FoxP2 isoforms delineate spatiotemporal transcriptional networks for vocal learning in the zebra finch

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Cite as: eLife 2018;7:e30649 doi: 10.7554/eLife.30649

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Abstract

Human speech is one of the few examples of vocal learning among mammals yet ~half of avian species exhibit this ability. Its neurogenetic basis is largely unknown beyond a shared requirement for FoxP2 in both humans and zebra finches. We manipulated FoxP2 isoforms in Area X, a song-specific region of the avian striatopallidum analogous to human anterior striatum, during a critical period for song development. We delineate, for the first time, unique contributions of each isoform to vocal learning. Weighted gene coexpression network analysis of RNA-seq data revealed gene modules correlated to singing, learning, or vocal variability. Coexpression related to singing was found in juvenile and adult Area X whereas coexpression correlated to learning was unique to juveniles. The confluence of learning and singing coexpression in juvenile Area X may underscore molecular processes that drive vocal learning in young zebra finches and, by analogy, humans.

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Zachary Daniel Burkett

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

For correspondence
zburkett@ucla.edu

Competing interests
The authors declare that no competing interests exist.

0000-0002-5153-485X
Nancy F Day

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.
Todd Haswell Kimball

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.
Caitlin M Aamodt

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.
Jonathan B Heston

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.

0000-0001-7479-1122
Austin T Hilliard

Department of Biology, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Xinshu Xiao

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.
Stephanie A White

Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.

Funding

National Institutes of Health (RO1MH07012)

Stephanie A White

National Institutes of Health (5T32HD007228)

Zachary Daniel Burkett

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal use was in accordance with NIH guidelines for experiments involving vertebrate animals and approved by the University of California, Los Angeles Chancellor's Institutional Animal Care and Use Committee (IACUC) under protocol (#2001-54). All surgical procedures were performed under isoflurane anesthetic.

Reviewing Editor

Liqun Luo, Howard Hughes Medical Institute, Stanford University, United States

Publication history

Received: July 24, 2017
Accepted: January 22, 2018
Accepted Manuscript published: January 23, 2018 (version 1)
Version of Record published: February 26, 2018 (version 2)
Version of Record updated: March 9, 2018 (version 3)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.