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Research ArticleConfirmation, Cognition and Behavior

Beyond Critical Period Learning: Striatal FoxP2 Affects the Active Maintenance of Learned Vocalizations in Adulthood

Nancy F. Day, Taylor G. Hobbs, Jonathan B. Heston and Stephanie A. White
eNeuro 22 March 2019, 6 (2) ENEURO.0071-19.2019; DOI: https://doi.org/10.1523/ENEURO.0071-19.2019
Nancy F. Day
Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA 90095
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Taylor G. Hobbs
Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA 90095
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Jonathan B. Heston
Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA 90095
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Stephanie A. White
Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA 90095
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Abstract

In humans, mutations in the transcription factor forkhead box P2 (FOXP2) result in language disorders associated with altered striatal structure. Like speech, birdsong is learned through social interactions during maturational critical periods, and it relies on auditory feedback during initial learning and on-going maintenance. Hearing loss causes learned vocalizations to deteriorate in adult humans and songbirds. In the adult songbird brain, most FoxP2-enriched regions (e.g., cortex, thalamus) show a static expression level, but in the striatal song control nucleus, area X, FoxP2 is regulated by singing and social context: when juveniles and adults sing alone, its levels drop, and songs are more variable. When males sing to females, FoxP2 levels remain high, and songs are relatively stable: this “on-line” regulation implicates FoxP2 in ongoing vocal processes, but its role in the auditory-based maintenance of learned vocalization has not been examined. To test this, we overexpressed FoxP2 in both hearing and deafened adult zebra finches and assessed effects on song sung alone versus songs directed to females. In intact birds singing alone, no changes were detected between songs of males expressing FoxP2 or a GFP construct in area X, consistent with the marked stability of mature song in this species. In contrast, songs of males overexpressing FoxP2 became more variable and were less preferable to females, unlike responses to songs of GFP-expressing control males. In deafened birds, song deteriorated more rapidly following FoxP2 overexpression relative to GFP controls. Together, these experiments suggest that behavior-driven FoxP2 expression and auditory feedback interact to precisely maintain learned vocalizations.

  • auditory feedback
  • basal ganglia
  • birdsong
  • sensorimotor
  • speech

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by National Institutes of Health Grants T32 HD07228 (to N.F.D.) and R01 MH070712 (to S.A.W.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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eneuro: 6 (2)
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March/April 2019
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Beyond Critical Period Learning: Striatal FoxP2 Affects the Active Maintenance of Learned Vocalizations in Adulthood
Nancy F. Day, Taylor G. Hobbs, Jonathan B. Heston, Stephanie A. White
eNeuro 22 March 2019, 6 (2) ENEURO.0071-19.2019; DOI: 10.1523/ENEURO.0071-19.2019

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Beyond Critical Period Learning: Striatal FoxP2 Affects the Active Maintenance of Learned Vocalizations in Adulthood
Nancy F. Day, Taylor G. Hobbs, Jonathan B. Heston, Stephanie A. White
eNeuro 22 March 2019, 6 (2) ENEURO.0071-19.2019; DOI: 10.1523/ENEURO.0071-19.2019
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Keywords

  • auditory feedback
  • basal ganglia
  • birdsong
  • sensorimotor
  • speech

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