Transcranial electrical stimulation during functional magnetic resonance imaging in patients with genetic generalized epilepsy: a pilot and feasibility study

Zachary Cohen; Mirja Steinbrenner; Rory J Piper; Chayanin Tangwiriyasakul; Mark P Richardson; David J Sharp; Ines R Violante; David W Carmichael

doi:10.3389/fnins.2024.1354523

Transcranial electrical stimulation during functional magnetic resonance imaging in patients with genetic generalized epilepsy: a pilot and feasibility study

Front Neurosci. 2024 Mar 19:18:1354523. doi: 10.3389/fnins.2024.1354523. eCollection 2024.

Authors

Zachary Cohen^#¹, Mirja Steinbrenner^#^{1

2}, Rory J Piper^{1

3}, Chayanin Tangwiriyasakul¹, Mark P Richardson⁴, David J Sharp⁵, Ines R Violante^#⁶, David W Carmichael^#¹

Affiliations

¹ Department of Biomedical Engineering, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom.
² Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
³ University College London Great Ormond Street Institute of Child Health, University College London, London, United Kingdom.
⁴ Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology, and Neuroscience, King's College London, London, United Kingdom.
⁵ The Computational, Cognitive and Clinical Neuroimaging Laboratory, Department of Medicine, Imperial College London, London, United Kingdom.
⁶ School of Psychology, Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom.

^# Contributed equally.

Abstract

Objective: A third of patients with epilepsy continue to have seizures despite receiving adequate antiseizure medication. Transcranial direct current stimulation (tDCS) might be a viable adjunct treatment option, having been shown to reduce epileptic seizures in patients with focal epilepsy. Evidence for the use of tDCS in genetic generalized epilepsy (GGE) is scarce. We aimed to establish the feasibility of applying tDCS during fMRI in patients with GGE to study the acute neuromodulatory effects of tDCS, particularly on sensorimotor network activity.

Methods: Seven healthy controls and three patients with GGE received tDCS with simultaneous fMRI acquisition while watching a movie. Three tDCS conditions were applied: anodal, cathodal and sham. Periods of 60 s without stimulation were applied between each stimulation condition. Changes in sensorimotor cortex connectivity were evaluated by calculating the mean degree centrality across eight nodes of the sensorimotor cortex defined by the Automated Anatomical Labeling atlas (primary motor cortex (precentral left and right), supplementary motor area (left and right), mid-cingulum (left and right), postcentral gyrus (left and right)), across each of the conditions, for each participant.

Results: Simultaneous tDCS-fMRI was well tolerated in both healthy controls and patients without adverse effects. Anodal and cathodal stimulation reduced mean degree centrality of the sensorimotor network (Friedman's ANOVA with Dunn's multiple comparisons test; adjusted p = 0.02 and p = 0.03 respectively). Mean degree connectivity of the sensorimotor network during the sham condition was not different to the rest condition (adjusted p = 0.94).

Conclusion: Applying tDCS during fMRI was shown to be feasible and safe in a small group of patients with GGE. Anodal and cathodal stimulation caused a significant reduction in network connectivity of the sensorimotor cortex across participants. This initial research supports the feasibility of using fMRI to guide and understand network modulation by tDCS that might facilitate its clinical application in GGE in the future.

Keywords: Juvenile Myoclonic Epilepsy; epilepsy; functional MRI; neuromodulation; sensorimotor; transcranial electrical stimulation.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by funding from Epilepsy Research UK (ERUK PGE1802). ZC was funded by the Engineering and Physical Sciences Research Council (EP/R513064/1). IV was funded by the Wellcome Trust (103045/Z/13/Z) and BBSRC (BB/S008314/1). This study represents independent research supported by the National Institute for Health Research (NIHR) / Wellcome Trust King’s Clinical Research Facility and the NIHR Biomedical Research Centre and Dementia Unit at South London and Maudsley NHS Foundation Trust and King’s College London and by the National Institute for Health Research (NIHR) Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust and King’s College London and/or the NIHR Clinical Research Facility. This study was also supported by core funding from the Wellcome/EPSRC Centre for Medical Engineering [WT203148/Z/16/Z]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care.