Altered beta-band oscillations and connectivity underlie detail-oriented visual processing in autism

Abstract

AbstractSensory and perceptual anomalies have been increasingly recognized as core phenotypic markers for autism spectrum disorders (ASD). A neurophysiological characterization of these anomalies is of utmost importance to understand more complex behavioural manifestations within the spectrum. The present study employed electroencephalography (EEG) to test whether detail-oriented visual perception, a recognized hallmark of ASD, is associated with altered neural oscillations and functional connectivity in beta (and alpha) frequency bands, considering their role in feedback and top-down reentrant signalling in the typical population. A sample of children with diagnosis of ASD (N=18) and typically developing peers (TD; N=20) performed a visual crowding task, where they had to discriminate a peripheral target letter surrounded by flankers at different distances, together with a control condition with no flankers. In TD participants the amplitude of the target-locked N1 component and its cortical sources was significantly modulated as a function of visual crowding, whereas such modulation was absent in the ASD group, suggesting that their visual scene analysis takes place without a flexible neural computation. The comparison between groups showed a decreased activity in the ASD group in occipital, infero-temporal and inferior/middle frontal regions in conditions requiring detail-oriented perception as opposed to conditions requiring the discrimination of target in isolation. Moreover, in TD participants detail-oriented perception was associated with an event-related beta power reduction (15-30 Hz), which was not evident in the ASD group. A data-driven functional connectivity analysis highlighted in the ASD sample an increased connectivity in the beta frequency range between occipital and infero-temporal regions. Notably, individual hyperconnectivity indexes correlated to less severe ASD symptomatology and to a diminished detail-oriented perception, suggesting a potential compensatory mechanism. Overall, these results show that altered communication in the beta frequency band may explain atypical perception in ASD, reflecting aberrant feedback connectivity within the visual system with potential cascade effects in visual scene parsing and higher-order functions.