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Modulation of EEG Functional Connectivity Networks in Subjects Undergoing Repetitive Transcranial Magnetic Stimulation

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Abstract

Transcranial magnetic stimulation (TMS) is a noninvasive brain stimulation technique that utilizes magnetic fluxes to alter cortical activity. Continuous theta-burst repetitive TMS (cTBS) results in long-lasting decreases in indices of cortical excitability, and alterations in performance of behavioral tasks. We investigated the effects of cTBS on cortical function via functional connectivity and graph theoretical analysis of EEG data. Thirty-one channel resting-state EEG recordings were obtained before and after 40 s of cTBS stimulation to the left primary motor cortex. Functional connectivity between nodes was assessed in multiple frequency bands using lagged max-covariance, and subsequently thresholded to construct undirected graphs. After cTBS, we find widespread decreases in functional connectivity in the alpha band. There are also simultaneous increases in functional connectivity in the high-beta bands, especially amongst anterior and interhemispheric connections. The analysis of the undirected graphs reveals that interhemispheric and interregional connections are more likely to be modulated after cTBS than local connections. There is also a shift in the topology of network connectivity, with an increase in the clustering coefficient after cTBS in the beta bands, and a decrease in clustering and increase in path length in the alpha band, with the alpha-band connectivity primarily decreased near the site of stimulation. cTBS produces widespread alterations in cortical functional connectivity, with resulting shifts in cortical network topology.

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Acknowledgments

Work on this study was supported by grants from the National Center for Research Resources: Harvard Clinical and Translational Science Center (UL1 RR025758), Center for Integration of Medicine and Innovative Technology (CIMIT), the Sidney R. Baer, Jr. Foundation, and Nexstim to APL. MMS was supported by funds from the National Center for Research Resources: Harvard Clinical and Translational Science Center (UL1 RR025758), and the Center for Integration of Medicine and Innovative Technology (CIMIT). MBW and SSC receive research support from the NIH/NINDS (RO1-NS062092). LO was supported by NIH fellowship F32MH080493 and 1KL2RR025757-01.

Disclosures

MMS, MBW, LO and SSC report no conflicts of interest. APL serves on the scientific advisory boards for Nexstim, Neuronix, Starlab Neuroscience, Allied Mind, Neosync, and Novavision, and is an inventor on patents and patent applications related to noninvasive brain stimulation and the real-time integration of transcranial magnetic stimulation with electroencephalography and magnetic resonance imaging.

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Authors and Affiliations

  1. Berenson-Allen Center for Noninvasive Brain Stimulation, Division of Cognitive Neurology, Department of Neurology, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA, 02215, USA

    Mouhsin M. Shafi, M. Brandon Westover, Lindsay Oberman & Alvaro Pascual-Leone

  2. Epilepsy Service, Department of Neurology, Beth Israel Deaconess Medical Center, West/Baker 5, Boston, MA, 02215, USA

    Mouhsin M. Shafi

  3. Department of Neurology, Harvard Medical School, Boston, MA, USA

    Mouhsin M. Shafi, M. Brandon Westover, Sydney S. Cash & Alvaro Pascual-Leone

  4. Epilepsy Service, Department of Neurology, Massachusetts General Hospital, Wang 720, Boston, MA, 02114, USA

    M. Brandon Westover & Sydney S. Cash

  5. Institut Universitari de Neurorehabilitacio′ Guttmann, Universidad Autónoma de Barcelona, Badalona, Spain

    Alvaro Pascual-Leone

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  1. Mouhsin M. Shafi
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Correspondence to Mouhsin M. Shafi.

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Mouhsin M. Shafi and M. Brandon Westover contributed equally to this study.

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Shafi, M.M., Brandon Westover, M., Oberman, L. et al. Modulation of EEG Functional Connectivity Networks in Subjects Undergoing Repetitive Transcranial Magnetic Stimulation. Brain Topogr 27, 172–191 (2014). https://doi.org/10.1007/s10548-013-0277-y

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