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, Abdullah Azeem Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University , Montréal QC H3A 2B4 , Correspondence to: Abdullah Azeem, Montreal Neurological Institute, 3801 Rue Université, Montréal, QC H3A 2B4, Canada, E-mail: Abdullah.azeem@mail.mcgill.ca Search for other works by this author on: Oxford Academic Chifaou Abdallah Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University , Montréal QC H3A 2B4 , Canada Search for other works by this author on: Oxford Academic Nicolás von Ellenrieder Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University , Montréal QC H3A 2B4 , Canada Search for other works by this author on: Oxford Academic Charbel El Kosseifi Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University , Montréal QC H3A 2B4 , Canada Search for other works by this author on: Oxford Academic Birgit Frauscher Department of Neurology, Duke University School of Medicine , Durham NC , USA Search for other works by this author on: Oxford Academic Jean Gotman Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University , Montréal QC H3A 2B4 , Canada Search for other works by this author on: Oxford Academic
https://orcid.org/0000-0002-4598-781X Brain, awae192, https://doi.org/10.1093/brain/awae192
Published:
14 June 2024
Article history
Received:
05 October 2023
Revision received:
11 April 2024
Accepted:
16 May 2024
Published:
14 June 2024
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Abdullah Azeem, Chifaou Abdallah, Nicolás von Ellenrieder, Charbel El Kosseifi, Birgit Frauscher, Jean Gotman, Explaining slow seizure propagation with white matter tractography, Brain, 2024;, awae192, https://doi.org/10.1093/brain/awae192
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Abstract
Epileptic seizures recorded with stereoelectroencephalography (SEEG) can take a fraction of a second or several seconds to propagate from one region to another. What explains such propagation patterns? We combine tractography and SEEG to determine the relationship between seizure propagation and the white matter architecture and to describe seizure propagation mechanisms.
Patient-specific spatiotemporal seizure propagation maps were combined with tractography from diffusion imaging of matched subjects from the Human Connectome Project. The onset of seizure activity was marked on a channel-by-channel basis by two board-certified neurologists for all channels involved in the seizure. We measured the tract connectivity (number of tracts) between regions-of-interest pairs among the seizure onset zone, regions of seizure spread, and non-involved regions. We also investigated how tract-connected the seizure onset zone is to regions of early seizure spread compared to regions of late spread. Comparisons were made after correcting for differences in distance.
Sixty-nine seizures were marked across 26 patients with drug-resistant epilepsy; 11 were seizure free after surgery (Engel IA) and 15 were not (Engel IB-IV). The seizure onset zone was more tract connected to regions of seizure spread than to non-involved regions (p<0.0001); however, regions of seizure spread were not differentially tract-connected to other regions of seizure spread compared to non-involved regions. In seizure free patients only, regions of seizure spread were more tract connected to the seizure onset zone than to other regions of spread (p<0.0001). Over the temporal evolution of a seizure, the seizure onset zone was significantly more tract connected to regions of early spread compared to regions of late spread in seizure free patients only (p<0.0001).
By integrating information on structure, we demonstrate that seizure propagation is likely mediated by white matter tracts. The pattern of connectivity between seizure onset zone, regions of spread and non-involved regions demonstrates that the onset zone may be largely responsible for seizures propagating throughout the brain, rather than seizures propagating to intermediate points, from which further propagation takes place. Our findings also suggest that seizure propagation over seconds may be the result of a continuous bombardment of action potentials from the seizure onset zone to regions of spread. In non-seizure free patients, the paucity of tracts from the presumed seizure onset zone to regions of spread suggests that the onset zone was missed. Fully understanding the structure-propagation relationship may eventually provide insight into selecting the correct targets for epilepsy surgery.
SEEG, diffusion MRI, seizure propagation, multi-modal epilepsy network, drug-resistant epilepsy
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© The Author(s) 2024. Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.
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