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Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography

Molecular Psychiatry (2024)Cite this article

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Abstract

Transcranial magnetic stimulation (TMS) is increasingly used as a noninvasive technique for neuromodulation in research and clinical applications, yet its mechanisms are not well understood. Here, we present the neurophysiological effects of TMS using intracranial electrocorticography (iEEG) in neurosurgical patients. We first evaluated safety in a gel-based phantom. We then performed TMS-iEEG in 22 neurosurgical participants with no adverse events. We next evaluated intracranial responses to single pulses of TMS to the dorsolateral prefrontal cortex (dlPFC) (N = 10, 1414 electrodes). We demonstrate that TMS is capable of inducing evoked potentials both locally within the dlPFC and in downstream regions functionally connected to the dlPFC, including the anterior cingulate and insular cortex. These downstream effects were not observed when stimulating other distant brain regions. Intracranial dlPFC electrical stimulation had similar timing and downstream effects as TMS. These findings support the safety and promise of TMS-iEEG in humans to examine local and network-level effects of TMS with higher spatiotemporal resolution than currently available methods.

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Fig. 1: TMS reliably and safely induces intracranial neural responses.
Fig. 2: TMS induces local evoked potentials within the dlPFC that correlate with electrical field strength.
Fig. 3: TMS evokes downstream iTEPs within the ACC and Insula.
Fig. 4: dlPFC TMS evokes downstream iTEPs in the ACC in a functionally connected and site-specific manner.
Fig. 5: Direct electrical stimulation of the dorsolateral prefrontal cortex (dlPFC) elicits responses in anterior cingulate cortex (ACC) and insula.

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Acknowledgements

First, we thank the neurosurgery patients who volunteered in this research. We also thank Christopher Kovach, Ariane Rhone, Haiming Chen, and Benjamin Pace for their assistance with image processing, coordinating, and conducting the experiments.

Funding

This research was supported by NIMH R01MH132074, R21MH120441 and 5R01dC004290-20. J.B.W. was supported by F30MH119763 and the Mark and Mary Stevens Interdisciplinary Graduate Fellowship. C.J.K was supported by R01MH126639, R01MH129018, and a Burroughs Wellcome Fund Career Award for Medical Scientists. A.D.B. was also supported by R01NS114405. N.T.T. was supported by 5T32-MH019113. We also thank Roy J. Carver Trust for funding this research. This work was conducted, in part, on an MRI instrument funded by 1S10OD025025-01.

Author information

Author notes

  1. These authors contributed equally: Jeffrey B. Wang, Umair Hassan.

  2. These authors jointly supervised this work: Corey J. Keller, Aaron D. Boes.

Authors and Affiliations

  1. Biophysics Graduate Program, Stanford University Medical Center, Stanford, CA, 94305, USA

    Jeffrey B. Wang

  2. Department of Psychiatry and Behavioral Sciences, Stanford University Medical Center, Stanford, CA, 94305, USA

    Jeffrey B. Wang, Umair Hassan & Corey J. Keller

  3. Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, CA, 94305, USA

    Umair Hassan & Corey J. Keller

  4. Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, USA

    Umair Hassan & Corey J. Keller

  5. Department of Neurology, Carver College of Medicine, University of Iowa, 200 Hawkins Drive, Iowa City, IA, 52242, USA

    Joel E. Bruss & Aaron D. Boes

  6. Department of Pediatrics, Carver College of Medicine, University of Iowa, 200 Hawkins Drive, Iowa City, IA, 52242, USA

    Joel E. Bruss, Brandt D. Uitermarkt & Aaron D. Boes

  7. Department of Neurosurgery, Carver College of Medicine, University of Iowa, 200 Hawkins Drive, Iowa City, IA, 52242, USA

    Hiroyuki Oya, Phillip E. Gander & Matthew A. Howard III

  8. Department of Psychiatry, Carver College of Medicine, University of Iowa, 200 Hawkins Drive, Iowa City, IA, 52242, USA

    Nicholas T. Trapp & Aaron D. Boes

  9. Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, 52242, USA

    Nicholas T. Trapp & Aaron D. Boes

  10. Department of Radiology, Carver College of Medicine, University of Iowa, 200 Hawkins Drive, Iowa City, IA, 52242, USA

    Phillip E. Gander

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  1. Jeffrey B. Wang
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  10. Aaron D. Boes
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Contributions

JBW, JEB, HO, CJK, and ADB conceived of the study. JBW and UH performed electrophysiology analyses. JEB performed imaging and electric field simulation analyses. HO performed safety testing and analyses and participated in experimental testing with TMS and intracranial stimulation. BDU, NTT, and PEG participated in experimental testing. MH helped with study design, safety, and subject recruitment. All authors contributed to writing and editing the manuscript. ADB and CJK jointly supervised all aspects of the study.

Corresponding author

Correspondence to Aaron D. Boes.

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Competing interests

CJK currently holds equity in Alto Neurosciences, Inc. The other authors declare no competing interests.

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Wang, J.B., Hassan, U., Bruss, J.E. et al. Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography. Mol Psychiatry (2024). https://doi.org/10.1038/s41380-024-02405-y

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