A common neural circuit mechanism for internally guided and externally reinforced forms of motor learning

Erin Hisey,Matthew Gene Kearney,Richard Mooney

doi:10.1038/s41593-018-0092-6

Abstract

The complex skills underlying verbal and musical expression can be learned without external punishment or reward, indicating their learning is internally guided. The neural mechanisms that mediate internally guided learning are poorly understood, but a circuit comprising dopamine-releasing neurons in the midbrain ventral tegmental area (VTA) and their targets in the basal ganglia are important to externally reinforced learning. Juvenile zebra finches copy a tutor song in a process that is internally guided and, in adulthood, can learn to modify the fundamental frequency (pitch) of a target syllable in response to external reinforcement with white noise. Here we combined intersectional genetic ablation of VTA neurons, reversible blockade of dopamine receptors in the basal ganglia, and singing-triggered optogenetic stimulation of VTA terminals to establish that a common VTA–basal ganglia circuit enables internally guided song copying and externally reinforced syllable pitch learning.

Highlights

The complex skills underlying verbal and musical expression can be learned without external punishment or reward, indicating their learning is internally guided
To mammalian basal ganglia (BG), Area X is densely innervated by neurons in the ventral tegmental area (VTA) and the substantia nigra pars compacta (SNc) that are positive for tyrosine hydroxylase (TH)[23], the synthetic enzyme for dopamine
The VTA mediates reinforcement learning by activating dopamine receptors in the BG8,9, and we have shown that pitch-contingent optogenetic stimulation of VTAX terminals in Area X can drive pitch learning through a D1-receptordependent mechanism

Summary

Introduction

The complex skills underlying verbal and musical expression can be learned without external punishment or reward, indicating their learning is internally guided. Recent studies show that VTAX neurons in adult zebra finches subjected to singing-contingent noise function to encode reward prediction error[26], a well-described property of mammalian VTA neurons that serves as an essential component in reinforcement learning[7,8,9,10] These parallels support a model in which dopamine release from VTAX neurons is crucial to adult pitch learning, an idea that has gained support from a recent study showing that 6-hydroxydopamine (6-OHDA) lesions of TH+ terminals in Area X interfere with this form of song plasticity[27]. Beyond testing the necessity and sufficiency of VTAX neurons and dopamine signaling in Area X in adult pitch learning, whether these same cells and signaling pathways are important to juvenile song copying remains unexplored

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Conclusion