Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum

Abstract

Individuals on the autism spectrum often exhibit atypicality in their sensory perception, but the neural underpinnings of these perceptual differences remain incompletely understood. One proposed mechanism is an imbalance in higher-order feedback re-entrant inputs to early sensory cortices during sensory perception, leading to increased propensity to focus on local object features over global context. We explored this theory by measuring visual evoked potentials during contour integration as considerable work has revealed that these processes are largely driven by feedback inputs from higher-order ventral visual stream regions. We tested the hypothesis that autistic individuals would have attenuated evoked responses to illusory contours compared with neurotypical controls. Electrophysiology was acquired while 29 autistic and 31 neurotypical children (7-17 years old, inclusive of both males and females) passively viewed a random series of Kanizsa figure stimuli, each consisting of four inducers that were aligned either at random rotational angles or such that contour integration would form an illusory square. Autistic children demonstrated attenuated automatic contour integration over lateral occipital regions relative to neurotypical controls. The data are discussed in terms of the role of predictive feedback processes on perception of global stimulus features and the notion that weakened "priors" may play a role in the visual processing anomalies seen in autism.SIGNIFICANCE STATEMENT Children on the autism spectrum differ from typically developing children in many aspects of their processing of sensory stimuli. One proposed mechanism for these differences is an imbalance in higher-order feedback to primary sensory regions, leading to an increased focus on local object features rather than global context. However, systematic investigation of these feedback mechanisms remains limited. Using EEG and a visual illusion paradigm that is highly dependent on intact feedback processing, we demonstrated significant disruptions to visual feedback processing in children with autism. This provides much needed experimental evidence that advances our understanding of the contribution of feedback processing to visual perception in autism spectrum disorder.

Keywords: autism spectrum disorder; illusory contours; object recognition; visual evoked potentials; visual feedback.

Figure 1.

A, Schematic representation of experimental paradigm and timing. IC/NC stimuli appear on the screen for 80 ms duration with 800-1400 ms stimulus onset asynchrony (SOA). Central fixation point changes from red to green at variable intervals (1-10 s). B, Schematic representation of central and left and right lateral stimulus presentations. IC/NC stimuli have a support ratio (the ratio of portion of the perimeter occupied by the inducers themselves to the total perimeter of the induced square shape) of 54% and subtend 3.5° of visual angle in both the horizontal and vertical directions. Lateral IC/NC stimuli have an offset of ± 2.5° from the vertical meridian to the nearest edge of the stimulus. C, Components used in the primary analysis as overlaid over the two analyzed bilateral lateral occipital sites (PO3 and PO4), collapsed across all groups (ASD, NT) and stimulus configuration (IC, NC) for the central stimulus presentations.

Figure 2.

A, Grand average VEPs for centrally presented stimuli at bilateral lateral occipital sites (PO3 and PO4) obtained in NT (top) and ASD (bottom) participants to NC (purple), and IC (green), and IC-NC difference potential (orange). Shaded regions represent ± standard error of the mean (SEM). B, Difference waveforms (IC-NC) obtained in ASD (blue) and NT (pink) participants at bilateral lateral occipital sites (PO3 and PO4).

Figure 3.

A, Grand average VEPs for laterally presented stimuli at bilateral lateral occipital sites (PO3 and PO4) obtained in NT (top) and ASD (bottom) participants to NC (purple), and IC (green), and IC-NC difference potential (orange). Shaded regions represent ± standard error of the mean (SEM). B, Difference waveforms (IC-NC) obtained in ASD (blue) and NT (pink) participants at bilateral lateral occipital sites (PO3 and PO4).

Figure 4.

A, Topographic representation of the difference in instantaneous amplitude of evoked response between IC and NC stimuli for central (top), left (middle), and right (bottom) stimulus locations for NT participants at 50 ms intervals between 100 and 350 ms after stimulus onset. B, Topographic representation of the difference in instantaneous amplitude of evoked response between IC and NC stimuli for central (top), left (middle), and right (bottom) stimulus locations for ASD participants at 50 ms intervals between 50 and 50 ms after stimulus onset.

Figure 5.

A, Violin plots represent the distribution of the difference in IC-NC mean amplitude (μV) for centrally presented stimuli during the IC effect time window (167-177 ms) at bilateral lateral occipital sites (PO3 and PO4) among ASD (purple) and NT (blue) participants. B, Violin plots represent the distribution of the difference in IC-NC mean amplitude (μV) for centrally presented stimuli during the N_cl time window (305-315 ms) at bilateral lateral occipital sites (PO3 and PO4) among ASD (purple) and NT (blue) participants. Horizontal dotted lines represent the group mean.

Figure 6.

Results of the exploratory factorial mass univariate analysis across all electrodes and time points between 100 and 300 ms with a between-subjects factor of group (NT, ASD) and within-subject factor of stimulus configuration (IC, NC). A, Regions and time points demonstrating a main effect of stimulus configuration. B, Regions and time points demonstrating a group × stimulus configuration interaction. There was no significant main effect of group.

Figure 7.

Topographic representation of the difference in instantaneous amplitude of evoked response between IC and NC stimuli for central stimulus locations comparing the FPz frontal reference electrode (top) with an average reference (bottom) for NT (A) and ASD (B) participants at 50 ms intervals between 100 and 350 ms after stimulus onset.

Figure 8.

Scatter plot represents in ASD (purple) and NT (blue) participants the relationship between difference in IC-NC mean amplitude (μV) for centrally presented stimuli during the IC effect time window and (A) Full-Scale IQ, (B) Block Design scaled score, (C) Matrix Reasoning scaled score, (D) SNAP-IV measure of ADHD symptoms, (E) SRS-2 Total T Score, and (F) ADOS-2 Comparison Score (ASD participants only).