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

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.