Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain

  1. James N McGregor  Is a corresponding author
  2. Abigail L Grassler
  3. Paul I Jaffe
  4. Amanda Louise Jacob
  5. Michael S Brainard
  6. Samuel J Sober
  1. Emory University, United States
  2. University of California, San Francisco, United States

Abstract

Songbirds and humans share the ability to adaptively modify their vocalizations based on sensory feedback. Prior studies have focused primarily on the role that auditory feedback plays in shaping vocal output throughout life. In contrast, it is unclear how non-auditory information drives vocal plasticity. Here, we first used a reinforcement learning paradigm to establish that somatosensory feedback (cutaneous electrical stimulation) can drive vocal learning in adult songbirds. We then assessed the role of a songbird basal ganglia thalamocortical pathway critical to auditory vocal learning in this novel form of vocal plasticity. We found that both this circuit and its dopaminergic inputs are necessary for non-auditory vocal learning, demonstrating that this pathway is critical for guiding adaptive vocal changes based on both auditory and somatosensory signals. The ability of this circuit to use both auditory and somatosensory information to guide vocal learning may reflect a general principle for the neural systems that support vocal plasticity across species.

Data availability

Source data are provided for all main figures and relevant figure supplements (Figure 2b-f, Figure 2 - Figure Supplements 1-7, Figure 3b-e, Figure 3 - Figure Supplement 1, and Figure 4b-d). MATLAB code for generating these figures is also provided in the associated source code files. Data and source code have also been uploaded to a public data repository on figshare, in a project titled 'Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain.'

The following data sets were generated

Article and author information

Author details

  1. James N McGregor

    Neuroscience Graduate Program, Emory University, Atlanta, United States
    For correspondence
    jmcgregor2292@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5187-0984
  2. Abigail L Grassler

    Neuroscience Graduate Program, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Paul I Jaffe

    Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0680-3923
  4. Amanda Louise Jacob

    Department of Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael S Brainard

    Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9425-9907
  6. Samuel J Sober

    Department of Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1140-7469

Funding

National Institutes of Health (R01- EB022872)

  • James N McGregor
  • Abigail L Grassler
  • Amanda Louise Jacob
  • Samuel J Sober

National Institutes of Health (R01- NS084844)

  • James N McGregor
  • Abigail L Grassler
  • Amanda Louise Jacob
  • Samuel J Sober

National Institutes of Health (R01- NS099375)

  • James N McGregor
  • Abigail L Grassler
  • Amanda Louise Jacob
  • Samuel J Sober

Simons Foundation (Emory International Consortium on Motor Control)

  • Samuel J Sober

Howard Hughes Medical Institute

  • Paul I Jaffe
  • Michael S Brainard

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 experimental protocols were approved by the Emory University and UC San Francisco Institutional Animal Care and Use Committees (protocol #201700359)

Reviewing Editor

  1. Jesse H Goldberg, Cornell University, United States

Publication history

  1. Received: November 19, 2021
  2. Accepted: September 14, 2022
  3. Accepted Manuscript published: September 15, 2022 (version 1)

Copyright

© 2022, McGregor et al.

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.

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  1. James N McGregor
  2. Abigail L Grassler
  3. Paul I Jaffe
  4. Amanda Louise Jacob
  5. Michael S Brainard
  6. Samuel J Sober
(2022)
Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
eLife 11:e75691.
https://doi.org/10.7554/eLife.75691
  1. Further reading

Further reading

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