Abstract
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.
Original language | English (US) |
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Pages (from-to) | e2006537 |
Journal | PLOS Biology |
Volume | 16 |
Issue number | 9 |
DOIs | |
State | Published - Sep 12 2018 |
Bibliographical note
KAUST Repository Item: Exported on 2020-10-01Acknowledgements: JSPS DC fellowship https://www.jsps.go.jp/english/e-grants/ (grant number JP26001737). to SH. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. JSPS KAKENHI https://www.jsps.go.jp/english/e-grants/ (grant number JP25290063, JP23115701, JP16H01261, JP17H05932, JP17H06380, JP17K19629, and JP18H02520). to KW. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. MEXT KAKENHI (grant number 221S0002). for RNA-seq experiments. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. MEXT Platform Project for Supporting in Drug Discovery and Life Science Research (grant number PDIS0030). for RNA-seq experiments. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.