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: Jiaonan Wu, Wei Ding, Xing Ye, Qiang Wei, Xinyi Lv, Qiqiang Tang, Yanghua Tian, Kai Wang, Yubao Jiang
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:0e5f279300ff4b50be72aa3b00e9e2a52021-11-15T14:03:54ZInterictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy1664-229510.3389/fneur.2021.720126https://doaj.org/article/0e5f279300ff4b50be72aa3b00e9e2a52021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fneur.2021.720126/fullhttps://doaj.org/toc/1664-2295Objective: 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.Jiaonan WuJiaonan WuWei DingXing YeXing YeQiang WeiQiang WeiXinyi LvQiqiang TangQiqiang TangYanghua TianYanghua TianKai WangKai WangYubao JiangYubao JiangFrontiers Media S.A.articlebinocular rivalryidiopathic generalized epilepsyelectroencephalogramexcitatory neurotransmitterinhibitory neurotransmitterNeurology. Diseases of the nervous systemRC346-429ENFrontiers in Neurology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic binocular rivalry
idiopathic generalized epilepsy
electroencephalogram
excitatory neurotransmitter
inhibitory neurotransmitter
Neurology. Diseases of the nervous system
RC346-429
spellingShingle binocular rivalry
idiopathic generalized epilepsy
electroencephalogram
excitatory neurotransmitter
inhibitory neurotransmitter
Neurology. Diseases of the nervous system
RC346-429
Jiaonan Wu
Jiaonan Wu
Wei Ding
Xing Ye
Xing Ye
Qiang Wei
Qiang Wei
Xinyi Lv
Qiqiang Tang
Qiqiang Tang
Yanghua Tian
Yanghua Tian
Kai Wang
Kai Wang
Yubao Jiang
Yubao Jiang
Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized Epilepsy
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.
format article
author Jiaonan Wu
Jiaonan Wu
Wei Ding
Xing Ye
Xing Ye
Qiang Wei
Qiang Wei
Xinyi Lv
Qiqiang Tang
Qiqiang Tang
Yanghua Tian
Yanghua Tian
Kai Wang
Kai Wang
Yubao Jiang
Yubao Jiang
author_facet Jiaonan Wu
Jiaonan Wu
Wei Ding
Xing Ye
Xing Ye
Qiang Wei
Qiang Wei
Xinyi Lv
Qiqiang Tang
Qiqiang Tang
Yanghua Tian
Yanghua Tian
Kai Wang
Kai Wang
Yubao Jiang
Yubao Jiang
author_sort Jiaonan Wu
title 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_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_sort interictal activity is associated with slower binocular rivalry in idiopathic generalized epilepsy
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/0e5f279300ff4b50be72aa3b00e9e2a5
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