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. 2023 Mar 15;43(11):1952-1962.
doi: 10.1523/JNEUROSCI.0608-22.2023. Epub 2023 Feb 9.

Diminished Repetition Suppression Reveals Selective and Systems-Level Face Processing Differences in ASD

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Diminished Repetition Suppression Reveals Selective and Systems-Level Face Processing Differences in ASD

Anila M D'Mello et al. J Neurosci. .

Abstract

Repeated exposure to a stimulus results in reduced neural response, or repetition suppression, in brain regions responsible for processing that stimulus. This rapid accommodation to repetition is thought to underlie learning, stimulus selectivity, and strengthening of perceptual expectations. Importantly, reduced sensitivity to repetition has been identified in several neurodevelopmental, learning, and psychiatric disorders, including autism spectrum disorder (ASD), a neurodevelopmental disorder characterized by challenges in social communication and repetitive behaviors and restricted interests. Reduced ability to exploit or learn from repetition in ASD is hypothesized to contribute to sensory hypersensitivities, and parallels several theoretical frameworks claiming that ASD individuals show difficulty using regularities in the environment to facilitate behavior. Using fMRI in autistic and neurotypical human adults (females and males), we assessed the status of repetition suppression across two modalities (vision, audition) and with four stimulus categories (faces, objects, printed words, and spoken words). ASD individuals showed domain-specific reductions in repetition suppression for face stimuli only, but not for objects, printed words, or spoken words. Reduced repetition suppression for faces was associated with greater challenges in social communication in ASD. We also found altered functional connectivity between atypically adapting cortical regions and higher-order face recognition regions, and microstructural differences in related white matter tracts in ASD. These results suggest that fundamental neural mechanisms and system-wide circuits are selectively altered for face processing in ASD and enhance our understanding of how disruptions in the formation of stable face representations may relate to higher-order social communication processes.SIGNIFICANCE STATEMENT A common finding in neuroscience is that repetition results in plasticity in stimulus-specific processing regions, reflecting selectivity and adaptation (repetition suppression [RS]). RS is reduced in several neurodevelopmental and psychiatric conditions including autism spectrum disorder (ASD). Theoretical frameworks of ASD posit that reduced adaptation may contribute to associated challenges in social communication and sensory processing. However, the scope of RS differences in ASD is unknown. We examined RS for multiple categories across visual and auditory domains (faces, objects, printed words, spoken words) in autistic and neurotypical individuals. We found reduced RS in ASD for face stimuli only and altered functional connectivity and white matter microstructure between cortical face-recognition areas. RS magnitude correlated with social communication challenges among autistic individuals.

Keywords: autism; diffusion weighted imaging; fMRI; faces; functional connectivity; repetition suppression.

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Figures

Figure 1.
Figure 1.
Repetition suppression task schematic. Example blocks of nonrepeating and repeating stimuli are shown for each stimulus category: (A) faces, (B) objects, (C) printed words, and (D) spoken words. Participants monitored for the rare target stimulus, which was vertically (visual stimuli) or temporally (auditory stimuli) inverted (shown here with a red border).
Figure 2.
Figure 2.
Repetition suppression for each stimulus category ROIs by group. Left, Glass brains show voxelwise p-values for statistical parametric maps for the group-level univariate no-repeat > repeat contrast across all participants (voxel p < 0.001, cluster pFWE < 0.05). Thick black outlines indicate a priori ROIs. Right, Values extracted from these ROIs. A, The ASD group had significantly less repetition suppression to faces in the right FusG ROI than the NT group. B–D, For all other stimulus category ROIs, the ASD and NT groups did not differ in the magnitude of repetition suppression. Points indicate mean repetition suppression (difference between nonrepeating and repeating conditions) for each participant. *p < 0.005.
Figure 3.
Figure 3.
Temporal development of repetition suppression to faces. A, The time course of repetition suppression magnitude in the right FusG ROI for each group, estimated with a finite impulse response model (mean ± SEM across participants). B, Repetition suppression magnitude to faces in the right FusG ROI estimated over stimuli in the first half versus (C) second half of each task block. Across both groups, repetition suppression was stronger in the second half of the block than the first. Across the time course, repetition suppression was greater in the NT than the ASD group.
Figure 4.
Figure 4.
Greater challenges in autism are associated with reduced repetition suppression to faces in right FusG.
Figure 5.
Figure 5.
Group differences in functional connectivity during face perception. On average, participants in the ASD group showed an increase in functional connectivity between the right FusG ROI and both (A) right ATL and (B) left OFC during the repeating faces condition versus a decrease in functional connectivity between right FusG and these regions during the nonrepeating faces condition. The NT group showed the opposite pattern, with reduced connectivity for repeating and greater connectivity for nonrepeating faces. Conventions are the same as in Figure 2. Lines link points from the same participant.
Figure 6.
Figure 6.
Local microstructural differences in right ILF in ASD. A, Structural projections of the right ILF in a representative participant. Colors represent the primary diffusion direction of local segments. Note the primarily anterior-posterior gradient of the tract from visual areas along the inferior temporal lobe. B, FA along the right ILF was significantly less in ASD versus NT in an extended portion of the tract located within ATL (marked by asterisk and gray shading; αFWE = 0.00156). Lines indicate group mean ± SEM across participants.

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