Structural Connectivity Alterations in Operculo-Insular Epilepsy

Operculo-insular epilepsy (OIE) is an under-recognized condition that can mimic temporal and extratemporal epilepsies. Previous studies have revealed structural connectivity changes in the epileptic network of focal epilepsy. However, most reports use the debated streamline-count to quantify ‘connec...

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Main Authors: Sami Obaid, François Rheault, Manon Edde, Guido I. Guberman, Etienne St-Onge, Jasmeen Sidhu, Alain Bouthillier, Alessandro Daducci, Jimmy Ghaziri, Michel W. Bojanowski, Dang K. Nguyen, Maxime Descoteaux
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Brain Sciences
Subjects:
Online Access:https://www.mdpi.com/2076-3425/11/8/1041
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spelling doaj-b30c5c7fb3ad41b1afca5a99b68ab81c2021-08-26T13:34:37ZengMDPI AGBrain Sciences2076-34252021-08-01111041104110.3390/brainsci11081041Structural Connectivity Alterations in Operculo-Insular EpilepsySami Obaid0François Rheault1Manon Edde2Guido I. Guberman3Etienne St-Onge4Jasmeen Sidhu5Alain Bouthillier6Alessandro Daducci7Jimmy Ghaziri8Michel W. Bojanowski9Dang K. Nguyen10Maxime Descoteaux11Departement of Neurosciences, Université de Montréal, Montreal, QC H3C 3J7, CanadaSherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC J1K 0A5, CanadaSherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC J1K 0A5, CanadaSherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC J1K 0A5, CanadaSherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC J1K 0A5, CanadaSherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC J1K 0A5, CanadaCentre Hospitalier de l’Université de Montréal (CHUM), Division of Neurosurgery, Montreal, QC H2X 3E4, CanadaDepartment of Computer Science, University of Verona, 37134 Verona, ItalyCentre de Recherche du CHUM (CRCHUM), Montreal, QC H2X 0A9, CanadaCentre Hospitalier de l’Université de Montréal (CHUM), Division of Neurosurgery, Montreal, QC H2X 3E4, CanadaDepartement of Neurosciences, Université de Montréal, Montreal, QC H3C 3J7, CanadaSherbrooke Connectivity Imaging Lab (SCIL), Sherbrooke University, Sherbrooke, QC J1K 0A5, CanadaOperculo-insular epilepsy (OIE) is an under-recognized condition that can mimic temporal and extratemporal epilepsies. Previous studies have revealed structural connectivity changes in the epileptic network of focal epilepsy. However, most reports use the debated streamline-count to quantify ‘connectivity strength’ and rely on standard tracking algorithms. We propose a sophisticated cutting-edge method that is robust to crossing fibers, optimizes cortical coverage, and assigns an accurate microstructure-reflecting quantitative conectivity marker, namely the COMMIT (Convex Optimization Modeling for Microstructure Informed Tractography)-weight. Using our pipeline, we report the connectivity alterations in OIE. COMMIT-weighted matrices were created in all participants (nine patients with OIE, eight patients with temporal lobe epilepsy (TLE), and 22 healthy controls (HC)). In the OIE group, widespread increases in ‘connectivity strength’ were observed bilaterally. In OIE patients, ‘hyperconnections’ were observed between the insula and the pregenual cingulate gyrus (OIE group vs. HC group) and between insular subregions (OIE vs. TLE). Graph theoretic analyses revealed higher connectivity within insular subregions of OIE patients (OIE vs. TLE). We reveal, for the first time, the structural connectivity distribution in OIE. The observed pattern of connectivity in OIE likely reflects a diffuse epileptic network incorporating insular-connected regions and may represent a structural signature and diagnostic biomarker.https://www.mdpi.com/2076-3425/11/8/1041epilepsyinsulaoperculumconnectomediffusion magnetic resonance imagingtractography
collection DOAJ
language English
format Article
sources DOAJ
author Sami Obaid
François Rheault
Manon Edde
Guido I. Guberman
Etienne St-Onge
Jasmeen Sidhu
Alain Bouthillier
Alessandro Daducci
Jimmy Ghaziri
Michel W. Bojanowski
Dang K. Nguyen
Maxime Descoteaux
spellingShingle Sami Obaid
François Rheault
Manon Edde
Guido I. Guberman
Etienne St-Onge
Jasmeen Sidhu
Alain Bouthillier
Alessandro Daducci
Jimmy Ghaziri
Michel W. Bojanowski
Dang K. Nguyen
Maxime Descoteaux
Structural Connectivity Alterations in Operculo-Insular Epilepsy
Brain Sciences
epilepsy
insula
operculum
connectome
diffusion magnetic resonance imaging
tractography
author_facet Sami Obaid
François Rheault
Manon Edde
Guido I. Guberman
Etienne St-Onge
Jasmeen Sidhu
Alain Bouthillier
Alessandro Daducci
Jimmy Ghaziri
Michel W. Bojanowski
Dang K. Nguyen
Maxime Descoteaux
author_sort Sami Obaid
title Structural Connectivity Alterations in Operculo-Insular Epilepsy
title_short Structural Connectivity Alterations in Operculo-Insular Epilepsy
title_full Structural Connectivity Alterations in Operculo-Insular Epilepsy
title_fullStr Structural Connectivity Alterations in Operculo-Insular Epilepsy
title_full_unstemmed Structural Connectivity Alterations in Operculo-Insular Epilepsy
title_sort structural connectivity alterations in operculo-insular epilepsy
publisher MDPI AG
series Brain Sciences
issn 2076-3425
publishDate 2021-08-01
description Operculo-insular epilepsy (OIE) is an under-recognized condition that can mimic temporal and extratemporal epilepsies. Previous studies have revealed structural connectivity changes in the epileptic network of focal epilepsy. However, most reports use the debated streamline-count to quantify ‘connectivity strength’ and rely on standard tracking algorithms. We propose a sophisticated cutting-edge method that is robust to crossing fibers, optimizes cortical coverage, and assigns an accurate microstructure-reflecting quantitative conectivity marker, namely the COMMIT (Convex Optimization Modeling for Microstructure Informed Tractography)-weight. Using our pipeline, we report the connectivity alterations in OIE. COMMIT-weighted matrices were created in all participants (nine patients with OIE, eight patients with temporal lobe epilepsy (TLE), and 22 healthy controls (HC)). In the OIE group, widespread increases in ‘connectivity strength’ were observed bilaterally. In OIE patients, ‘hyperconnections’ were observed between the insula and the pregenual cingulate gyrus (OIE group vs. HC group) and between insular subregions (OIE vs. TLE). Graph theoretic analyses revealed higher connectivity within insular subregions of OIE patients (OIE vs. TLE). We reveal, for the first time, the structural connectivity distribution in OIE. The observed pattern of connectivity in OIE likely reflects a diffuse epileptic network incorporating insular-connected regions and may represent a structural signature and diagnostic biomarker.
topic epilepsy
insula
operculum
connectome
diffusion magnetic resonance imaging
tractography
url https://www.mdpi.com/2076-3425/11/8/1041
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