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Research Articles, Behavioral/Cognitive

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

Anila M. D'Mello, Isabelle R. Frosch, Steven L. Meisler, Hannah Grotzinger, Tyler K. Perrachione and John D.E. Gabrieli
Journal of Neuroscience 15 March 2023, 43 (11) 1952-1962; DOI: https://doi.org/10.1523/JNEUROSCI.0608-22.2023
Anila M. D'Mello
1McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139
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  • ORCID record for Anila M. D'Mello
Isabelle R. Frosch
1McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139
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Steven L. Meisler
2Program in Speech and Hearing Bioscience and Technology, Harvard University, Cambridge, Massachusetts, 02115
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Hannah Grotzinger
1McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139
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Tyler K. Perrachione
3Department of Speech, Language, and Hearing Sciences, Boston University, Boston, Massachusetts 02215
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John D.E. Gabrieli
1McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139
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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.

  • autism
  • diffusion weighted imaging
  • faces
  • fMRI
  • functional connectivity
  • repetition suppression

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The Journal of Neuroscience: 43 (11)
Journal of Neuroscience
Vol. 43, Issue 11
15 Mar 2023
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Diminished Repetition Suppression Reveals Selective and Systems-Level Face Processing Differences in ASD
Anila M. D'Mello, Isabelle R. Frosch, Steven L. Meisler, Hannah Grotzinger, Tyler K. Perrachione, John D.E. Gabrieli
Journal of Neuroscience 15 March 2023, 43 (11) 1952-1962; DOI: 10.1523/JNEUROSCI.0608-22.2023

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Diminished Repetition Suppression Reveals Selective and Systems-Level Face Processing Differences in ASD
Anila M. D'Mello, Isabelle R. Frosch, Steven L. Meisler, Hannah Grotzinger, Tyler K. Perrachione, John D.E. Gabrieli
Journal of Neuroscience 15 March 2023, 43 (11) 1952-1962; DOI: 10.1523/JNEUROSCI.0608-22.2023
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Keywords

  • autism
  • diffusion weighted imaging
  • faces
  • fMRI
  • functional connectivity
  • repetition suppression

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