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  Temporal lobe epilepsy perturbs the brain‐wide excitation‐inhibition balance: Associations with microcircuit organization, clinical parameters, and cognitive dysfunction

Xie, K., Royer, J., Rodriguez‐Cruces, R., Horwood, L., Ngo, A., Arafat, T., et al. (2025). Temporal lobe epilepsy perturbs the brain‐wide excitation‐inhibition balance: Associations with microcircuit organization, clinical parameters, and cognitive dysfunction. Advanced Science, 12(9): e2406835. doi:10.1002/advs.202406835.

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Item Permalink: https://hdl.handle.net/21.11116/0000-0010-7D19-7 Version Permalink: https://hdl.handle.net/21.11116/0000-0010-DCFE-9
Genre: Journal Article

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 Creators:
Xie, Ke1, Author
Royer, Jessica1, Author
Rodriguez‐Cruces, Raul1, Author
Horwood, Linda1, Author
Ngo, Alexander1, Author
Arafat, Thaera1, Author
Auer, Hans1, Author
Sahlas, Ella1, Author
Chen, Judy1, Author
Zhou, Yigu1, Author
Valk, Sofie L.2, 3, 4, Author                 
Hong, Seok‐Jun5, 6, 7, Author
Frauscher, Birgit8, Author
Pana, Raluca9, Author
Bernasconi, Andrea1, Author
Bernasconi, Neda1, Author
Concha, Luis10, Author
Bernhardt, Boris C.1, Author
Affiliations:
1McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, QC, Canada, ou_persistent22              
2Otto Hahn Group Cognitive Neurogenetics, MPI for Human Cognitive and Brain Sciences, Max Planck Society, ou_3222264              
3Institute of Neuroscience and Medicine (INM-7), Brain and Behavior, Research Center Jülich, Germany, ou_persistent22              
4Institute of Systems Neuroscience, University Hospital Düsseldorf, Germany, ou_persistent22              
5Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon, Republic of Korea, ou_persistent22              
6Department of Biomedical Engineering, Sungkyunkwan University, Suwon, Republic of Korea, ou_persistent22              
7Center for the Developing Brain, Child Mind Institute, New York, NY, USA, ou_persistent22              
8Department of Biomedical Engineering, Duke University, Durham, NC, USA, ou_persistent22              
9Montreal Neurological Institute and Hospital, McGill University, QC, Canada, ou_persistent22              
10Institute of Neurobiology, Universidad Nacional Autónoma de Mexico, Queretaro, Mexico, ou_persistent22              

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Free keywords: Cognitive impairment; Excitation/inhibition imbalance; Microcircuit perturbation; Multimodal MRI; Temporal lobe epilepsy
 Abstract: Excitation-inhibition (E/I) imbalance is theorized as a key mechanism in the pathophysiology of epilepsy, with ample research focusing on elucidating its cellular manifestations. However, few studies investigate E/I imbalance at the macroscale, whole-brain level, and its microcircuit-level mechanisms and clinical significance remain incompletely understood. Here, the Hurst exponent, an index of the E/I ratio, is computed from resting-state fMRI time series, and microcircuit parameters are simulated using biophysical models. A broad decrease in the Hurst exponent is observed in pharmaco-resistant temporal lobe epilepsy (TLE), suggesting more excitable network dynamics. Connectome decoders point to temporolimbic and frontocentral cortices as plausible network epicenters of E/I imbalance. Furthermore, computational simulations reveal that enhancing cortical excitability in TLE reflects atypical increases in recurrent connection strength of local neuronal ensembles. Mixed cross-sectional and longitudinal analyses show stronger E/I ratio elevation in patients with longer disease duration, more frequent electroclinical seizures as well as interictal epileptic spikes, and worse cognitive functioning. Hurst exponent-informed classifiers discriminate patients from healthy controls with high accuracy (72.4% [57.5%-82.5%]). Replicated in an independent dataset, this work provides in vivo evidence of a macroscale shift in E/I balance in TLE patients and points to progressive functional imbalances that relate to cognitive decline.

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Language(s): eng - English
 Dates: 2024-10-232024-06-192025-01-132025-03
 Publication Status: Issued
 Pages: -
 Publishing info: -
 Table of Contents: -
 Rev. Type: -
 Identifiers: DOI: 10.1002/advs.202406835
Other: epub 2025
PMID: 39806576
 Degree: -

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Project name : -
Grant ID : CSC-202006070175
Funding program : -
Funding organization : China Scholarship Council
Project name : -
Grant ID : FDN-154298; PJT-174995
Funding program : -
Funding organization : Canadian Institutes of Health Research (CIHR)
Project name : -
Grant ID : IB201712; IG200117; IN204720; IN213423
Funding program : -
Funding organization : Dirección General de Asuntos del Personal Académico (DGAPA)
Project name : -
Grant ID : Discovery-1304413
Funding program : -
Funding organization : National Science and Engineering Research Council of Canada (NSERC)
Project name : -
Grant ID : NI17-039
Funding program : -
Funding organization : SickKids Foundation
Project name : -
Grant ID : 181508; 1782; FC218-2023
Funding program : -
Funding organization : Consejo Nacional de Ciencia y Tecnología
Project name : -
Grant ID : IBS-R015-D1
Funding program : -
Funding organization : Institute for Basic Science of Korea
Project name : -
Grant ID : NRF-2022R1C1C1007095; R5-2023-00217361; RS-2024-00398768
Funding program : -
Funding organization : National Research Foundation of Korea (NRF)

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Title: Advanced Science
  Other : Adv. Sci.
Source Genre: Journal
 Creator(s):
Affiliations:
Publ. Info: Weinheim : Wiley-VCH
Pages: - Volume / Issue: 12 (9) Sequence Number: e2406835 Start / End Page: - Identifier: ISSN: 2198-3844
CoNE: https://pure.mpg.de/cone/journals/resource/2198-3844