Transition to seizure in focal epilepsy: From SEEG phenomenology to underlying mechanisms.

epilepsy fast‐onset activity ictal activity interictal‐ictal transition model‐based interpretation neural mass model pre‐ictal spikes synchronization pattern

Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
30 Oct 2024
Historique:
revised: 15 10 2024
received: 31 05 2024
accepted: 15 10 2024
medline: 30 10 2024
pubmed: 30 10 2024
entrez: 30 10 2024
Statut: aheadofprint

Résumé

For the pre-surgical evaluation of patients with drug-resistant focal epilepsy, stereo-electroencephalographic (SEEG) signals are routinely recorded to identify the epileptogenic zone network (EZN). This network consists of remote brain regions involved in seizure initiation. However, the pathophysiological mechanisms underlying typical SEEG patterns that occur during the transition from interictal to ictal activity in distant brain nodes of the EZN remain poorly understood. The primary aim is to identify and explain these mechanisms using a novel physiologically-plausible model of the EZN. We analyzed SEEG signals recorded from the EZN in 10 patients during the transition from interictal to ictal activity. This transition consisted of a sequence of periods during which SEEG signals from distant neocortical regions showed stereotypical patterns of activity: sustained preictal spiking activity preceding a fast activity occurring at seizure onset, followed by the ictal activity. Spectral content and non-linear correlation of SEEG signals were analyzed. In addition, we developed a novel neuro-inspired computational model consisting of bidirectionally coupled neuronal populations. The proposed model captured the essential characteristics of the patient signals, including the quasi-synchronous onset of rapid discharges in distant interconnected epileptogenic zones. Statistical analysis confirmed the dynamic correlation/de-decorrelation pattern observed in the patient signals and accurately reproduced in the simulated signals. This study provides insight into the abnormal dynamic changes in glutamatergic and γ-aminobutyric acid (GABA)ergic synaptic transmission that occur during the transition to seizures. The results strongly support the hypothesis that bidirectional connections between distant neuronal populations of the EZN (from pyramidal cells to vaso-intestinal peptide-positive interneurons) play a key role in this transition, while parvalbumin-positive interneurons intervene in the emergence of rapid discharges at seizure onset.

Identifiants

pubmed: 39474858
doi: 10.1111/epi.18173
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : H2020 European Research Council
ID : 855109

Informations de copyright

© 2024 The Author(s). Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

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Auteurs

Mehmet Alihan Kayabas (MA)

INSERM, LTSI U1099, Université de Rennes, Rennes, France.

Elif Köksal Ersöz (E)

INSERM, LTSI U1099, Université de Rennes, Rennes, France.

Maxime Yochum (M)

INSERM, LTSI U1099, Université de Rennes, Rennes, France.

Fabrice Bartolomei (F)

Epileptology and Cerebral Rhythmology, Timone Hospital, APHM, Marseille, France.
Univ Aix Marseille, INSERM, INS, Inst Neurosci Syst, Marseille, France.

Pascal Benquet (P)

INSERM, LTSI U1099, Université de Rennes, Rennes, France.

Fabrice Wendling (F)

INSERM, LTSI U1099, Université de Rennes, Rennes, France.

Classifications MeSH