Transient sensorimotor projections in the developmental song learning period

Memory recall and guidance are essential for motor skill acquisition. Like humans learning to speak, male zebra finches learn to sing by first memorizing and then matching their vocalization to the tutor’s song (TS) during specific developmental periods. Yet, the neuroanatomical substrate supporting auditory-memory-guided sensorimotor learning has remained elusive. Here, using a whole-brain connectome analysis with activity-dependent viral expression, we identified a transient projection into the motor region, HVC, from neuronal ensembles responding to TS in the auditory forebrain, the caudomedial nidopallium (NCM), in juveniles. Virally induced cell death of the juvenile, but not adult, TS-responsive NCM neurons impaired song learning. Moreover, isolation, which delays closure of the sensory, but not the motor, learning period, did not affect the decrease of projections into the HVC from the NCM TS-responsive neurons after the song learning period. Taken together, our results suggest that dynamic axonal pruning may regulate timely auditory-memory-guided vocal learning during development. [Display omitted] •Specific manipulation of song-responsive neurons with a cFos-TetON system is created•Ablating tutor’s song (TS)-responsive neurons prevents juveniles from song learning•TS-responsive neurons transiently project to song premotor area, HVC, in juveniles•Sensory isolation does not delay song crystallization or axon pruning in HVC Auditory memory guidance for motor shaping is necessary for vocal learning. Here, Louder et al. show transient axonal projections to the song premotor area from the neurons responsive to the tutor’s song (TS) playback in the auditory forebrain. Ablating TS-responsive neurons disrupts song learning in juveniles but not in adults.