EARLY SONG LEARNING EXPERIENCES REGULATE DEVELOPMENTAL DYNAMICS OF THE AUDITORY TO MOTOR CIRCUIT IN ZEBRA FINCHES

Like human infants learning to speak, juvenile songbirds learn to sing by memorizing and then matching their vocalizations to their tutor's song (TS) during development. We recently found that the projections from TS-responsive neurons in the zebra finch higher auditory area, the caudomedial nidopallium (NCM) to premotor song nucleus, HVC are dense during early sensorimotor period but become sparse in later sensorimotor period (Louder et al., 2024).
Here, we examined whether song experiences and their timing affect the time course of NCM-HVC projection dynamics. Juvenile zebra finches were instructed by the first tutor (T1), and then by the second tutor (T2) after an isolation period. These sequentially tutored zebra finches learned songs from T2 beyond the normal learning period and produced less stable songs at the end of the typical sensorimotor period. Using activity-dependent viral labeling (AAV9-cFos-TetON-EGFP and AA9-cFos-TetOFF-mRFP), we visualized the NCM neurons responsive to each tutor song. Projections from T2-responsive NCM neurons appeared in the HVC within 12 hours after encountering T2. Strikingly, in adulthood, when NCM-HVC projections are normally sparse, projections from both the T1- and T2-responsive NCM neurons retained in the birds that learned from two tutors sequentially.
Preliminary results of electrophysiological recordings from the NCM neurons in the juveniles learning from T2 further suggest that the exposure to T2 modulates the NCM neuronal circuits and neuronal responsiveness established by learning from T1.
Together, these findings suggest that early song learning experiences and their timing shape auditory-motor neuronal circuits and learning time course.