Abstract

Speech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.

Highlights

  • Speech is a highly complex motor skill which requires precise and fast coordination between vocal, facial and respiratory muscles

  • To test the hypothesis that cerebellar signals are sent to the song-related basal ganglia circuits and that the cerebellum participates in song learning, we performed the following experiments

  • Anatomical connections exist from the deep cerebellar nuclei (DCN) to the basal ganglia via the thalamus We performed anatomical tracing experiments to confirm the previously reported (Person et al, 2008) indirect connection from the DCN to the song-related basal ganglia nucleus Area X, via the dorsal thalamic zone (DTZ)

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Summary

Introduction

Speech is a highly complex motor skill which requires precise and fast coordination between vocal, facial and respiratory muscles. Human infants learn to reproduce adult vocalizations and to progressively master speech motor coordination within their first few years of life through an imitation process that builds up on motor sequence learning and strongly relies on auditory feedback (Kuhl and Meltzoff, 1996). This process, called vocal learning, is widely believed to rely on similar mechanisms as sensorimotor learning in general (Doupe and Kuhl, 1999; Kuhl and Meltzoff, 1996). Avian song learning has been used as a paradigm to study the neural mechanisms of vocal learning, as it shares striking similarities with human speech learning (reviewed in Doupe and Kuhl, 1999)

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