Abstract

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.

Highlights

  • When incongruent images are presented to the two eyes, perceptual awareness spontaneously alternates every few seconds between one image and the other rather than forming a stable composite [1,2,3]

  • Patients were stratified into abnormal ambulatory EEG (AB-AEEG) and normal ambulatory EEG (N-AEEG) subgroups depending on the presence or absence, respectively, of interictal epileptiform discharges (IEDs) on the ambulatory EEG

  • Post-hoc pair-wise comparisons revealed that Beck Depression Inventory (BDI) score was significantly higher in the AB-AEEG group than the healthy control (HC) group (p < 0.001) but did not differ between the N-AEEG and HC groups (p = 0.220), or the N-AEEG and AB-AEEG groups (p = 0.287)

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Summary

Introduction

When incongruent images are presented to the two eyes, perceptual awareness spontaneously alternates every few seconds between one image and the other rather than forming a stable composite [1,2,3]. This phenomenon, known as “binocular rivalry” (BR), is mediated by competitive interactions between populations of neurons that code for the two inputs at various levels of visual processing. Since the stimulus remains constant, the spontaneous perceptual alternation characteristic of bistable perception reflects inherent dynamic operations in the brain and may offer a tool to distinguish normal from abnormal neural dynamics. The neural dynamics reflective of BR critically depend on the balance between excitation and inhibition (E/I balance) in the cortex [2, 16,17,18,19,20], suggesting that the characteristics of BR may change in pathological conditions involving E/I disruption, such as epilepsy and autism spectrum disorder

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