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ORIGINAL RESEARCH article

Front. Neurosci.
Sec. Translational Neuroscience
Volume 18 - 2024 | doi: 10.3389/fnins.2024.1424401

Evaluating Cortical Excitatory and Inhibitory Activity Through Interictal Intracranial Electroencephalography in Mesial Temporal Lobe Epilepsy

Provisionally accepted
Keisuke Nagata Keisuke Nagata 1*Naoto Kunii Naoto Kunii 2Shigeta Fujitani Shigeta Fujitani 1Seijiro Shimada Seijiro Shimada 1Nobuhito Saito Nobuhito Saito 1
  • 1 The University of Tokyo, Bunkyo, Tōkyō, Japan
  • 2 Jichi Medical University, Tochigi, Tochigi, Japan

The final, formatted version of the article will be published soon.

    Gamma oscillation regularity (GOR) indicates the synchronization of inhibitory interneurons, while the reactivity of cortico-cortical evoked potentials (CCEPs) is supposed to reflect local cortical excitability. Under the assumption that the early response of CCEP near the stimulation site also indicates excitatory activity primarily mediated by pyramidal cells, we aimed to visualize the cortical inhibitory and excitatory activities using GOR and CCEP in combination and to use them to predict the epileptogenic zone (EZ) in mesial temporal lobe epilepsy (MTLE). In five patients who underwent intracranial electrode implantation, GOR and CCEP reactivity in the vicinity of the stimulation site was quantified. The interictal GOR was calculated using multiscale entropy (MSE), the decrease of which was related to the enhanced GOR. These parameters were compared on an electrode-and-electrode basis, and spatially visualized on the brain surface. As a result, elevated GOR and CCEP reactivities, indicative of enhanced inhibitory and excitatory activities, were observed in the epileptogenic regions. Elevated CCEP reactivity was found to be localized to a restricted area centered on the seizure onset region, whereas GOR elevation was observed in a broader region surrounding it. Although these parameters independently predicted the EZ with high specificity, we combined the two to introduce a novel parameter, the excitatory and inhibitory (EI) index. The EI index predicted EZ with increased specificity compared with GOR or CCEP reactivity alone. Our results demonstrate that GOR and CCEP reactivity provided a quantitative visualization of the distribution of cortical inhibitory and excitatory activities and highlighted the relationship between the two parameters. The combination of GOR and CCEP reactivities are expected to serve as biomarkers for localizing the epileptogenic zone in MTLE from interictal intracranial electroencephalograms.

    Keywords: Excitatory and inhibitory balance, electrocorticogram, gamma oscillation regularity, multiscale entropy, Cortico-cortical evoked potential, epileptogenic zone

    Received: 28 Apr 2024; Accepted: 02 Sep 2024.

    Copyright: © 2024 Nagata, Kunii, Fujitani, Shimada and Saito. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

    * Correspondence: Keisuke Nagata, The University of Tokyo, Bunkyo, 113-8654, Tōkyō, Japan

    Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.