Visualization of ictal networks using gamma oscillation regularity correlation analysis in focal motor epilepsy: Illustrative cases
- Department of Neurosurgery, Showa University School of Medicine, Shinagawa-ku, Japan.
Yosuke Sato, Department of Neurosurgery, Showa University School of Medicine, Shinagawa-ku, Japan.
DOI:10.25259/SNI_193_2022Copyright: © 2022 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Tomonobu Nakamura, Yosuke Sato, Yusuke Kobayashi, Yuta Kawauchi, Katsuyoshi Shimizu, Tohru Mizutani. Visualization of ictal networks using gamma oscillation regularity correlation analysis in focal motor epilepsy: Illustrative cases. 25-Mar-2022;13:105
How to cite this URL: Tomonobu Nakamura, Yosuke Sato, Yusuke Kobayashi, Yuta Kawauchi, Katsuyoshi Shimizu, Tohru Mizutani. Visualization of ictal networks using gamma oscillation regularity correlation analysis in focal motor epilepsy: Illustrative cases. 25-Mar-2022;13:105. Available from: https://surgicalneurologyint.com/surgicalint-articles/11485/
Background: Focal motor epilepsy is difficult to localize within the epileptogenic zone because ictal activity quickly spreads to the motor cortex through ictal networks. We previously reported the usefulness of gamma oscillation (30–70 Hz) regularity (GOR) correlation analysis using interictal electrocorticographic (ECoG) data to depict epileptogenic networks. We conducted GOR correlation analysis using ictal ECoG data to visualize the ictal networks originating from the epileptogenic zone in two cases — a 26-year-old woman with negative motor seizures and a 53-year-old man with supplementary motor area (SMA) seizures.
Case Description: In both cases, we captured several habitual seizures during monitoring after subdural electrode implantation and performed GOR correlation analysis using ictal ECoG data. A significantly high GOR suggestive of epileptogenicity was identified in the SMA ipsilateral to the lesions, which were connected to the motor cortex through supposed ictal networks. We resected the high GOR locations in the SMA and the patients’ previously identified tumors were removed. The patients were seizure-free without any neurological deficits after surgery.
Conclusion: The GOR correlation analysis using ictal ECoG data could be a powerful tool for visualizing ictal networks in focal motor epilepsy.
Keywords: Epilepsy surgery, Gamma oscillation regularity, Ictal motor networks, Negative motor seizure, Supplementary motor area seizure
Focal motor epilepsy typically involves swift and complex motor behaviors,[
In view of the context of epilepsy as a network disorder,[
The patient was a 26-year-old woman who experienced an indescribable aura and subsequent atonic seizures in the right hemibody without loss of consciousness for more than 5 years, which was considered to be NMS. Contrast-enhanced magnetic resonance imaging (MRI) showed a 27 × 21 mm tumor within the left frontal lobe in contact with the SMA. The tumor comprised solid and cystic components and no calcification was observed [
Illustrative results of Case 1. (a) Preoperative contrast-enhanced magnetic resonance imaging shows a tumor in the left mesial frontal lobe. (b) Iomazenil single-photon emission computed tomography shows decreased accumulation in the left prefrontal cortex. (c) Intracranial electrocorticographic (ECoG) monitoring shows seizre onset zone (SOZ) at electrode 12, and right-hand motor areas at electrodes 3, 4, 5, 9, 10, 14, and 15. (d) Interictal ECoG shows spikes at electrodes 12 and 13. (e) Gamma oscillation (30–70 Hz) regularity (GOR) analysis with interictal ECoG data reveals significantly high GOR at electrodes 7, 8, 12, and 13. (f) Ictal ECoG shows spikes at electrode 12, which spread into electrodes 7, 8, and 13. (g) GOR correlation analysis with ictal ECoG data reveals ictal networks between the epileptogenic focus (electrodes 7, 8, 12, and 13) and ipsilateral motor cortex (electrodes 3, 9, and 14). (h) The epileptogenic focus (electrodes 7, 8, 12, and 13) within the supplementary motor area was resected, and the tumor was subsequently removed.
