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 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.

Slow rhythmic eye motion predicts periodic alternation of bistable perception

Bistable perception is characterized by periodic alternation between two different perceptual interpretations, the mechanism of which is poorly understood. Herein, we show that perceptual decisions in bistable perception are strongly correlated with slow rhythmic eye motion, the frequency of which varies across individuals. From eye gaze trajectory measurements during three types of bistable tasks, we found that each subject’s gaze position oscillates slowly(less than 1Hz), and that this frequency matches that of bistable perceptual alternation. Notably, the motion of the eye apparently moves in opposite directions before two opposite perceptual decisions, and this enables the prediction of the timing and direction of perceptual alternation from eye motion. We also found that the correlation between eye movement and a perceptual decision is maintained during variations of the alternation frequency by the intentional switching or retaining of perceived states. This result suggests that periodic bistable perception is phase-locked with rhythmic eye motion.

Alpha fluctuations regulate the accrual of visual information to awareness

Endogenous brain processes play a paramount role in shaping up perceptual phenomenology, as illustrated by the alternations experienced by humans (and other animals) when watching perceptually ambiguous, static images. Here, we hypothesised that endogenous alpha fluctuations in the visual cortex pace the accumulation of sensory information leading to perceptual outcomes. We addressed this hypothesis using binocular rivalry combined with visual entrainment and electroencephalography in humans (42 female, 40 male). The results revealed a correlation between the individual frequency of alpha oscillations in the occipital cortex and perceptual alternation rates experienced during binocular rivalry. In subsequent experiments we show that regulating endogenous brain activity via entrainment produced corresponding changes in perceptual alternation rate, which were observed only in the alpha range but not at lower entrainment frequencies. Overall, rhythmic alpha stimulation resulted in faster perceptual alternation rates, compared to arrhythmic or no stimulation. These findings support the notion that visual information is accumulated via alpha cycles to promote the emergence of conscious perceptual representations. We suggest that models of binocular rivalry incorporating posterior alpha as a pacemaker can provide an important advance in the comprehension of the dynamics of visual awareness.Significance statementMainstream theories in cognitive neuroscience agree that endogenous brain processes play a paramount role in shaping our perceptual experience of sensory inputs. In vision, endogenous fluctuations in the alpha rhythm have been pointed out to regulate visual inputs to perception. In support of this hypothesis, here we used EEG recordings and visual entrainment to demonstrate that inter-individual differences in the speed of endogenous alpha fluctuations in the brain are causally related to the accrual of visual information to awareness. These findings provide, for the first time, evidence for alpha-gated regulation of the dynamics of alternations in conscious visual perception.

Intrinsic timescales of sensory integration for motion perception

A subject-specific process of accumulation of information may be responsible for variations in decision time following visual perceptions in humans. A detailed profile of this perceptual decision making, however, has not yet been verified. Using a coherence-varying motion discrimination task, we precisely measured the perceptual decision kernel of subjects. We observed that the kernel size (decision time) is consistent within subjects, independent of stimulus dynamics, and the observed kernel could accurately predict each subject’s performance. Interestingly, the performance of most subjects was optimized when stimulus duration was matched to their kernel size. We also found that the observed kernel size was strongly correlated with the perceptual alternation in bistable conditions. Our result suggests that the observed decision kernel reveals a subject-specific feature of sensory integration.