Abstract

Although the basal ganglia have been implicated in a growing list of human behaviors, they include some of the least understood nuclei in the brain. For several decades studies have employed numerous methodologies to uncover evidence pointing to the basal ganglia as a hub of both motor and non-motor function. Recently, new electrophysiological characterization of the basal ganglia in humans has become possible through direct access to these deep structures as part of routine neurosurgery. Electrophysiological approaches for identifying non-motor function have the potential to unlock a deeper understanding of pathways that may inform clinical interventions and particularly neuromodulation. Various electrophysiological modalities can also be combined to reveal functional connections between the basal ganglia and traditional structures throughout the neocortex that have been linked to non-motor behavior. Several reviews have previously summarized evidence for non-motor function in the basal ganglia stemming from behavioral, clinical, computational, imaging, and non-primate animal studies; in this review, instead we turn to electrophysiological studies of non-human primates and humans. We begin by introducing common electrophysiological methodologies for basal ganglia investigation, and then we discuss studies across numerous non-motor domains–emotion, response inhibition, conflict, decision-making, error-detection and surprise, reward processing, language, and time processing. We discuss the limitations of current approaches and highlight the current state of the information.

Highlights

  • The putative role of the basal ganglia as a predominantly motor structure in the brain is being increasingly challenged

  • We focus on electrophysiological evidence for non-motor function in human and non-human primate basal ganglia, primarily of the subthalamic nucleus (STN)

  • We have reviewed an extensive literature on non-motor electrophysiology of human and non-human primate basal ganglia, primarily from single-unit and local field potentials (LFPs) studies

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Summary

INTRODUCTION

The putative role of the basal ganglia as a predominantly motor structure in the brain is being increasingly challenged. Negative valence (i.e., threat of loss or punishment) and single unit responses to reward were first investigated in a recent study of the STN and GPi during a modified Go/No-Go task (Rossi et al, 2017) While both structures showed neurons responsive to reward, this large study of 53 PD DBS patients demonstrated that regardless of the valence-related stimulus—whether being a reward receipt or successful avoidance of loss—the STN modulated more than the GPi. Most of the neurons identified, which were distributed throughout both structures in a non-tripartite fashion, were exclusive for reward anticipation, reward receipt, threat of loss, or successful avoidance of loss. These results suggest involvement of the basal ganglia in giving the initiating prompt of behaviors involving sequential timing (Bartolo and Merchant, 2015)

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