The patient underwent cortical resection of the epileptogenic focus (electrodes 7, 8, 12, and 13) within the SMA and subsequent tumor removal [
The patient was a 53-year-old man who experienced short tonic posturing of the left hand for over 2 years. Contrast-enhanced MRI showed a 9.2 × 9.4 mm tumor at the right mesial frontal lobe, and high intensity was seen in fluid-attenuated inversion recovery (FLAIR) images [
Illustrative results of Case 2. (a) Preoperative contrast-enhanced magnetic resonance imaging shows a tumor at the right mesial frontal lobe. (b) Iomazenil single-photon emission computed tomography shows slightly decreased accumulation in the right mesial frontal cortex. (c) Intracranial electrocorticographic (ECoG) monitoring shows SOZ at electrodes 21 and 22 on the right mesial frontal cortex and left-hand motor areas at electrodes 11, 12, 17, and 18 on the lateral frontal cortex. (d) Interictal ECoG shows spikes at electrodes 21 and 22. (e) Gamma oscillation (30–70 Hz) regularity (GOR) analysis with interictal ECoG data reveals significantly high GOR at electrodes 21 and 22. (f) Ictal ECoG shows spikes at electrodes 21 and 22, which spread into electrodes 12, 13, 14, 17, 18, and 19. (g) GOR correlation analysis with ictal ECoG data reveals ictal networks between the epileptogenic focus (electrode 22) and ipsilateral premotor cortex (electrode 19) and motor cortex (electrode 12). (h) The epileptogenic focus (electrodes 21 and 22) within the supplementary motor area was removed.
ECoG data recordings
ECoG data were recorded using a Nihon Kohden Neurofax EEG system (Nihon Kohden, Tokyo, Japan) with a bandpass filter from 0.16 to 300 Hz with a sampling rate of 1 kHz. A 60-Hz notch filter was applied to all channels and the sensitivity was between 30 and 100 µV/mm according to the amplitudes of the background activities and epileptic discharges. Recordings were obtained using a reference electrode placed on the forehead. All selected ECoG epochs were inspected to ensure that they were not contaminated by artifacts.
The detailed algorithm employed for GOR analysis using the sample entropy method has been described in the previous studies.[
Sij is the covariance of electrodes i and j, and Si is the standard deviation of electrode i. In the network diagram, the threshold was set to 0.7 in this case. The edge was placed between nodes i and j when rij = 0.7. We weighted the threshold between 0.7 and 1 linearly with the thickness of the edge. To visually assess the GOR, we color-coded the average GOR over 10 s. These procedures were performed using a custom program developed in cooperation with EFken Inc. (Tokyo, Japan).
Focal motor epilepsy is difficult to diagnose because of its very rapid propagation, and abnormalities in scalp EEG often remain undetected.[
We previously reported the usefulness of GOR analysis in locating the epileptogenic focus[
The brain’s U-fibers, which connect the neighboring cortical regions,[
A limitation of this study is that the networks are presented as an undirected graph; hence, the direction of the seizure propagation cannot be strictly evaluated. As we were able to show that there is a connection between the epileptogenic focus and the motor areas as symptomatic zones and that the removal of such epileptogenic foci resulted in liberation from seizures, we can only indirectly understand that seizure activities start from the epileptogenic focus and subsequently propagate to the motor areas. To solve this problem, we are currently developing a GOR correlation analysis to depict visualized networks as a directed graph. In addition, ECoG data can only be used for planar network analysis. Our goal is to use SEEG data with our GOR correlation analysis to enable three-dimensional network depiction for more minimally invasive epilepsy surgery.
GOR correlation analysis using ictal ECoG data as described here could be a very useful method for visualizing ictal networks in focal motor epilepsy.
Data availability statement
The raw data supporting this article will be made available by the authors, without undue reservation.
Declaration of patient consent
Institutional Review Board (IRB) permission obtained for the study.
Financial support and sponsorship
JSPS KAKENHI Grant Number JP 20K09356.
Conflicts of interest
There are no conflicts of interest.
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