An underlying motor bias shapes individuality during vocal learning

Abstract The emergence of individuality during learned behavior is a general feature of animal species, yet the biological bases of its development remain unknown. Similar to human speech, songbirds develop individually-unique songs with species-specific traits through vocal learning. By taking advantage of songbirds as a model system for studying the neural basis of vocal learning and development, we utilized F1 hybrid songbirds (Taeniopygia guttata cross with T. bichenovii) to examine the developmental and molecular mechanisms underlying individuality in vocal learning. When tutoring with songs from both parental species, F1 pupils showed vast individual differences in their acquired songs. Approximately 30% of F1 hybrids selectively learned either song of the two parental species, whereas others developed merged songs between the parental species. Vocal acoustic biases during vocal babbling were initially observed as individual differences in songs among F1 juveniles, which were maintained through the sensitive period of song vocal learning. These individual differences in vocal acoustic biases appeared independently from the auditory experience of hearing biological farther’s and passive tutored songs. Furthermore, the idiosyncratic traits of F1 hybrids’ songs were not correlated with peripheral vocal organ morphology. However, we identified unique transcriptional signatures from the glutamatergic neurons projecting from the cortical vocal output nucleus to the hypoglossal nuclei associated with individual differences in the acoustic vocal biases, even at the initial stage of vocal learning. These results indicate that a predisposed motor bias influences the individuality observed when learning new motor skills.