Is High‐Frequency Activity at Seizure Onset Inhibitory? A Stereoelectroencephalographic Study of Motor Cortex Seizures

Author:

Shaker Hussam1ORCID,Li Jian23ORCID,Kobayashi Masako4,Grinenko Olesya1ORCID,Bulacio Juan5ORCID,Leahy Richard M.6ORCID,Chauvel Patrick7ORCID

Affiliation:

1. Epilepsy Center Trinity Health Hauenstein Center Grand Rapids MI USA

2. Athinoula A. Martinos Center for Biomedical Imaging Massachusetts General Hospital and Harvard Medical School Charlestown MA USA

3. Center for Neurotechnology and Neurorecovery, Department of Neurology Massachusetts General Hospital and Harvard Medical School Boston MA USA

4. Department of Neurology Kyoto University Graduate School of Medicine Kyoto Japan

5. Epilepsy Center Cleveland Clinic Neurological Institute Cleveland OH USA

6. Signal and Image Processing Institute University of Southern California Los Angeles CA USA

7. Neurological Institute Cleveland Clinic Cleveland OH USA

Abstract

ObjectiveIn the era of stereoelectroencephalography (SEEG), many studies have been devoted to understanding the role of interictal high‐frequency oscillations. High‐frequency activity (HFA) at seizure onset has been identified as a marker of epileptogenic zone. We address the physiological significance of ictal HFAs and their relation to clinical semiology.MethodsWe retrospectively identified patients with pure focal primary motor epilepsy. We selected only patients in whom SEEG electrodes were optimally placed in the motor cortex as confirmed by electrical stimulation. Based on these narrow inclusion criteria, we extensively studied 5 patients (3 males and 2 females, mean age = 22.4 years) using time–frequency analysis and time correlation with motor signs onset.ResultsA total of 157 analyzable seizures were recorded in 5 subjects. The first 2 subjects had tonic or clonic semiology with rare secondary generalization. Subject 3 had atonic onset followed by clonic hand/arm flexion. Subject 4 had clusters of tonic and atonic facial movements. Subject 5 had upper extremity tonic movements. The median frequency of the fast activity extracted from the Epileptogenic Zone Fingerprint pipeline in the first 4 subjects was 76 Hz (interquartile range = 21.9Hz). Positive motor signs did not occur concomitantly with high gamma activity developing in the motor cortex. Motor signs began at the end of HFAs.InterpretationThis study supports the hypothesis of an inhibitory effect of ictal HFAs. The frequency range in the gamma band was associated with the direction of the clinical output effect. Changes from inhibitory to excitatory effect occurred when discharge frequency dropped to low gamma or beta. ANN NEUROL 2024;95:1127–1137

Funder

National Institute of Biomedical Imaging and Bioengineering

National Institute of Neurological Disorders and Stroke

Publisher

Wiley

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