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Bidirectional modulation of human emotional conflict resolution using intracranial stimulation

View ORCID ProfileAngelique C. Paulk, Ali Yousefi, Kristen K. Ellard, Kara Farnes, Noam Peled, Britni Crocker, Rina Zelmann, Deborah Vallejo-Lopez, Gavin Belok, Sam Zorowitz, Ishita Basu, Afsana Afzal, Anna Gilmour, Daniel S. Weisholtz, G. Reese Cosgrove, Bernard S. Chang, Jeffrey E. Arle, Ziv M. Williams, Uri T. Eden, Thilo Deckersbach, Darin D. Dougherty, Emad N. Eskandar, Alik S. Widge, Sydney S. Cash
doi: https://doi.org/10.1101/825893
Angelique C. Paulk
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
2Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
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  • ORCID record for Angelique C. Paulk
  • For correspondence: apaulk@mgh.harvard.edu
Ali Yousefi
2Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
3Department of Mathematics and Statistics, Boston University, Boston, MA, 02215
4Department of Computer Science, Worcester Polytechnic Institute (WPI), Worcester, MA 01609
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Kristen K. Ellard
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Kara Farnes
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
2Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
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Noam Peled
6Dept. of Radiology, MGH/HST Martinos Center for Biomedical Imaging and Harvard Medical School, Boston, MA
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Britni Crocker
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
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Rina Zelmann
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
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Deborah Vallejo-Lopez
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
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Gavin Belok
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
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Sam Zorowitz
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Ishita Basu
2Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Afsana Afzal
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Anna Gilmour
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Daniel S. Weisholtz
7Department of Neurology, Brigham and Women’s Hospital, Massachusetts 02115
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G. Reese Cosgrove
8Department of Neurosurgery, Brigham and Women’s Hospital, Massachusetts 02115
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Bernard S. Chang
9Department of Neurology, Beth Israel Deaconess Hospital, Boston, MA
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Jeffrey E. Arle
10Department of Neurosurgery, Beth Israel Deaconess Hospital, Boston, MA
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Ziv M. Williams
2Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
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Uri T. Eden
3Department of Mathematics and Statistics, Boston University, Boston, MA, 02215
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Thilo Deckersbach
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Darin D. Dougherty
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
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Emad N. Eskandar
2Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
11Department of Neurosurgery, Albert Einstein College of Medicine, Montefiore Medical Center, Bronx, NY 10467
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Alik S. Widge
5Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129
12Picower Institute for Learning & Memory, Massachusetts Institute of Technology, Cambridge, MA 02124
13Department of Psychiatry, University of Minnesota, Minneapolis, MN 55455
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Sydney S. Cash
1Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA
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Abstract

The ability to regulate emotions in the service of meeting ongoing goals and task demands is a key aspect of adaptive human behavior in our volatile social world. Consequently, difficulties in processing and responding to emotional stimuli underlie many psychiatric diseases ranging from depression to anxiety, the common thread being effects on behavior. Behavior, which is made up of shifting, difficult to measure hidden states such as attention and emotion reactivity, is a product of integrating external input and latent mental processes. Directly measuring, and differentiating, separable hidden cognitive, emotional, and attentional states contributing to emotion conflict resolution, however, is challenging, particularly when only using task-relevant behavioral measures such as reaction time. State-space representations are a powerful method for investigating hidden states underlying complex systems. Using state-space modeling of behavior, we identified relevant hidden cognitive states and predicted behavior in a standardized emotion regulation task. After identifying and validating models which best fit the behavior and narrowing our focus to one model, we used targeted intracranial stimulation of the emotion regulation-relevant neurocircuitry, including prefrontal structures and the amygdala, to causally modulate separable states. Finally, we focused on this one validated state-space model to perform real-time, bidirectional closed-loop adaptive stimulation in a subset of participants. These approaches enable an improved understanding of how to sample and understand emotional processing in a way which could be leveraged in neuromodulatory therapy for disorders of emotional regulation.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 31, 2019.
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Bidirectional modulation of human emotional conflict resolution using intracranial stimulation
Angelique C. Paulk, Ali Yousefi, Kristen K. Ellard, Kara Farnes, Noam Peled, Britni Crocker, Rina Zelmann, Deborah Vallejo-Lopez, Gavin Belok, Sam Zorowitz, Ishita Basu, Afsana Afzal, Anna Gilmour, Daniel S. Weisholtz, G. Reese Cosgrove, Bernard S. Chang, Jeffrey E. Arle, Ziv M. Williams, Uri T. Eden, Thilo Deckersbach, Darin D. Dougherty, Emad N. Eskandar, Alik S. Widge, Sydney S. Cash
bioRxiv 825893; doi: https://doi.org/10.1101/825893
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Bidirectional modulation of human emotional conflict resolution using intracranial stimulation
Angelique C. Paulk, Ali Yousefi, Kristen K. Ellard, Kara Farnes, Noam Peled, Britni Crocker, Rina Zelmann, Deborah Vallejo-Lopez, Gavin Belok, Sam Zorowitz, Ishita Basu, Afsana Afzal, Anna Gilmour, Daniel S. Weisholtz, G. Reese Cosgrove, Bernard S. Chang, Jeffrey E. Arle, Ziv M. Williams, Uri T. Eden, Thilo Deckersbach, Darin D. Dougherty, Emad N. Eskandar, Alik S. Widge, Sydney S. Cash
bioRxiv 825893; doi: https://doi.org/10.1101/825893

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