It’s all in the timing: Delayed feedback in autism may weaken predictive mechanisms during contour integration

Author:

Knight Emily J.ORCID,Altschuler Ted S.ORCID,Molholm SophieORCID,Murphy Jeremy W.ORCID,Freedman Edward G.ORCID,Foxe John J.ORCID

Abstract

ABSTRACTHumans rely on predictive mechanisms during visual processing to efficiently resolve incomplete or ambiguous sensory signals. While initial low-level sensory data are conveyed by feedforward connections, feedback connections are believed to shape sensory processing through conveyance of statistical predictions based on prior exposure to stimulus configurations. Individuals with autism spectrum disorder (ASD) show biases in stimulus processing toward parts rather than wholes, suggesting their sensory processing may be less shaped by statistical predictions acquired through prior exposure to global stimulus properties. Investigations of illusory contour (IC) processing in neurotypical (NT) adults have established a well-tested marker of contour integration characterized by a robust modulation of the visually evoked potential (VEP) – theIC-effect– that occurs over lateral occipital scalp during the timeframe of the N1 component. Converging evidence strongly supports the notion that thisIC-effectindexes a signal with significant feedback contributions. Using high-density VEPs, we compared theIC-effectin 6–17-year-old children with ASD (n=32) or NT development (n=53). Both groups of children generated anIC-effectthat was equivalent in amplitude. However, theIC-effectnotably onset 21ms later in ASD, even though timing of initial VEP afference was identical across groups. This suggests that feedforward information predominated during perceptual processing for 15% longer in ASD compared to NT children. This delay in the feedback dependentIC-effect, in the context of known developmental differences between feedforward and feedback fibers, suggests a potential pathophysiological mechanism of visual processing in ASD, whereby ongoing stimulus processing is less shaped by statistical prediction mechanisms.SIGNIFICANCE STATEMENTChildren with autism often present with an atypical visual perceptual style that emphasizes parts or details over the whole. Using electroencephalography (EEG), this study identifies delays in the visual feedback from higher order sensory brain areas to primary sensory regions. Because this type of visual feedback is thought to carry information about prior sensory experiences, individuals with autism may have difficulty efficiently using prior experience and predictions to help make sense of incoming new visual information. This provides empirical neural evidence to support theories of disrupted sensory perception mechanisms in autism.

Publisher

Cold Spring Harbor Laboratory

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