Abstract

The human nucleus accumbens is thought to play an important role in guiding future action selection via an evaluation of current action outcomes. Here we provide electrophysiological evidence for a more direct, i.e., online, role during action preparation. We recorded local field potentials from the nucleus accumbens in patients with epilepsy undergoing surgery for deep brain stimulation. We found a consistent decrease in the power of alpha/beta oscillations (10-30 Hz) before and around the time of movements. This perimovement alpha/beta desynchronization was observed in seven of eight patients and was present both before instructed movements in a serial reaction time task as well as before self-paced, deliberate choices in a decision making task. A similar beta decrease over sensorimotor cortex and in the subthalamic nucleus has been directly related to movement preparation and execution. Our results support the idea of a direct role of the human nucleus accumbens in action preparation and execution.

Highlights

  • The present work clarifies how the nucleus accumbens contributes to action

  • In a recent study of local field potentials (LFPs) from the human NUCLEUS ACCUMBENS (NAcc) we found a cortical drive of delta oscillations prior to choices in an economic decision making task (Stenner et al 2015a), in line with findings of a similar coupling during instrumental behavior in rodents (Gruber et al 2009)

  • We tested whether a characteristic movement-related signal consistently observed in scalp EEG electrodes over sensorimotor cortex, namely, a decrease of beta power before and around the time of movement (Pfurtscheller et al 2003), is evident in LFPs recorded from the NAcc

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Summary

Introduction

The present work clarifies how the nucleus accumbens contributes to action. This region is often assumed to influence behavior “off-line” by evaluating outcomes. The NAcc is often assumed to influence behavior via an evaluation of action outcomes Supporting this view, functional imaging studies and single-unit recordings in humans describe signals in the NAcc consistent with reward prediction errors (RPEs), the difference between actual and expected rewards (Abler et al 2006; Patel et al 2012; Rutledge et al 2010; but see Stenner et al 2015b). RPE signals in the NAcc have been taken as evidence that the ventral striatum, which includes the NAcc, functions as a “critic” (Sutton and Barto 1998) by learning to predict reward, while an “actor” located elsewhere in the brain performs action selection (Montague et al 2004; O’Doherty et al 2004) In this framework, the NAcc fulfils an indirect, “off-line,” behavioral function at a time when no action is being prepared rather than contributing directly to the ongoing selection of imminent actions. PERIMOVEMENT BETA DECREASE IN THE ACCUMBENS imminent action, beyond its putative function in evaluating action outcomes

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