A Unified Functional Network Target for Deep Brain Stimulation in Obsessive-Compulsive Disorder.

ALIC Anterior limb of the internal capsule Connectome DBS Deep brain stimulation Functional connectivity OCD Obsessive-compulsive disorder STN Subthalamic nucleus

Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
15 11 2021
Historique:
received: 18 01 2021
revised: 26 03 2021
accepted: 12 04 2021
pubmed: 18 6 2021
medline: 19 11 2021
entrez: 17 6 2021
Statut: ppublish

Résumé

Multiple deep brain stimulation (DBS) targets have been proposed for treating intractable obsessive-compulsive disorder (OCD). Here, we investigated whether stimulation effects of different target sites would be mediated by one common or several segregated functional brain networks. First, seeding from active electrodes of 4 OCD patient cohorts (N = 50) receiving DBS to anterior limb of the internal capsule or subthalamic nucleus zones, optimal functional connectivity profiles for maximal Yale-Brown Obsessive Compulsive Scale improvements were calculated and cross-validated in leave-one-cohort-out and leave-one-patient-out designs. Second, we derived optimal target-specific connectivity patterns to determine brain regions mutually predictive of clinical outcome for both targets and others predictive for either target alone. Functional connectivity was defined using resting-state functional magnetic resonance imaging data acquired in 1000 healthy participants. While optimal functional connectivity profiles showed both commonalities and differences between target sites, robust cross-predictions of clinical improvements across OCD cohorts and targets suggested a shared network. Connectivity to the anterior cingulate cortex, insula, and precuneus, among other regions, was predictive regardless of stimulation target. Regions with maximal connectivity to these commonly predictive areas included the insula, superior frontal gyrus, anterior cingulate cortex, and anterior thalamus, as well as the original stereotactic targets. Pinpointing the network modulated by DBS for OCD from different target sites identified a set of brain regions to which DBS electrodes associated with optimal outcomes were functionally connected-regardless of target choice. On these grounds, we establish potential brain areas that could prospectively inform additional or alternative neuromodulation targets for obsessive-compulsive disorder.

Sections du résumé

BACKGROUND
Multiple deep brain stimulation (DBS) targets have been proposed for treating intractable obsessive-compulsive disorder (OCD). Here, we investigated whether stimulation effects of different target sites would be mediated by one common or several segregated functional brain networks.
METHODS
First, seeding from active electrodes of 4 OCD patient cohorts (N = 50) receiving DBS to anterior limb of the internal capsule or subthalamic nucleus zones, optimal functional connectivity profiles for maximal Yale-Brown Obsessive Compulsive Scale improvements were calculated and cross-validated in leave-one-cohort-out and leave-one-patient-out designs. Second, we derived optimal target-specific connectivity patterns to determine brain regions mutually predictive of clinical outcome for both targets and others predictive for either target alone. Functional connectivity was defined using resting-state functional magnetic resonance imaging data acquired in 1000 healthy participants.
RESULTS
While optimal functional connectivity profiles showed both commonalities and differences between target sites, robust cross-predictions of clinical improvements across OCD cohorts and targets suggested a shared network. Connectivity to the anterior cingulate cortex, insula, and precuneus, among other regions, was predictive regardless of stimulation target. Regions with maximal connectivity to these commonly predictive areas included the insula, superior frontal gyrus, anterior cingulate cortex, and anterior thalamus, as well as the original stereotactic targets.
CONCLUSIONS
Pinpointing the network modulated by DBS for OCD from different target sites identified a set of brain regions to which DBS electrodes associated with optimal outcomes were functionally connected-regardless of target choice. On these grounds, we establish potential brain areas that could prospectively inform additional or alternative neuromodulation targets for obsessive-compulsive disorder.

Identifiants

pubmed: 34134839
pii: S0006-3223(21)01223-3
doi: 10.1016/j.biopsych.2021.04.006
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

701-713

Informations de copyright

Copyright © 2021 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Ningfei Li (N)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany. Electronic address: ningfei.li@charite.de.

Barbara Hollunder (B)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany; Charité - Universitätsmedizin Berlin, Einstein Center for Neurosciences Berlin, Berlin, Germany; Berlin School of Mind and Brain, Faculty of Philosophy, Humboldt-Universität zu Berlin, Berlin, Germany.

Juan Carlos Baldermann (JC)

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

Astrid Kibleur (A)

Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut des Neurosciences (AK, SC, MP), Grenoble; and OpenMind Innovation (AK), Paris, France; OpenMind Innovation, Paris, France.

Svenja Treu (S)

Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Madrid, Spain.

Harith Akram (H)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, United Kingdom; National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Trust (UCLH), London, United Kingdom.

Bassam Al-Fatly (B)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany.

Bryan A Strange (BA)

Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Madrid, Spain.

Juan A Barcia (JA)

Neurosurgery Department, Hospital Clínico San Carlos, Universidad Complutense de Madrid, Madrid, Spain.

Ludvic Zrinzo (L)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, United Kingdom; National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Trust (UCLH), London, United Kingdom.

Eileen M Joyce (EM)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, United Kingdom; National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Trust (UCLH), London, United Kingdom.

Stephan Chabardes (S)

Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut des Neurosciences (AK, SC, MP), Grenoble; and OpenMind Innovation (AK), Paris, France.

Veerle Visser-Vandewalle (V)

Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany.

Mircea Polosan (M)

Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut des Neurosciences (AK, SC, MP), Grenoble; and OpenMind Innovation (AK), Paris, France.

Jens Kuhn (J)

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

Andrea A Kühn (AA)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany; Charité - Universitätsmedizin Berlin, Einstein Center for Neurosciences Berlin, Berlin, Germany; Berlin School of Mind and Brain, Faculty of Philosophy, Humboldt-Universität zu Berlin, Berlin, Germany.

Andreas Horn (A)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany; Charité - Universitätsmedizin Berlin, Einstein Center for Neurosciences Berlin, Berlin, Germany.

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