Internal Capsule/Nucleus Accumbens Deep Brain Stimulation Increases Impulsive Decision Making in Obsessive-Compulsive Disorder.

Cambridge Gambling Task Deep brain stimulation Impulsive decision making Internal capsule/nucleus accumbens Obsessive-compulsive disorder

Journal

Biological psychiatry. Cognitive neuroscience and neuroimaging
ISSN: 2451-9030
Titre abrégé: Biol Psychiatry Cogn Neurosci Neuroimaging
Pays: United States
ID NLM: 101671285

Informations de publication

Date de publication:
03 2023
Historique:
received: 29 06 2022
revised: 22 09 2022
accepted: 15 10 2022
pubmed: 5 2 2023
medline: 11 3 2023
entrez: 4 2 2023
Statut: ppublish

Résumé

Deep brain stimulation of the anterior limb of the internal capsule (ALIC)/nucleus accumbens is an effective treatment in patients with obsessive-compulsive disorder but may increase impulsive behavior. We aimed to investigate how active stimulation alters subdomains of impulsive decision making and whether respective effects depend on the location of stimulation sites. We assessed 15 participants with obsessive-compulsive disorder performing the Cambridge Gambling Task during active and inactive ALIC/nucleus accumbens deep brain stimulation. Specifically, we determined stimulation-induced changes in risk adjustment and delay aversion. To characterize underlying neural pathways, we computed probabilistic stimulation maps and applied fiber filtering based on normative structural connectivity data to identify "hot" and "cold" spots/fibers related to changes in impulsive decision making. Active stimulation significantly reduced risk adjustment while increasing delay aversion, both implying increased impulsive decision making. Changes in risk adjustment were robustly associated with stimulation sites located in the central ALIC and fibers connecting the thalamus and subthalamic nucleus with the medial and lateral prefrontal cortex. Both hot spots and fibers for changes in risk adjustment were robust to leave-one-out cross-validation. Changes in delay aversion were similarly associated with central ALIC stimulation, but validation hereof was nonsignificant. Our findings provide experimental evidence that ALIC/nucleus accumbens stimulation increases impulsive decision making in obsessive-compulsive disorder. We show that changes in risk adjustment depend on the location of stimulation volumes and affected fiber bundles. The relationship between impulsive decision making and long-term clinical outcomes requires further investigation.

Sections du résumé

BACKGROUND
Deep brain stimulation of the anterior limb of the internal capsule (ALIC)/nucleus accumbens is an effective treatment in patients with obsessive-compulsive disorder but may increase impulsive behavior. We aimed to investigate how active stimulation alters subdomains of impulsive decision making and whether respective effects depend on the location of stimulation sites.
METHODS
We assessed 15 participants with obsessive-compulsive disorder performing the Cambridge Gambling Task during active and inactive ALIC/nucleus accumbens deep brain stimulation. Specifically, we determined stimulation-induced changes in risk adjustment and delay aversion. To characterize underlying neural pathways, we computed probabilistic stimulation maps and applied fiber filtering based on normative structural connectivity data to identify "hot" and "cold" spots/fibers related to changes in impulsive decision making.
RESULTS
Active stimulation significantly reduced risk adjustment while increasing delay aversion, both implying increased impulsive decision making. Changes in risk adjustment were robustly associated with stimulation sites located in the central ALIC and fibers connecting the thalamus and subthalamic nucleus with the medial and lateral prefrontal cortex. Both hot spots and fibers for changes in risk adjustment were robust to leave-one-out cross-validation. Changes in delay aversion were similarly associated with central ALIC stimulation, but validation hereof was nonsignificant.
CONCLUSIONS
Our findings provide experimental evidence that ALIC/nucleus accumbens stimulation increases impulsive decision making in obsessive-compulsive disorder. We show that changes in risk adjustment depend on the location of stimulation volumes and affected fiber bundles. The relationship between impulsive decision making and long-term clinical outcomes requires further investigation.

Identifiants

pubmed: 36739254
pii: S2451-9022(22)00251-8
doi: 10.1016/j.bpsc.2022.10.005
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

281-289

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Thomas Schüller (T)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Sina Kohl (S)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Till Dembek (T)

Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Marc Tittgemeyer (M)

Max-Planck-Institute for Metabolism Research, Cologne, Germany; Cologne Cluster of Excellence in Cellular Stress and Aging associated Disease (CECAD), Cologne, Germany.

Daniel Huys (D)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany; Department of Psychiatry and Psychotherapy III, LVR Hospital Bonn, Bonn, Germany.

Veerle Visser-Vandewalle (V)

Department of Psychiatry and Psychotherapy III, LVR Hospital Bonn, Bonn, Germany.

Ningfei Li (N)

Movement Disorders and Neuromodulation Unit, Department for Neurology, Charité - University Medicine Berlin, Berlin, Germany.

Laura Wehmeyer (L)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany; Department of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Michael Barbe (M)

Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Jens Kuhn (J)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany; Department of Psychiatry, Psychotherapy, and Psychosomatics, Johanniter Hospital Oberhausen, Oberhausen, Germany.

Juan Carlos Baldermann (JC)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany; Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany. Electronic address: juan.baldermann@uk-koeln.de.

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Classifications MeSH