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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Frontiers Media S.A.
2021-11-01
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| Series: | Frontiers in Neurology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fneur.2021.720126/full |
| _version_ | 1819002377178447872 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-20T23:04:08Z |
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| institution | Directory Open Access Journal |
| issn | 1664-2295 |
| language | English |
| last_indexed | 2024-12-20T23:04:08Z |
| publishDate | 2021-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Neurology |
| spelling | doaj.art-0e5f279300ff4b50be72aa3b00e9e2a52022-12-21T19:23:55ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-11-011210.3389/fneur.2021.720126720126Interictal Activity Is Associated With Slower Binocular Rivalry in Idiopathic Generalized EpilepsyJiaonan Wu0Jiaonan Wu1Wei Ding2Xing Ye3Xing Ye4Qiang Wei5Qiang Wei6Xinyi Lv7Qiqiang Tang8Qiqiang Tang9Yanghua Tian10Yanghua Tian11Kai Wang12Kai Wang13Yubao Jiang14Yubao Jiang15Department of Neurology, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, ChinaDepartment of Neurology, Anhui Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, ChinaDepartment of Nephrology, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, ChinaDepartment of Neurology, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of Neurology, The First Affiliated Hospital of Anhui Medical University, Hefei, ChinaDepartment of Neurology, The First Affiliated Hospital of Anhui Medical University, Hefei, ChinaKey Laboratory of Cognition and Neuropsychiatric Disorders, Hefei, ChinaDepartment of Neurology, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, ChinaDepartment of Neurology, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, ChinaDepartment of Neurology, Anhui Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, ChinaDepartment of Neurology, The First Affiliated Hospital of Anhui Medical University, Hefei, ChinaKey Laboratory of Cognition and Neuropsychiatric Disorders, Hefei, ChinaDepartment of Neurology, The First Affiliated Hospital of Anhui Medical University, Hefei, ChinaKey Laboratory of Cognition and Neuropsychiatric Disorders, Hefei, ChinaDepartment of Neurology, The First Affiliated Hospital of Anhui Medical University, Hefei, ChinaKey Laboratory of Cognition and Neuropsychiatric Disorders, Hefei, ChinaObjective: 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.https://www.frontiersin.org/articles/10.3389/fneur.2021.720126/fullbinocular rivalryidiopathic generalized epilepsyelectroencephalogramexcitatory neurotransmitterinhibitory neurotransmitter |
| spellingShingle | 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 Frontiers in Neurology binocular rivalry idiopathic generalized epilepsy electroencephalogram excitatory neurotransmitter inhibitory neurotransmitter |
| 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 | binocular rivalry idiopathic generalized epilepsy electroencephalogram excitatory neurotransmitter inhibitory neurotransmitter |
| url | https://www.frontiersin.org/articles/10.3389/fneur.2021.720126/full |
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