Functional connectome contractions in temporal lobe epilepsy: Microstructural underpinnings and predictors of surgical outcome.


Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
06 2020
Historique:
received: 16 01 2020
revised: 27 04 2020
accepted: 27 04 2020
pubmed: 27 5 2020
medline: 1 12 2020
entrez: 27 5 2020
Statut: ppublish

Résumé

Temporal lobe epilepsy (TLE) is the most common drug-resistant epilepsy in adults. Although it is commonly related to hippocampal pathology, increasing evidence suggests structural changes beyond the mesiotemporal lobe. Functional anomalies and their link to underlying structural alterations, however, remain incompletely understood. We studied 30 drug-resistant TLE patients and 57 healthy controls using multimodal magnetic resonance imaging (MRI) analyses. All patients had histologically verified hippocampal sclerosis and underwent postoperative imaging to outline the extent of their surgical resection. Our analysis leveraged a novel resting-state functional MRI framework that parameterizes functional connectivity distance, consolidating topological and physical properties of macroscale brain networks. Functional findings were integrated with morphological and microstructural metrics, and utility for surgical outcome prediction was assessed using machine learning techniques. Compared to controls, TLE patients showed connectivity distance reductions in temporoinsular and prefrontal networks, indicating topological segregation of functional networks. Testing for morphological and microstructural associations, we observed that functional connectivity contractions occurred independently from TLE-related cortical atrophy but were mediated by microstructural changes in the underlying white matter. Following our imaging study, all patients underwent an anterior temporal lobectomy as a treatment of their seizures, and postsurgical seizure outcome was determined at a follow-up at least 1 year after surgery. Using a regularized supervised machine learning paradigm with fivefold cross-validation, we demonstrated that patient-specific functional anomalies predicted postsurgical seizure outcome with 76 ± 4% accuracy, outperforming classifiers operating on clinical and structural imaging features. Our findings suggest connectivity distance contractions as a macroscale substrate of TLE. Functional topological isolation may represent a microstructurally mediated network mechanism that tilts the balance toward epileptogenesis in affected networks and that may assist in patient-specific surgical prognostication.

Identifiants

pubmed: 32452574
doi: 10.1111/epi.16540
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1221-1233

Subventions

Organisme : National Natural Science Foundation of China
ID : 81422022
Pays : International
Organisme : Hospital for Sick Children
ID : NI17-039
Pays : International
Organisme : Institute of Neurosciences, Mental Health and Addiction
ID : FDN-154298
Pays : International
Organisme : Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada
ID : 1304413
Pays : International

Informations de copyright

© 2020 International League Against Epilepsy.

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Auteurs

Sara Larivière (S)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Yifei Weng (Y)

Department of Medical Imaging, Jinling Hospital, Nanjing University School of Medicine, Nanjing, China.

Reinder Vos de Wael (R)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Jessica Royer (J)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Birgit Frauscher (B)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Zhengge Wang (Z)

Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Nanjing University Medical School, Nanjing, China.

Andrea Bernasconi (A)

Neuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Neda Bernasconi (N)

Neuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Dewi V Schrader (DV)

Department of Pediatrics, BC Children's Hospital, University of British Columbia, Vancouver, British Columbia, Canada.

Zhiqiang Zhang (Z)

Department of Medical Imaging, Jinling Hospital, Nanjing University School of Medicine, Nanjing, China.

Boris C Bernhardt (BC)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

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