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

  • Author Footnotes
    1 NL and BH contributed equally to this work.
    Ningfei Li
    Correspondence
    Address correspondence to Ningfei Li, M.Sc.
    Footnotes
    1 NL and BH contributed equally to this work.
    Affiliations
    Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany
    Search for articles by this author
  • Author Footnotes
    1 NL and BH contributed equally to this work.
    Barbara Hollunder
    Footnotes
    1 NL and BH contributed equally to this work.
    Affiliations
    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
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  • Juan Carlos Baldermann
    Affiliations
    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
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  • Astrid Kibleur
    Affiliations
    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
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  • Svenja Treu
    Affiliations
    Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Madrid, Spain
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  • Harith Akram
    Affiliations
    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
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  • Bassam Al-Fatly
    Affiliations
    Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Movement Disorders and Neuromodulation Unit, Department of Neurology, Berlin, Germany
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  • Bryan A. Strange
    Affiliations
    Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Madrid, Spain
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  • Juan A. Barcia
    Affiliations
    Neurosurgery Department, Hospital Clínico San Carlos, Universidad Complutense de Madrid, Madrid, Spain
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  • Ludvic Zrinzo
    Affiliations
    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
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  • Eileen M. Joyce
    Affiliations
    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
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  • Stephan Chabardes
    Affiliations
    Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut des Neurosciences (AK, SC, MP), Grenoble; and OpenMind Innovation (AK), Paris, France
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  • Veerle Visser-Vandewalle
    Affiliations
    Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany
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  • Mircea Polosan
    Affiliations
    Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut des Neurosciences (AK, SC, MP), Grenoble; and OpenMind Innovation (AK), Paris, France
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  • Jens Kuhn
    Affiliations
    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
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  • Andrea A. Kühn
    Affiliations
    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
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  • Andreas Horn
    Affiliations
    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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  • Author Footnotes
    1 NL and BH contributed equally to this work.

      Abstract

      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.

      Keywords

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