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Multimodal mapping of regional brain vulnerability to focal cortical dysplasia

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Title
Multimodal mapping of regional brain vulnerability to focal cortical dysplasia
Author(s)
Lee, Hyo M.; Seok-Jun Hong; Gill, Ravnoor; Caldairou, Benoit; Wang, Irene; Zhang, Jian-Guo; Deleo, Francesco; Schrader, Dewi; Bartolomei, Fabrice; Guye, Maxime; Cho, Kyoo Ho; Barba, Carmen; Sisodiya, Sanjay; Jackson, Graeme; Hogan, R Edward; Wong-Kisiel, Lily; Cascino, Gregory D.; Schulze-Bonhage, Andreas; Lopes-Cendes, Iscia; Cendes, Fernando; Guerrini, Renzo; Bernhardt, Boris; Bernasconi, Neda; Bernasconi, Andrea
Publication Date
2023-08
Journal
Brain : a journal of neurology, v.146, no.8, pp.3404 - 3415
Publisher
NLM (Medline)
Abstract
Focal cortical dysplasia (FCD) type II is a highly epileptogenic developmental malformation and a common cause of surgically treated drug-resistant epilepsy. While clinical observations suggest frequent occurrence in the frontal lobe, mechanisms for such propensity remain unexplored. Here, we hypothesized that cortex-wide spatial associations of FCD distribution with cortical cytoarchitecture, gene expression and organizational axes may offer complementary insights into processes that predispose given cortical regions to harbour FCD. We mapped the cortex-wide MRI distribution of FCDs in 337 patients collected from 13 sites worldwide. We then determined its associations with (i) cytoarchitectural features using histological atlases by Von Economo and Koskinas and BigBrain; (ii) whole-brain gene expression and spatiotemporal dynamics from prenatal to adulthood stages using the Allen Human Brain Atlas and PsychENCODE BrainSpan; and (iii) macroscale developmental axes of cortical organization. FCD lesions were preferentially located in the prefrontal and fronto-limbic cortices typified by low neuron density, large soma and thick grey matter. Transcriptomic associations with FCD distribution uncovered a prenatal component related to neuroglial proliferation and differentiation, likely accounting for the dysplastic makeup, and a postnatal component related to synaptogenesis and circuit organization, possibly contributing to circuit-level hyperexcitability. FCD distribution showed a strong association with the anterior region of the antero-posterior axis derived from heritability analysis of interregional structural covariance of cortical thickness, but not with structural and functional hierarchical axes. Reliability of all results was confirmed through resampling techniques. Multimodal associations with cytoarchitecture, gene expression and axes of cortical organization indicate that prenatal neurogenesis and postnatal synaptogenesis may be key points of developmental vulnerability of the frontal lobe to FCD. Concordant with a causal role of atypical neuroglial proliferation and growth, our results indicate that FCD-vulnerable cortices display properties indicative of earlier termination of neurogenesis and initiation of cell growth. They also suggest a potential contribution of aberrant postnatal synaptogenesis and circuit development to FCD epileptogenicity. © The Author(s) 2023. Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
URI
https://pr.ibs.re.kr/handle/8788114/14375
DOI
10.1093/brain/awad060
ISSN
0006-8950
Appears in Collections:
Center for Neuroscience Imaging Research (뇌과학 이미징 연구단) > 1. Journal Papers (저널논문)
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