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

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 plast...

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Main Authors: James N McGregor, Abigail L Grassler, Paul I Jaffe, Amanda Louise Jacob, Michael S Brainard, Samuel J Sober
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/75691
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author James N McGregor
Abigail L Grassler
Paul I Jaffe
Amanda Louise Jacob
Michael S Brainard
Samuel J Sober
author_facet James N McGregor
Abigail L Grassler
Paul I Jaffe
Amanda Louise Jacob
Michael S Brainard
Samuel J Sober
author_sort James N McGregor
collection DOAJ
description 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.
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spelling doaj.art-62aca497bb16498ca279a64545ca6a5a2022-12-22T04:32:14ZengeLife Sciences Publications LtdeLife2050-084X2022-09-011110.7554/eLife.75691Shared mechanisms of auditory and non-auditory vocal learning in the songbird brainJames N McGregor0https://orcid.org/0000-0002-5187-0984Abigail L Grassler1Paul I Jaffe2https://orcid.org/0000-0003-0680-3923Amanda Louise Jacob3Michael S Brainard4https://orcid.org/0000-0002-9425-9907Samuel J Sober5https://orcid.org/0000-0002-1140-7469Neuroscience Graduate Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University, Atlanta, United StatesDepartment of Biology, Emory University, Atlanta, United StatesCenter for Integrative Neuroscience, University of California, San Francisco, San Francisco, United StatesDepartment of Biology, Emory University, Atlanta, United StatesCenter for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDepartment of Biology, Emory University, Atlanta, United StatesSongbirds 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.https://elifesciences.org/articles/75691Bengalese finchsongbirdlonchura striata var. domestica
spellingShingle James N McGregor
Abigail L Grassler
Paul I Jaffe
Amanda Louise Jacob
Michael S Brainard
Samuel J Sober
Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
eLife
Bengalese finch
songbird
lonchura striata var. domestica
title Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
title_full Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
title_fullStr Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
title_full_unstemmed Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
title_short Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain
title_sort shared mechanisms of auditory and non auditory vocal learning in the songbird brain
topic Bengalese finch
songbird
lonchura striata var. domestica
url https://elifesciences.org/articles/75691
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