Nucleus accumbens is involved in human action monitoring: evidence from invasive electrophysiological recordings

Thomas F Münte

doi:10.3389/neuro.09.011.2007

Abstract

The Nucleus accumbens (Nacc) has been proposed to act as a limbic-motor interface. Here, using invasive intraoperative recordings in an awake patient suffering from obsessive-compulsive disease (OCD), we demonstrate that its activity is modulated by the quality of performance of the subject in a choice reaction time task designed to tap action monitoring processes. Action monitoring, that is, error detection and correction, is thought to be supported by a system involving the dopaminergic midbrain, the basal ganglia, and the medial prefrontal cortex. In surface electrophysiological recordings, action monitoring is indexed by an error-related negativity (ERN) appearing time-locked to the erroneous responses and emanating from the medial frontal cortex. In preoperative scalp recordings the patient's ERN was found to be significantly increased compared to a large (n = 83) normal sample, suggesting enhanced action monitoring processes. Intraoperatively, error-related modulations were obtained from the Nacc but not from a site 5 mm above. Importantly, cross-correlation analysis showed that error-related activity in the Nacc preceded surface activity by 40 ms. We propose that the Nacc is involved in action monitoring, possibly by using error signals from the dopaminergic midbrain to adjust the relative impact of limbic and prefrontal inputs on frontal control systems in order to optimize goal-directed behavior.

Highlights

We continuously evaluate our actions in order to detect and correct performance errors suggesting that we are endowed with a cognitive system that monitors and optimizes our behavior
The error-related negativity (ERN) has been proposed to be driven by reinforcement learning signals originating in the mesencephalic dopamine system (MDS; Holroyd and Coles, 2002)
This fits well with previous investigations from our (Johannes et al, 2001, 2002) and other laboratories (Gehring et al, 2000; Hajcak and Simons, 2002; Santesso et al, 2006) which have reported an increased amplitude of the ERN in obsessive-compulsive disease (OCD) patients, patients with Tourette’s syndrome with comorbid OCD, and normal participants with obsessivecompulsive personality traits. These findings have been interpreted as reflecting increased action monitoring in OCD subjects, an interpretation which is supported by a recent fMRI study that reported significantly greater error-related activation of the rostral ACC in OCD compared to healthy subjects (Fitzgerald et al, 2005)

Summary

Introduction

We continuously evaluate our actions in order to detect and correct performance errors suggesting that we are endowed with a cognitive system that monitors and optimizes our behavior. A monitoring system located in the basal ganglia is thought to evaluate internal “efference copies” of ongoing actions From this information, the monitoring system predicts whether ongoing events will end in success or failure. If the system revises its predictions for the worse, as in performance errors, it induces a phasic decrease in the activity of the MDS. These positive and negative reward prediction error signals are carried by the MDS to various brain areas including the anterior cingulate cortex, where they are used to improve performance on the task at hand in line with principles of reinforcement learning (Schultz, 2006)

Methods

Results

Conclusion