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Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy

Objective: Perceptual alternations evoked by binocular rivalry (BR) reflect cortical dynamics strongly dependent on the excitatory–inhibitory balance, suggesting potential utility as a biomarker for epileptogenesis. Therefore, we investigated the characteristics of BR in patients with idiopathic gen...

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Autores principales: Wu, Jiaonan, Ding, Wei, Ye, Xing, Wei, Qiang, Lv, Xinyi, Tang, Qiqiang, Tian, Yanghua, Wang, Kai, Jiang, Yubao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8634877/
https://www.ncbi.nlm.nih.gov/pubmed/34867711
http://dx.doi.org/10.3389/fneur.2021.720126
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author Wu, Jiaonan
Ding, Wei
Ye, Xing
Wei, Qiang
Lv, Xinyi
Tang, Qiqiang
Tian, Yanghua
Wang, Kai
Jiang, Yubao
author_facet Wu, Jiaonan
Ding, Wei
Ye, Xing
Wei, Qiang
Lv, Xinyi
Tang, Qiqiang
Tian, Yanghua
Wang, Kai
Jiang, Yubao
author_sort Wu, Jiaonan
collection PubMed
description Objective: Perceptual alternations evoked by binocular rivalry (BR) reflect cortical dynamics strongly dependent on the excitatory–inhibitory balance, suggesting potential utility as a biomarker for epileptogenesis. Therefore, we investigated the characteristics of BR in patients with idiopathic generalized epilepsy (IGE) and potential associations with clinical variables. Methods: Sixty-two healthy controls (HCs) and 94 IGE patients completed BR task. Perceptual alternation rates were compared between HC and IGE groups as well as among the HC group and IGE patients stratified according to the presence or absence of interictal activity on the ambulatory electroencephalogram (EEG), termed the abnormal ambulatory EEG group (AB-AEEG, n = 64) and normal ambulatory EEG group (N-AEEG, n = 30), respectively. Results: The IGE patients demonstrated a slower rate of BR perceptual alternation than HC subjects (t = −4.364, p < 0.001). The alternation rate also differed among the HC, AB-AEEG, and N-AEEG groups (F = 44.962, df = 2, p < 0.001), and post hoc comparisons indicated a significantly slower alternation rate in the AB-AEEG group compared with the N-AEEG and HC groups (0.28 vs. 0.46, and 0.43 Hz). Stepwise linear regression revealed positive correlations between the BR alternation rate and both the ambulatory EEG status (β, 0.173; standard error, 0.022 p < 0.001) and Montreal Cognitive Assessment score (β, 0.013; standard error, 0.004; p = 0.003). Receiver operating characteristic curve analysis of the BR alternation rate distinguished AB-AEEG from N-AEEG subjects with 90.00% sensitivity and 76.90% specificity (area under the curve = 0.881; 95% confidence interval = 0.801– 0.961, cut-off = 0.319). Alternatively, Montreal Cognitive Assessment score did not accurately distinguish AB-AEEG from N-AEEG subjects and the area under the receiver operating characteristic curve combining the BR alternation rate and Montreal Cognitive Assessment score was not markedly larger than that of the BR alternation rate alone (0.894, 95% confidence interval = 0.822–0.966, p < 0.001). K-fold cross-validation was used to evaluate the predictive performance of BR alternation rate, MoCA score, and the combination of both, which yielded average AUC values of 0.870, 0.584 and 0.847, average sensitivity values of 89.36, 92.73, and 91.28%, and average specificity values of 62.25, 13.42, and 61.78%, respectively. The number of interictal epileptiform discharges was significantly correlated with the alternation rate in IGE patients (r = 0.296, p = 0.018). A forward stepwise linear regression model identified the number of interictal epileptiform discharges (β, 0.001; standard error, 0.001; p = 0.025) as an independent factor associated with BR alternation rate in these patients. Conclusion: These results suggest that interictal epileptiform discharges are associated with disruptions in perceptual awareness, and that the BR may be a useful auxiliary behavioral task to diagnosis and dynamically monitor IGE patients with interictal discharge.
