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Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy

Park, Bo-yong
Larivière, Sara
Rodríguez-Cruces, Raul
Royer, Jessica
Tavakol, Shahin
Wang, Yezhou
Caciagli, Lorenzo
Caligiuri, Maria Eugenia
Gambardella, Antonio
Concha, Luis
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Author
Park, Bo-yong
Larivière, Sara
Rodríguez-Cruces, Raul
Royer, Jessica
Tavakol, Shahin
Wang, Yezhou
Caciagli, Lorenzo
Caligiuri, Maria Eugenia
Gambardella, Antonio
Concha, Luis
Keller, Simon S
Cendes, Fernando
Alvim, Marina K M
Yasuda, Clarissa
Bonilha, Leonardo
Gleichgerrcht, Ezequiel
Focke, Niels K
Kreilkamp, Barbara A K
Domin, Martin
von Podewils, Felix
Langner, Soenke
Rummel, Christian
Rebsamen, Michael
Wiest, Roland
Martin, Pascal
Kotikalapudi, Raviteja
Bender, Benjamin
O’Brien, Terence J
Law, Meng
Sinclair, Benjamin
Vivash, Lucy
Kwan, Patrick
Desmond, Patricia M
Malpas, Charles B
Lui, Elaine
Alhusaini, Saud
Doherty, Colin P
Cavalleri, Gianpiero L
Delanty, Norman
Kälviäinen, Reetta
Jackson, Graeme D
Kowalczyk, Magdalena
Mascalchi, Mario
Semmelroch, Mira
Thomas, Rhys H
Soltanian-Zadeh, Hamid
Davoodi-Bojd, Esmaeil
Zhang, Junsong
Lenge, Matteo
Guerrini, Renzo
Bartolini, Emanuele
Hamandi, Khalid
Foley, Sonya
Weber, Bernd
Depondt, Chantal
Absil, Julie
Carr, Sarah J A
Abela, Eugenio
Richardson, Mark P
Devinsky, Orrin
Severino, Mariasavina
Striano, Pasquale
Parodi, Costanza
Tortora, Domenico
Hatton, Sean N
Vos, Sjoerd B
Duncan, John S
Galovic, Marian
Whelan, Christopher D
Bargalló, Núria
Pariente, Jose
Conde-Blanco, Estefania
Vaudano, Anna Elisabetta
Tondelli, Manuela
Meletti, Stefano
Kong, Xiang‐Zhen
Francks, Clyde
Fisher, Simon E
Caldairou, Benoit
Ryten, Mina
Labate, Angelo
Sisodiya, Sanjay M
Thompson, Paul M
McDonald, Carrie R
Bernasconi, Andrea
Bernasconi, Neda
Bernhardt, Boris C
Abstract
Temporal lobe epilepsy, a common drug-resistant epilepsy in adults, is primarily a limbic network disorder associated with predominant unilateral hippocampal pathology. Structural MRI has provided an in vivo window into whole-brain grey matter structural alterations in temporal lobe epilepsy relative to controls, by either mapping (i) atypical inter-hemispheric asymmetry; or (ii) regional atrophy. However, similarities and differences of both atypical asymmetry and regional atrophy measures have not been systematically investigated. Here, we addressed this gap using the multisite ENIGMA-Epilepsy dataset comprising MRI brain morphological measures in 732 temporal lobe epilepsy patients and 1418 healthy controls. We compared spatial distributions of grey matter asymmetry and atrophy in temporal lobe epilepsy, contextualized their topographies relative to spatial gradients in cortical microstructure and functional connectivity calculated using 207 healthy controls obtained from Human Connectome Project and an independent dataset containing 23 temporal lobe epilepsy patients and 53 healthy controls and examined clinical associations using machine learning. We identified a marked divergence in the spatial distribution of atypical inter-hemispheric asymmetry and regional atrophy mapping. The former revealed a temporo-limbic disease signature while the latter showed diffuse and bilateral patterns. Our findings were robust across individual sites and patients. Cortical atrophy was significantly correlated with disease duration and age at seizure onset, while degrees of asymmetry did not show a significant relationship to these clinical variables. Our findings highlight that the mapping of atypical inter-hemispheric asymmetry and regional atrophy tap into two complementary aspects of temporal lobe epilepsy-related pathology, with the former revealing primary substrates in ipsilateral limbic circuits and the latter capturing bilateral disease effects. These findings refine our notion of the neuropathology of temporal lobe epilepsy and may inform future discovery and validation of complementary MRI biomarkers in temporal lobe epilepsy.
Keywords
temporal lobe epilepsy, asymmetry, cortical thickness, multi-site, gradients
Date
2022
Type
Journal article
Journal
Brain
Book
Volume
145
Issue
4
Page Range
1285-1298
Article Number
ACU Department
School of Behavioural and Health Sciences
Faculty of Health Sciences
Relation URI
Source URL
Event URL
Open Access Status
Published as ‘gold’ (paid) open access
License
CC BY-NC 4.0
File Access
Open
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