A neural circuit mechanism for regulating vocal variability during song learning in zebra finches

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Abstract

Motor skill learning is characterized by improved performance and reduced motor variability. The neural mechanisms that couple skill level and variability, however, are not known. The zebra finch, a songbird, presents a unique opportunity to address this question because production of learned song and induction of vocal variability are instantiated in separate circuits that converge on a motor cortex analogue controlling vocal output. To probe the interplay between learning and variability, we made intracellular recordings from neurons in this area, characterizing how their inputs from the functionally distinct pathways change throughout song development. We found that inputs that drive stereotyped song-patterns are strengthened and pruned, while inputs that induce variability remain unchanged. A simple network model showed that strengthening and pruning of action-specific connections reduces the sensitivity of motor control circuits to variable input and neural 'noise'. This identifies a simple and general mechanism for learning-related regulation of motor variability.

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Jonathan Garst-Orozco

Center for Brain Science, Harvard University, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.
Baktash Babadi

Center for Brain Science, Harvard University, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.
Bence P Ölveczky

Center for Brain Science, Harvard University, Cambridge, United States

For correspondence
olveczky@fas.harvard.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: The 124 male zebra finches (Taeniopygia guttata) used for this study were obtained from our breeding colony. The care and experimental manipulation of the animals were carried out in accordance with guidelines of the National Institutes of Health and were reviewed and approved by the Harvard Institutional Animal Care and Use Committee (Protocol #: 10-09).

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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.