Error-Related Activity in Striatal Local Field Potentials and Medial Frontal Cortex: Evidence From Patients With Severe Opioid Abuse Disorder

Elena Sildatke; Thomas Schüller; Theo O J Gründler; Markus Ullsperger; Veerle Visser-Vandewalle; Daniel Huys; Jens Kuhn

doi:10.3389/fnhum.2020.627564

Error-Related Activity in Striatal Local Field Potentials and Medial Frontal Cortex: Evidence From Patients With Severe Opioid Abuse Disorder

Front Hum Neurosci. 2021 Feb 1:14:627564. doi: 10.3389/fnhum.2020.627564. eCollection 2020.

Authors

Elena Sildatke¹, Thomas Schüller¹, Theo O J Gründler², Markus Ullsperger^{3

4}, Veerle Visser-Vandewalle⁵, Daniel Huys¹, Jens Kuhn^{1

6}

Affiliations

¹ Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
² Center for Military Mental Health, Military Hospital Berlin, Berlin, Germany.
³ Department of Psychology, Otto-von-Guericke University, Magdeburg, Germany.
⁴ Center for Behavioral Brain Sciences, Magdeburg, Germany.
⁵ Department of Stereotactic and Functional Surgery, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁶ Department of Psychiatry, Psychotherapy, and Psychosomatic Medicine, Johanniter Hospital Oberhausen, Oberhausen, Germany.

Abstract

For successful goal-directed behavior, a performance monitoring system is essential. It detects behavioral errors and initiates behavioral adaptations to improve performance. Two electrophysiological potentials are known to follow errors in reaction time tasks: the error-related negativity (ERN), which is linked to error processing, and the error positivity (Pe), which is associated with subjective error awareness. Furthermore, the correct-related negativity (CRN) is linked to uncertainty about the response outcome. Here we attempted to identify the involvement of the nucleus accumbens (NAc) in the aforementioned performance monitoring processes. To this end, we simultaneously recorded cortical activity (EEG) and local field potentials (LFP) during a flanker task performed by four patients with severe opioid abuse disorder who underwent electrode implantation in the NAc for deep brain stimulation. We observed significant accuracy-related modulations in the LFPs at the time of the ERN/CRN in two patients and at the time of Pe in three patients. These modulations correlated with the ERN in 2/8, with CRN in 5/8 and with Pe in 6/8, recorded channels, respectively. Our results demonstrate the functional interrelation of striatal and cortical processes in performance monitoring specifically related to error processing and subjective error awareness.

Keywords: deep brain stimulation; error positivity; error processing; error-related negativity; intracranial recordings; local field potential; nucleus accumbens; performance monitoring.