Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds

• Authors: Varun Saravanan, Emory University; Lukas A. Hoffmann, Emory University; Amanda L. Jacob, Emory University; Gordon J Berman, Emory University; Samuel J Sober, Emory University
• Journal Title: eNeuro
• Volume: Volume 6, Number 3
• Publisher: Society for Neuroscience: eNeuro | 2019-05-01
• Type of Work: Article | Final Publisher PDF
• Publisher DOI: http://doi.org/10.1523/ENEURO.0190-19.2019
• Subjects: Biology, Neuroscience; Biology, Physiology
• Keywords: Bengalese finch; basal ganglia; dopamine; sensorimotor adaptation; songbird; vocal learning

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.