Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy
Journal article
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, ... Bernhardt, Boris C. (2022). Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy. Brain. 145(4), pp. 1285-1298. https://doi.org/10.1093/brain/awab417
Authors | 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 and Bernhardt, Boris C |
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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 |
Year | 2022 |
Journal | Brain |
Journal citation | 145 (4), pp. 1285-1298 |
Publisher | Oxford University Press |
ISSN | 0006-8950 |
Digital Object Identifier (DOI) | https://doi.org/10.1093/brain/awab417 |
PubMed ID | 35333312 |
Scopus EID | 2-s2.0-85132702732 |
PubMed Central ID | PMC9128824 |
Open access | Published as ‘gold’ (paid) open access |
Page range | 1285-1298 |
Funder | National Research Foundation of Korea |
Publisher's version | License File Access Level Open |
Output status | Published |
Publication dates | |
Online | 19 Nov 2021 |
Publication process dates | |
Accepted | 14 Aug 2021 |
Deposited | 18 Aug 2023 |
Grant ID | NRF-2021R1F1A1052303 |
2020–0-01389 | |
2021–0-02068 | |
IBS-R015-D1 | |
R01 NS110347 | |
2021XZZX006 | |
32171031 | |
IB201712 | |
IG200117 | |
181508 | |
MR/K013998/1 | |
2021XZZX006 | |
32171031 | |
NSERC Discovery-1304413 | |
FDN-154298 | |
PJT-174995 | |
NI17-039 | |
2013/07559–3 | |
NET-2013–02355313 | |
NIH/NINDS R21NS107739 | |
NIH/NINDS R01 NS122827 | |
NIH/NINDS R01 NS122827 | |
MRF1136427 |
https://acuresearchbank.acu.edu.au/item/8z8q8/topographic-divergence-of-atypical-cortical-asymmetry-and-atrophy-patterns-in-temporal-lobe-epilepsy
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Publisher's version
OA_Park_2022_Topographic_divergence_of_atypical_cortical_asymmetry.pdf | |
License: CC BY-NC 4.0 | |
File access level: Open |
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