Performance monitoring in obsessive-compulsive disorder: Insights from internal capsule/nucleus accumbens deep brain stimulation

Thomas Schüller; Theo O J Gruendler; Ezra E Smith; Juan Carlos Baldermann; Sina Kohl; Adrian G Fischer; Veerle Visser-Vandewalle; Markus Ullsperger; Jens Kuhn; Daniel Huys

doi:10.1016/j.nicl.2021.102746

Performance monitoring in obsessive-compulsive disorder: Insights from internal capsule/nucleus accumbens deep brain stimulation

Neuroimage Clin. 2021:31:102746. doi: 10.1016/j.nicl.2021.102746. Epub 2021 Jun 29.

Authors

Affiliations

¹ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Psychiatry and Psychotherapy, Cologne, Germany. Electronic address: thomas.schueller@uk-koeln.de.
² Center for Military Mental Health, Military Hospital Berlin, Berlin, Germany.
³ Division of Translational Epidemiology, New York State Psychiatric Institute, New York, NY, USA.
⁴ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Psychiatry and Psychotherapy, Cologne, Germany; University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany.
⁵ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Psychiatry and Psychotherapy, Cologne, Germany.
⁶ Otto von Guericke University, Center for Behavioral Brain Sciences, Magdeburg, Germany; Freie Universität Berlin, Center for Cognitive Neuroscience, Berlin, Germany.
⁷ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Stereotactic and Functional Neurosurgery, Cologne, Germany.
⁸ Otto von Guericke University, Center for Behavioral Brain Sciences, Magdeburg, Germany; Otto von Guericke University, Institute of Psychology, Magdeburg, Germany.
⁹ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Psychiatry and Psychotherapy, Cologne, Germany; Johanniter Hospital Oberhausen, Department of Psychiatry, Psychotherapy and Psychosomatic, Oberhausen, Germany.

Abstract

Background: Symptoms of obsessive-compulsive disorder (OCD) are partly related to impaired cognitive control processes and theta modulations constitute an important electrophysiological marker for cognitive control processes such as signaling negative performance feedback in a fronto-striatal network. Deep brain stimulation (DBS) targeting the anterior limb of the internal capsule (ALIC)/nucleus accumbens (NAc) shows clinical efficacy in OCD, while the exact influence on the performance monitoring system remains largely unknown.

Methods: Seventeen patients with treatment-refractory OCD performed a probabilistic reinforcement learning task. Analyses were focused on 4-8 Hz (theta) power, intertrial phase coherence (ITPC) and debiased weighted Phase-Lag Index (dwPLI) in response to negative performance feedback. Combined EEG and local field potential (LFP) recordings were obtained shortly after DBS electrode implantation to investigate fronto-striatal network modulations. To assess the impact of clinically effective DBS on negative performance feedback modulations, EEG recordings were obtained pre-surgery and at follow-up with DBS on and off.

Results: Medial frontal cortex ITPC, striatal ITPC and striato-frontal dwPLI were increased following negative performance feedback. Decreased right-lateralized dwPLI was associated with pre-surgery symptom severity. ITPC was globally decreased during DBS-off.

Conclusion: We observed a theta phase coherence mediated fronto-striatal performance monitoring network. Within this network, decreased connectivity was related to increased OCD symptomatology, consistent with the idea of impaired cognitive control in OCD. While ALIC/NAc DBS decreased theta network activity globally, this effect was unrelated to clinical efficacy and performance monitoring.

Keywords: Deep brain stimulation; Internal capsule/nucleus accumbens; Obsessive-compulsive disorder; Performance monitoring; Theta frequency.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Deep Brain Stimulation*
Humans
Internal Capsule / diagnostic imaging
Nucleus Accumbens
Obsessive-Compulsive Disorder* / therapy
Treatment Outcome