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      Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds

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          Abstract

          Dopamine is hypothesized to convey error information in reinforcement learning tasks with explicit appetitive or aversive cues. However, during motor skill learning feedback signals arise from an animal’s evaluation of sensory feedback resulting from its own behavior, rather than any external reward or punishment. It has previously been shown that intact dopaminergic signaling from the ventral tegmental area/substantia nigra pars compacta (VTA/SNc) complex is necessary for vocal learning when songbirds modify their vocalizations to avoid hearing distorted auditory feedback (playbacks of white noise). However, it remains unclear whether dopaminergic signaling underlies vocal learning in response to more naturalistic errors (pitch-shifted feedback delivered via headphones). We used male Bengalese finches ( Lonchura striata var. domestica) to test the hypothesis that the necessity of dopamine signaling is shared between the two types of learning. We combined 6-hydroxydopamine (6-OHDA) lesions of dopaminergic terminals within Area X, a basal ganglia nucleus critical for song learning, with a headphones learning paradigm that shifted the pitch of auditory feedback and compared their learning to that of unlesioned controls. We found that 6-OHDA lesions affected song behavior in two ways. First, over a period of days lesioned birds systematically lowered their pitch regardless of the presence or absence of auditory errors. Second, 6-OHDA lesioned birds also displayed severe deficits in sensorimotor learning in response to pitch-shifted feedback. Our results suggest roles for dopamine in both motor production and auditory error processing, and a shared mechanism underlying vocal learning in response to both distorted and pitch-shifted auditory feedback.

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          Author and article information

          Journal
          eNeuro
          eNeuro
          eneuro
          eneuro
          eNeuro
          eNeuro
          Society for Neuroscience
          2373-2822
          24 May 2019
          11 June 2019
          May-Jun 2019
          : 6
          : 3
          : ENEURO.0190-19.2019
          Affiliations
          [1 ]Neuroscience Graduate Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University , Atlanta, GA 30322
          [2 ]Department of Biology, Emory University , Atlanta, GA 30322
          [3 ]Department of Physics, Emory University , Atlanta, GA 30322
          Author notes

          The authors declare no competing financial interests.

          Author contributions: V.S., L.A.H., and S.J.S. designed research; V.S., L.A.H., and A.L.J. performed research; V.S. and G.J.B. analyzed data; V.S., A.L.J., G.J.B., and S.J.S. wrote the paper.

          This work was supported by National Institutes of Health (NIH) National Institute of Neurologic Disorders and Stroke Grants F31 NS100406 and R01 NS084844, the NIH National Institute of Biomedical Imaging and Bioengineering Grant R01EB022872, the NIH National Institute of Mental Health Grant R01 MH115831-01, the National Science Foundation Grant 1456912, and by Emory’s Udall Center of Excellence for Parkinson’s Disease Research.

          [*]

          L. A. Hoffmann’s present address: Micromeritics Instrument Corporation, Norcross, GA, 30093.

          Correspondence should be addressed to Samuel J. Sober at samuel.j.sober@ 123456emory.edu
          Author information
          http://orcid.org/0000-0002-1140-7469
          Article
          eN-NWR-0190-19
          10.1523/ENEURO.0190-19.2019
          6565373
          31126913
          8ed7f240-1849-46cd-be6c-829244546785
          Copyright © 2019 Saravanan et al.

          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.

          History
          : 17 May 2019
          : 18 May 2019
          Page count
          Figures: 6, Tables: 2, Equations: 5, References: 80, Pages: 17, Words: 13165
          Funding
          Funded by: http://doi.org/10.13039/100000065HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
          Award ID: F31 NS100406
          Award ID: R01 NS084844
          Funded by: http://doi.org/10.13039/100000070HHS | NIH | National Institute of Biomedical Imaging and Bioengineering (NIBIB)
          Award ID: R01 EB022872
          Funded by: http://doi.org/10.13039/100000025HHS | NIH | National Institute of Mental Health (NIMH)
          Award ID: R01 MH115831-01
          Funded by: http://doi.org/10.13039/100000154NSF | BIO | Division of Integrative Organismal Systems (IOS)
          Award ID: 1456912
          Funded by: Udall Center of Excellence for Parkinson's disease Research
          Categories
          1
          1.1
          New Research
          Cognition and Behavior
          Custom metadata
          May/June 2019

          basal ganglia,bengalese finch,dopamine,sensorimotor adaptation,songbird,vocal learning

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