Dopaminergic Contributions to Vocal Learning

J Neurosci. 2016 Feb 17;36(7):2176-89. doi: 10.1523/JNEUROSCI.3883-15.2016.

Abstract

Although the brain relies on auditory information to calibrate vocal behavior, the neural substrates of vocal learning remain unclear. Here we demonstrate that lesions of the dopaminergic inputs to a basal ganglia nucleus in a songbird species (Bengalese finches, Lonchura striata var. domestica) greatly reduced the magnitude of vocal learning driven by disruptive auditory feedback in a negative reinforcement task. These lesions produced no measureable effects on the quality of vocal performance or the amount of song produced. Our results suggest that dopaminergic inputs to the basal ganglia selectively mediate reinforcement-driven vocal plasticity. In contrast, dopaminergic lesions produced no measurable effects on the birds' ability to restore song acoustics to baseline following the cessation of reinforcement training, suggesting that different forms of vocal plasticity may use different neural mechanisms.

Significance statement: During skill learning, the brain relies on sensory feedback to improve motor performance. However, the neural basis of sensorimotor learning is poorly understood. Here, we investigate the role of the neurotransmitter dopamine in regulating vocal learning in the Bengalese finch, a songbird with an extremely precise singing behavior that can nevertheless be reshaped dramatically by auditory feedback. Our findings show that reduction of dopamine inputs to a region of the songbird basal ganglia greatly impairs vocal learning but has no detectable effect on vocal performance. These results suggest a specific role for dopamine in regulating vocal plasticity.

Keywords: Bengalese finch; basal ganglia; dopamine; negative reinforcement; songbird; vocal learning.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basal Ganglia / cytology
  • Basal Ganglia / physiology
  • Cell Count
  • Conditioning, Operant / physiology
  • Dopamine / physiology*
  • Feedback, Physiological
  • Finches / physiology*
  • Learning / physiology*
  • Male
  • Nerve Fibers / physiology
  • Neurons / physiology
  • Reinforcement, Psychology
  • Vocalization, Animal / physiology*

Substances

  • Dopamine