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Theta-burst direct electrical stimulation remodels human brain networks

Author

Listed:
  • Yuhao Huang

    (Stanford University)

  • Rina Zelmann

    (Massachusetts General Hospital, Harvard Medical School
    Massachusetts General Hospital)

  • Peter Hadar

    (Massachusetts General Hospital, Harvard Medical School)

  • Jaquelin Dezha-Peralta

    (Massachusetts General Hospital, Harvard Medical School
    Massachusetts General Hospital)

  • R. Mark Richardson

    (Massachusetts General Hospital and Harvard Medical School)

  • Ziv M. Williams

    (Massachusetts General Hospital and Harvard Medical School)

  • Sydney S. Cash

    (Massachusetts General Hospital, Harvard Medical School
    Massachusetts General Hospital)

  • Corey J. Keller

    (Stanford University
    Stanford University
    and Clinical Center (MIRECC))

  • Angelique C. Paulk

    (Massachusetts General Hospital, Harvard Medical School
    Massachusetts General Hospital)

Abstract

Theta-burst stimulation (TBS), a patterned brain stimulation technique that mimics rhythmic bursts of 3–8 Hz endogenous brain rhythms, has emerged as a promising therapeutic approach for treating a wide range of brain disorders, though the neural mechanism of TBS action remains poorly understood. We investigated the neural effects of TBS using intracranial EEG (iEEG) in 10 pre-surgical epilepsy participants undergoing intracranial monitoring. Here we show that individual bursts of direct electrical TBS at 29 frontal and temporal sites evoked strong neural responses spanning broad cortical regions. These responses exhibited dynamic local field potential voltage changes over the course of stimulation presentations, including either increasing or decreasing responses, suggestive of short-term plasticity. Stronger stimulation augmented the mean TBS response amplitude and spread with more recording sites demonstrating short-term plasticity. TBS responses were stimulation site-specific with stronger TBS responses observed in regions with strong baseline stimulation effective (cortico-cortical evoked potentials) and functional (low frequency phase locking) connectivity. Further, we could use these measures to predict stable and varying (e.g. short-term plasticity) TBS response locations. Future work may integrate pre-treatment connectivity alongside other biophysical factors to personalize stimulation parameters, thereby optimizing induction of neuroplasticity within disease-relevant brain networks.

Suggested Citation

  • Yuhao Huang & Rina Zelmann & Peter Hadar & Jaquelin Dezha-Peralta & R. Mark Richardson & Ziv M. Williams & Sydney S. Cash & Corey J. Keller & Angelique C. Paulk, 2024. "Theta-burst direct electrical stimulation remodels human brain networks," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51443-1
    DOI: 10.1038/s41467-024-51443-1
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    References listed on IDEAS

    as
    1. Kai J Miller & Klaus-Robert Müller & Dora Hermes, 2021. "Basis profile curve identification to understand electrical stimulation effects in human brain networks," PLOS Computational Biology, Public Library of Science, vol. 17(9), pages 1-20, September.
    2. Cynthia D. Rittenhouse & Harel Z. Shouval & Michael A. Paradiso & Mark F. Bear, 1999. "Monocular deprivation induces homosynaptic long-term depression in visual cortex," Nature, Nature, vol. 397(6717), pages 347-350, January.
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    4. Sankaraleengam Alagapan & Ki Sueng Choi & Stephen Heisig & Patricio Riva-Posse & Andrea Crowell & Vineet Tiruvadi & Mosadoluwa Obatusin & Ashan Veerakumar & Allison C. Waters & Robert E. Gross & Sinea, 2023. "Cingulate dynamics track depression recovery with deep brain stimulation," Nature, Nature, vol. 622(7981), pages 130-138, October.
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