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spelling pubmed-86348772021-12-02 Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy Wu, Jiaonan Ding, Wei Ye, Xing Wei, Qiang Lv, Xinyi Tang, Qiqiang Tian, Yanghua Wang, Kai Jiang, Yubao Front Neurol Neurology Objective: Perceptual alternations evoked by binocular rivalry (BR) reflect cortical dynamics strongly dependent on the excitatory–inhibitory balance, suggesting potential utility as a biomarker for epileptogenesis. Therefore, we investigated the characteristics of BR in patients with idiopathic generalized epilepsy (IGE) and potential associations with clinical variables. Methods: Sixty-two healthy controls (HCs) and 94 IGE patients completed BR task. Perceptual alternation rates were compared between HC and IGE groups as well as among the HC group and IGE patients stratified according to the presence or absence of interictal activity on the ambulatory electroencephalogram (EEG), termed the abnormal ambulatory EEG group (AB-AEEG, n = 64) and normal ambulatory EEG group (N-AEEG, n = 30), respectively. Results: The IGE patients demonstrated a slower rate of BR perceptual alternation than HC subjects (t = −4.364, p < 0.001). The alternation rate also differed among the HC, AB-AEEG, and N-AEEG groups (F = 44.962, df = 2, p < 0.001), and post hoc comparisons indicated a significantly slower alternation rate in the AB-AEEG group compared with the N-AEEG and HC groups (0.28 vs. 0.46, and 0.43 Hz). Stepwise linear regression revealed positive correlations between the BR alternation rate and both the ambulatory EEG status (β, 0.173; standard error, 0.022 p < 0.001) and Montreal Cognitive Assessment score (β, 0.013; standard error, 0.004; p = 0.003). Receiver operating characteristic curve analysis of the BR alternation rate distinguished AB-AEEG from N-AEEG subjects with 90.00% sensitivity and 76.90% specificity (area under the curve = 0.881; 95% confidence interval = 0.801– 0.961, cut-off = 0.319). Alternatively, Montreal Cognitive Assessment score did not accurately distinguish AB-AEEG from N-AEEG subjects and the area under the receiver operating characteristic curve combining the BR alternation rate and Montreal Cognitive Assessment score was not markedly larger than that of the BR alternation rate alone (0.894, 95% confidence interval = 0.822–0.966, p < 0.001). K-fold cross-validation was used to evaluate the predictive performance of BR alternation rate, MoCA score, and the combination of both, which yielded average AUC values of 0.870, 0.584 and 0.847, average sensitivity values of 89.36, 92.73, and 91.28%, and average specificity values of 62.25, 13.42, and 61.78%, respectively. The number of interictal epileptiform discharges was significantly correlated with the alternation rate in IGE patients (r = 0.296, p = 0.018). A forward stepwise linear regression model identified the number of interictal epileptiform discharges (β, 0.001; standard error, 0.001; p = 0.025) as an independent factor associated with BR alternation rate in these patients. Conclusion: These results suggest that interictal epileptiform discharges are associated with disruptions in perceptual awareness, and that the BR may be a useful auxiliary behavioral task to diagnosis and dynamically monitor IGE patients with interictal discharge. Frontiers Media S.A. 2021-11-10 /pmc/articles/PMC8634877/ /pubmed/34867711 http://dx.doi.org/10.3389/fneur.2021.720126 Text en Copyright © 2021 Wu, Ding, Ye, Wei, Lv, Tang, Tian, Wang and Jiang. https://creativecommons.org/licenses/by/4.0/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) and the copyright owner(s) 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.
spellingShingle Neurology
Wu, Jiaonan
Ding, Wei
Ye, Xing
Wei, Qiang
Lv, Xinyi
Tang, Qiqiang
Tian, Yanghua
Wang, Kai
Jiang, Yubao
Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
title Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
title_full Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
title_fullStr Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
title_full_unstemmed Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
title_short Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
title_sort interictal activity is associated with slower binocular rivalry in idiopathic generalized epilepsy
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8634877/
https://www.ncbi.nlm.nih.gov/pubmed/34867711
http://dx.doi.org/10.3389/fneur.2021.720126
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