially overlapping and more