A mesocortical dopamine circuit enables the cultural transmission of vocal behavior

Abstract

The cultural transmission of behavior depends on a pupil’s ability to identify and emulate an appropriate tutor ^{1– 4} . How the pupil’s brain detects a suitable tutor and encodes the tutor’s behavior is largely unknown. Juvenile zebra finches readily copy songs of adult tutors they interact with, but not songs they listen to passively through a speaker ^{5, 6} , indicating that social cues generated by the tutor facilitate song imitation. Here we show that neurons in the midbrain periaqueductal gray (PAG) of juvenile finches are selectively excited by a singing tutor and, by releasing dopamine (DA) in a sensorimotor cortical analogue (HVC), help encode tutor song representations used for vocal copying. Blocking DA signaling in the pupil’s HVC during tutoring blocked copying, whereas pairing stimulation of PAG terminals in HVC with song played through a speaker was sufficient to drive copying. Exposure to a singing tutor triggered the rapid emergence of responses to the tutor song in the pupil’s HVC and a rapid increase in the pupil’s song complexity, an early signature of song copying ^{7, 8} . These findings reveal that a dopaminergic mesocortical circuit detects a tutor’s presence and helps encode the tutor’s performance, facilitating the cultural transmission of vocal behavior.