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Author Notes:

Samuel J. Sober : samuel.j.sober@emory.edu

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.

We thank David Hercules and Connor G. Gallimore for their role in assisting Amanda L. Jacob with tissue processing and imaging for some of the histology presented in this paper.

The authors declare no competing financial interests.

Subjects:

Research Funding:

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.

Keywords:

  • Bengalese finch
  • basal ganglia
  • dopamine
  • sensorimotor adaptation
  • songbird
  • vocal learning

Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds

Journal Title:

eNeuro

Volume:

Volume 6, Number 3

Publisher:

Type of Work:

Article | Final Publisher PDF

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.

Copyright information:

Copyright © 2019 Saravanan et al.

This is an Open Access work distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/).
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