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Prospective Validation That Subgenual Connectivity Predicts Antidepressant Efficacy of Transcranial Magnetic Stimulation Sites

  • Author Footnotes
    1 AW and AH contributed equally to this work.
    Anne Weigand
    Footnotes
    1 AW and AH contributed equally to this work.
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany
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  • Author Footnotes
    1 AW and AH contributed equally to this work.
    Andreas Horn
    Footnotes
    1 AW and AH contributed equally to this work.
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Department of Neurology, Movement Disorder and Neuromodulation Unit, Charité – Universitätsmedizin, Berlin, Germany
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  • Ruth Caballero
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Bioengineering and Telemedicine Center, ETSI Telecomunicación, Universidad Politécnica de Madrid, Madrid, Spain
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  • Danielle Cooke
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts
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  • Adam P. Stern
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Division of Cognitive Neurology, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts
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  • Stephan F. Taylor
    Affiliations
    Department of Psychiatry, University of Michigan, Ann Arbor, Michigan
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  • Daniel Press
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Division of Cognitive Neurology, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts
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  • Alvaro Pascual-Leone
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Division of Cognitive Neurology, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Institut Guttmann, Universitat Autonoma de Barcelona, Madrid, Spain
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  • Michael D. Fox
    Correspondence
    Address correspondence to Michael D. Fox, M.D., Ph.D., Beth Israel Deaconess Medical Center, Department of Neurology, 330 Brookline Ave, Boston, MA 02215.
    Affiliations
    Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachusetts

    Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts

    Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, Massachusetts
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  • Author Footnotes
    1 AW and AH contributed equally to this work.
Published:November 09, 2017DOI:https://doi.org/10.1016/j.biopsych.2017.10.028

      Abstract

      Background

      The optimal target in the dorsolateral prefrontal cortex for treating depression with repetitive transcranial magnetic stimulation (rTMS) remains unknown. Better efficacy has been associated with stimulation sites that are 1) more anterior and lateral and 2) more functionally connected to the subgenual cingulate. Here we prospectively test whether these factors predict response in individual patients.

      Methods

      A primary cohort (Boston, n = 25) with medication-refractory depression underwent conventional open-label rTMS to the left dorsolateral prefrontal cortex. A secondary cohort (Michigan, n = 16) underwent 4 weeks of sham followed by open-label rTMS for nonresponders (n = 12). In each patient, the location of the stimulation site was recorded with frameless stereotaxy. Connectivity between each patient’s stimulation site and the subgenual cingulate was assessed using resting-state functional connectivity magnetic resonance imaging from a cohort of healthy subjects (n = 1000) and confirmed using connectivity from patients with depression (n = 38).

      Results

      In our primary cohort, antidepressant efficacy was predicted by stimulation sites that were both more anterolateral (r = .51, p < .01) and more negatively correlated with the subgenual cingulate (r = −.55, p < .005). However, subgenual connectivity was the only independent predictor of response and the only factor to predict response to active (r = −.52, p < .05) but not sham rTMS in our secondary cohort.

      Conclusions

      This study provides prospective validation that functional connectivity between an individual’s rTMS cortical target and the subgenual cingulate predicts antidepressant response. Implications for improving the cortical rTMS target for depression are discussed.

      Keywords

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      Linked Article

      • Where to Target? The Precision Medicine Approach to Brain Stimulation
        Biological PsychiatryVol. 84Issue 1
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          Across mental health disorders, there is a clear need to develop novel therapeutic strategies that are targeted to individual patient characteristics. Weigand et al. (1) demonstrate the possible value of connectivity-based targeting approaches for brain stimulation treatment of depression. The use of imaging biomarkers to guide individualized treatments for patients is an active area of research with several promising leads (2,3). This approach fits within the precision medicine approach of linking biological variables of individual patients to treatment options (4).
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