Neural correlates of vocal initiation in the VTA/SNc of juvenile male zebra finches

Shin Yanagihara,Ryosuke O Tachibana,Maki Ikebuchi,Kazuo Okanoya,Chihiro Mori

doi:10.1038/s41598-021-01955-3

Abstract

Initiation and execution of complex learned vocalizations such as human speech and birdsong depend on multiple brain circuits. In songbirds, neurons in the motor cortices and basal ganglia circuitry exhibit preparatory activity before initiation of song, and that activity is thought to play an important role in successful song performance. However, it remains unknown where a start signal for song is represented in the brain and how such a signal would lead to appropriate vocal initiation. To test whether neurons in the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) show activity related to song initiation, we carried out extracellular recordings of VTA/SNc single units in singing juvenile male zebra finches. We found that a subset of VTA/SNc units exhibit phasic activity precisely time-locked to the onset of the song bout, and that the activity occurred specifically at the beginning of song. These findings suggest that phasic activity in the VTA/SNc represents a start signal that triggers song vocalization.

Highlights

Initiation and execution of complex learned vocalizations such as human speech and birdsong depend on multiple brain circuits
We observed that ventral tegmental area (VTA)/substantia nigra pars compacta (SNc) single units exhibited changes in activity while a bird was singing (34/85 single units, 6 birds, Friedman test, p < 0.05), and these single units were classified into four types based on the activity profiles
Seventeen single units were classified as type-1, which showed a phasic increase in firing rate at the onset of the song bout, followed by a rapid decline in firing rate during singing (Fig. 1a,e,f, type-1, 4 birds)

Summary

Introduction

Initiation and execution of complex learned vocalizations such as human speech and birdsong depend on multiple brain circuits. To test whether neurons in the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) show activity related to song initiation, we carried out extracellular recordings of VTA/SNc single units in singing juvenile male zebra finches. Basal ganglia-projecting VTA dopaminergic neurons encode performance e rrors[32] and manipulations of this dopaminergic pathway have been shown to affect vocal learning[33,34,35] These studies underscore the importance of the VTA dopaminergic system in vocal learning in songbirds; the role of the dopaminergic system in the initiation of song vocalization has not been verified. We examined whether VTA/SNc neurons exhibit activity related to the initiation of song by recording extracellular single unit activity from singing juvenile zebra finches

Methods

Results

Conclusion