Neural circuit for social authentication in song learning

Social interactions are essential when learning to communicate. In human speech and bird song, infants must acquire accurate vocalization patterns and learn to associate them with live tutors and not mimetic sources. However, the neural mechanism of social reality during vocal learning remains unknown. Here, we characterize a neural circuit for social authentication in support of accurate song learning in the zebra finch. We recorded neural activity in the attention/arousal state control center, the locus coeruleus (LC), of juvenile birds during song learning from a live adult tutor. LC activity increased with real, not artificial, social information during learning that enhanced the precision and robustness of the learned song. During live social song learning, LC activity regulated long-term song-selective neural responsiveness in an auditory memory region, the caudomedial nidopallium (NCM). In accord, optogenetic inhibition of LC presynaptic signaling in the NCM reduced NCM neuronal responsiveness to live tutor singing and impaired song learning. These results demonstrate that the LC-NCM neural circuit integrates sensory evidence of real social interactions, distinct from song acoustic features, to authenticate song learning. The findings suggest a general mechanism for validating social information in brain development.