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Autonomic arousal elicited by subcallosal cingulate stimulation is explained by white matter connectivity

  • Author Footnotes
    1 Authors contributed equally to this manuscript.
    Patricio Riva-Posse
    Correspondence
    Corresponding author. Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, 101 Woodruff Cir NE, Suite 4309, Atlanta, GA, 30322, USA.
    Footnotes
    1 Authors contributed equally to this manuscript.
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, 101 Woodruff Circle, Atlanta, 30322, GA, USA
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  • Author Footnotes
    1 Authors contributed equally to this manuscript.
    Cory S. Inman
    Footnotes
    1 Authors contributed equally to this manuscript.
    Affiliations
    Department of Neurosurgery, Emory University School of Medicine, 1365 Clifton Road, Atlanta, 30322, GA, USA

    Department of Psychology, Emory University, 36 Eagle Row, Atlanta, 30322, GA, USA
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  • Ki Sueng Choi
    Affiliations
    Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 1470 Madison Ave, New York, 10029, NY, USA
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  • Andrea L. Crowell
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, 101 Woodruff Circle, Atlanta, 30322, GA, USA
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  • Robert E. Gross
    Affiliations
    Department of Neurosurgery, Emory University School of Medicine, 1365 Clifton Road, Atlanta, 30322, GA, USA

    Department of Neurology, Emory University School of Medicine, 1365 Clifton Road, Atlanta, 30322, GA, USA

    Coulter Department of Biomedical Engineering, Georgia Institute of Technology & Emory University School of Medicine, 1760 Haygood Dr., Atlanta, 30322, GA, USA
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  • Stephan Hamann
    Affiliations
    Department of Psychology, Emory University, 36 Eagle Row, Atlanta, 30322, GA, USA
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  • Helen S. Mayberg
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, 101 Woodruff Circle, Atlanta, 30322, GA, USA

    Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 1470 Madison Ave, New York, 10029, NY, USA
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  • Author Footnotes
    1 Authors contributed equally to this manuscript.
Published:January 25, 2019DOI:https://doi.org/10.1016/j.brs.2019.01.015

      Highlights

      • Autonomic changes with SCC DBS correspond to the salience of behavioral responses.
      • These changes are evidence of the distant effects of SCC DBS in midcingulate cortex.
      • These findings aid in the optimal selection of contacts and parameters in SCC DBS surgery.

      Abstract

      Background

      Subcallosal cingulate deep brain stimulation (SCC DBS) is an experimental treatment for severe depression. Surgery is performed with awake patients and intraoperative stimulation produces acute behavioral responses in select contacts. While there have been reports on the relationship between acute intraoperative behaviors and their relation to the location of the contacts, there are no descriptions of the physiological changes that accompany them.

      Objective

      The present study sought to examine these physiological readouts, and their association with the anatomical substrates that generated them.

      Methods

      Nine patients with severe, treatment-resistant depression were tested intraoperatively. The stimulation protocol consisted of 12 three-minute, sham-controlled, double-blind trials. Changes in heart rate and skin conductance were recorded during each stimulation cycle. Probabilistic tractography between the stimulated contacts and predefined regions of the mood regulation network was performed.

      Results

      Acute intraoperative SCC stimulation produced increases in autonomic sympathetic response that correlated with the salience of the behavioral responses. The autonomic changes were observed within seconds of initiating acute stimulation and prior to verbalization of subjective experiences. The probabilistic tractography analysis suggested that structural connectivity between the stimulated area and the midcingulate cortex is the primary pathway that mediates autonomic responsivity to SCC DBS.

      Conclusions

      These findings demonstrate that acute SCC stimulation produces autonomic and behavioral changes in the operating room that are explained by the modulation of networks associated with long term antidepressant response. Intraoperative autonomic recordings paired with careful behavioral observations and precise anatomical mapping aid in the identification and classification of the intraoperative phenomena.

      Keywords

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