The development of highly complex vocal skill, like human language and bird songs, is underlain by learning. Vocal learning, even when occurring in adulthood, is thought to largely depend on a sensitive/critical period during postnatal development, and learned vocal patterns emerge gradually as the long-term consequence of vocal practice during this critical period. In this scenario, it is presumed that the effect of vocal practice is thus mainly limited by the intrinsic timing of age-dependent maturation factors that close the critical period and reduce neural plasticity. However, an alternative, as-yet untested hypothesis is that vocal practice itself, independently of age, regulates vocal learning plasticity. Here, we explicitly discriminate between the influences of age and vocal practice using a songbird model system. We prevented zebra finches from singing during the critical period of sensorimotor learning by reversible postural manipulation. This enabled to us to separate lifelong vocal experience from the effects of age. The singing-prevented birds produced juvenile-like immature song and retained sufficient ability to acquire a tutored song even at adulthood when allowed to sing freely. Genome-wide gene expression network analysis revealed that this adult vocal plasticity was accompanied by an intense induction of singing activity-dependent genes, similar to that observed in juvenile birds, rather than of age-dependent genes. The transcriptional changes of activity-dependent genes occurred in the vocal motor robust nucleus of the arcopallium (RA) projection neurons that play a critical role in the production of song phonology. These gene expression changes were accompanied by neuroanatomical changes: dendritic spine pruning in RA projection neurons. These results show that self-motivated practice itself changes the expression dynamics of activity-dependent genes associated with vocal learning plasticity and that this process is not tightly linked to age-dependent maturational factors. Author summary How is plasticity associated with vocal learning regulated during a critical period? Although there are abundant studies on the critical period in sensory systems, which are passively regulated by the external environment, few studies have manipulated the sensorimotor experience through the entire critical period. Thus, it is a commonly held belief that age or intrinsic maturation is a crucial factor for the closure of the critical period of vocal learning. Contrary to this idea, our study using songbirds provides a new insight that self-motivated vocal practice, not age, regulates vocal learning plasticity during the critical period. To examine the effects of vocal practice on vocal learning, we prevented juvenile zebra finches from singing during the critical period by postural manipulation, which separated the contribution of lifelong vocal experience from that of age. When these birds were allowed to freely sing as adults, they generated highly plastic songs and maintained the ability to mimic tutored songs, as normal juveniles did. Genome-wide transcriptome analysis revealed that both juveniles and singing-prevented adults, but not normally reared adults, expressed a similar set of singing-dependent genes in a song nucleus in the brain that regulates syllable acoustics. However, age-dependent genes were still similarly expressed in both singing-prevented and normally reared adult birds. These results exhibit that vocal learning plasticity is actively controlled by self-motivated vocal practice.
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