Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG

Functional connectivity analysis of intracranial electroencephalography (iEEG) plays an important role in understanding the mechanism of epilepsy and seizure dynamics. However, existing connectivity analysis is only suitable for low-frequency bands below 80 Hz. High-frequency oscillations (HFOs) and...

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Main Authors: Mu Shen, Lin Zhang, Yi Gong, Lei Li, Xianzeng Liu
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:Bioengineering
Subjects:
Online Access:https://www.mdpi.com/2306-5354/10/4/461
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author Mu Shen
Lin Zhang
Yi Gong
Lei Li
Xianzeng Liu
author_facet Mu Shen
Lin Zhang
Yi Gong
Lei Li
Xianzeng Liu
author_sort Mu Shen
collection DOAJ
description Functional connectivity analysis of intracranial electroencephalography (iEEG) plays an important role in understanding the mechanism of epilepsy and seizure dynamics. However, existing connectivity analysis is only suitable for low-frequency bands below 80 Hz. High-frequency oscillations (HFOs) and high-frequency activity (HFA) in the high-frequency band (80–500 Hz) are thought to be specific biomarkers in epileptic tissue localization. However, the transience in duration and variability of occurrence time and amplitudes of these events pose a challenge for conducting effective connectivity analysis. To deal with this problem, we proposed skewness-based functional connectivity (SFC) in the high-frequency band and explored its utility in epileptic tissue localization and surgical outcome evaluation. SFC comprises three main steps. The first step is the quantitative measurement of amplitude distribution asymmetry between HFOs/HFA and baseline activity. The second step is functional network construction on the basis of rank correlation of asymmetry across time. The third step is connectivity strength extraction from the functional network. Experiments were conducted in two separate datasets which consist of iEEG recordings from 59 patients with drug-resistant epilepsy. Significant difference (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><mi>p</mi><mo><</mo><mn>0.001</mn></mrow></semantics></math></inline-formula>) in connectivity strength was found between epileptic and non-epileptic tissue. Results were quantified via the receiver operating characteristic curve and the area under the curve (AUC). Compared with low-frequency bands, SFC demonstrated superior performance. With respect to pooled and individual epileptic tissue localization for seizure-free patients, AUCs were 0.66 (95% confidence interval (CI): 0.63–0.69) and (0.63 95% CI 0.56–0.71), respectively. For surgical outcome classification, the AUC was 0.75 (95% CI 0.59–0.85). Therefore, SFC can act as a promising assessment tool in characterizing the epileptic network and potentially provide better treatment options for patients with drug-resistant epilepsy.
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spelling doaj.art-9e7442de63474bc2b9d459ec4aed342b2023-11-17T18:22:25ZengMDPI AGBioengineering2306-53542023-04-0110446110.3390/bioengineering10040461Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEGMu Shen0Lin Zhang1Yi Gong2Lei Li3Xianzeng Liu4School of Artificial Intelligence, Beijing University of Posts and Telecommunications, Beijing 100876, ChinaSchool of Artificial Intelligence, Beijing University of Posts and Telecommunications, Beijing 100876, ChinaSchool of Information and Communication Engineering, Beijing Information Science and Technology University, Beijing 100096, ChinaSchool of Artificial Intelligence, Beijing University of Posts and Telecommunications, Beijing 100876, ChinaDepartment of Neurology, Peking University International Hospital, and Peking University Clinical Research Institute, Beijing 102206, ChinaFunctional connectivity analysis of intracranial electroencephalography (iEEG) plays an important role in understanding the mechanism of epilepsy and seizure dynamics. However, existing connectivity analysis is only suitable for low-frequency bands below 80 Hz. High-frequency oscillations (HFOs) and high-frequency activity (HFA) in the high-frequency band (80–500 Hz) are thought to be specific biomarkers in epileptic tissue localization. However, the transience in duration and variability of occurrence time and amplitudes of these events pose a challenge for conducting effective connectivity analysis. To deal with this problem, we proposed skewness-based functional connectivity (SFC) in the high-frequency band and explored its utility in epileptic tissue localization and surgical outcome evaluation. SFC comprises three main steps. The first step is the quantitative measurement of amplitude distribution asymmetry between HFOs/HFA and baseline activity. The second step is functional network construction on the basis of rank correlation of asymmetry across time. The third step is connectivity strength extraction from the functional network. Experiments were conducted in two separate datasets which consist of iEEG recordings from 59 patients with drug-resistant epilepsy. Significant difference (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><mi>p</mi><mo><</mo><mn>0.001</mn></mrow></semantics></math></inline-formula>) in connectivity strength was found between epileptic and non-epileptic tissue. Results were quantified via the receiver operating characteristic curve and the area under the curve (AUC). Compared with low-frequency bands, SFC demonstrated superior performance. With respect to pooled and individual epileptic tissue localization for seizure-free patients, AUCs were 0.66 (95% confidence interval (CI): 0.63–0.69) and (0.63 95% CI 0.56–0.71), respectively. For surgical outcome classification, the AUC was 0.75 (95% CI 0.59–0.85). Therefore, SFC can act as a promising assessment tool in characterizing the epileptic network and potentially provide better treatment options for patients with drug-resistant epilepsy.https://www.mdpi.com/2306-5354/10/4/461connectivityepilepsyhigh-frequency activityhigh-frequency oscillationsintracranial EEGlocalization
spellingShingle Mu Shen
Lin Zhang
Yi Gong
Lei Li
Xianzeng Liu
Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG
Bioengineering
connectivity
epilepsy
high-frequency activity
high-frequency oscillations
intracranial EEG
localization
title Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG
title_full Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG
title_fullStr Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG
title_full_unstemmed Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG
title_short Epileptic Tissue Localization through Skewness-Based Functional Connectivity in the High-Frequency Band of Intracranial EEG
title_sort epileptic tissue localization through skewness based functional connectivity in the high frequency band of intracranial eeg
topic connectivity
epilepsy
high-frequency activity
high-frequency oscillations
intracranial EEG
localization
url https://www.mdpi.com/2306-5354/10/4/461
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AT yigong epileptictissuelocalizationthroughskewnessbasedfunctionalconnectivityinthehighfrequencybandofintracranialeeg
AT leili epileptictissuelocalizationthroughskewnessbasedfunctionalconnectivityinthehighfrequencybandofintracranialeeg
AT xianzengliu epileptictissuelocalizationthroughskewnessbasedfunctionalconnectivityinthehighfrequencybandofintracranialeeg