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A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism

Overly stable visual perception seen in individuals with autism spectrum disorder (ASD) is related to higher-order core symptoms of the condition. However, the neural basis by which these seemingly different symptoms are simultaneously observed in individuals with ASD remains unclear. Here, we aimed...

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Autores principales: Watanabe, Takamitsu, Lawson, Rebecca P., Walldén, Ylva S.E., Rees, Geraint
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697400/
https://www.ncbi.nlm.nih.gov/pubmed/31213484
http://dx.doi.org/10.1523/JNEUROSCI.2831-18.2019
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author Watanabe, Takamitsu
Lawson, Rebecca P.
Walldén, Ylva S.E.
Rees, Geraint
author_facet Watanabe, Takamitsu
Lawson, Rebecca P.
Walldén, Ylva S.E.
Rees, Geraint
author_sort Watanabe, Takamitsu
collection PubMed
description Overly stable visual perception seen in individuals with autism spectrum disorder (ASD) is related to higher-order core symptoms of the condition. However, the neural basis by which these seemingly different symptoms are simultaneously observed in individuals with ASD remains unclear. Here, we aimed to identify such a neuroanatomical substrate linking perceptual stability to autistic cognitive rigidity, a part of core restricted, repetitive behaviors (RRBs). First, using a bistable visual perception test, we measured the perceptual stability of 22 high-functioning adults with ASD and 22 age-, IQ-, and sex-matched typically developing human individuals and confirmed overstable visual perception in autism. Next, using a spontaneous task-switching (TS) test, we showed that the individuals with ASD were more likely to repeat the same task voluntarily and spontaneously, and such rigid TS behavior was associated with the severity of their RRB symptoms. We then compared these perceptual and cognitive behaviors and found a significant correlation between them for individuals with ASD. Finally, we found that this behavioral link was supported by a smaller gray matter volume (GMV) of the posterior superior parietal lobule (pSPL) in individuals with ASD. Moreover, this smaller GMV in the pSPL was also associated with the RRB symptoms and replicated in two independent datasets. Our findings suggest that the pSPL could be one of the neuroanatomical mediators of cognitive and perceptual inflexibility in autism, which could help a unified biological understanding of the mechanisms underpinning diverse symptoms of this developmental disorder. SIGNIFICANCE STATEMENT Behavioral studies show perceptual overstability in autism spectrum disorder (ASD). However, the neural mechanisms by which such sensory symptoms can coexist and often correlate with seemingly separate core symptoms remain unknown. Here, we have identified such a key neuroanatomical substrate. We have revealed that overstable sensory perception of individuals with ASD is linked with their cognitive rigidity, a part of core restricted, repetitive behavior symptoms, and such a behavioral link is underpinned by a smaller gray matter volume in the posterior superior parietal lobule in autism. These findings uncover a key neuroanatomical mediator of autistic perceptual and cognitive inflexibility and would ignite future studies on how the core symptoms of ASD interact with its unique sensory perception.
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spelling pubmed-66974002019-08-20 A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism Watanabe, Takamitsu Lawson, Rebecca P. Walldén, Ylva S.E. Rees, Geraint J Neurosci Research Articles Overly stable visual perception seen in individuals with autism spectrum disorder (ASD) is related to higher-order core symptoms of the condition. However, the neural basis by which these seemingly different symptoms are simultaneously observed in individuals with ASD remains unclear. Here, we aimed to identify such a neuroanatomical substrate linking perceptual stability to autistic cognitive rigidity, a part of core restricted, repetitive behaviors (RRBs). First, using a bistable visual perception test, we measured the perceptual stability of 22 high-functioning adults with ASD and 22 age-, IQ-, and sex-matched typically developing human individuals and confirmed overstable visual perception in autism. Next, using a spontaneous task-switching (TS) test, we showed that the individuals with ASD were more likely to repeat the same task voluntarily and spontaneously, and such rigid TS behavior was associated with the severity of their RRB symptoms. We then compared these perceptual and cognitive behaviors and found a significant correlation between them for individuals with ASD. Finally, we found that this behavioral link was supported by a smaller gray matter volume (GMV) of the posterior superior parietal lobule (pSPL) in individuals with ASD. Moreover, this smaller GMV in the pSPL was also associated with the RRB symptoms and replicated in two independent datasets. Our findings suggest that the pSPL could be one of the neuroanatomical mediators of cognitive and perceptual inflexibility in autism, which could help a unified biological understanding of the mechanisms underpinning diverse symptoms of this developmental disorder. SIGNIFICANCE STATEMENT Behavioral studies show perceptual overstability in autism spectrum disorder (ASD). However, the neural mechanisms by which such sensory symptoms can coexist and often correlate with seemingly separate core symptoms remain unknown. Here, we have identified such a key neuroanatomical substrate. We have revealed that overstable sensory perception of individuals with ASD is linked with their cognitive rigidity, a part of core restricted, repetitive behavior symptoms, and such a behavioral link is underpinned by a smaller gray matter volume in the posterior superior parietal lobule in autism. These findings uncover a key neuroanatomical mediator of autistic perceptual and cognitive inflexibility and would ignite future studies on how the core symptoms of ASD interact with its unique sensory perception. Society for Neuroscience 2019-08-14 /pmc/articles/PMC6697400/ /pubmed/31213484 http://dx.doi.org/10.1523/JNEUROSCI.2831-18.2019 Text en Copyright © 2019 Watanabe et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Watanabe, Takamitsu
Lawson, Rebecca P.
Walldén, Ylva S.E.
Rees, Geraint
A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism
title A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism
title_full A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism
title_fullStr A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism
title_full_unstemmed A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism
title_short A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism
title_sort neuroanatomical substrate linking perceptual stability to cognitive rigidity in autism
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697400/
https://www.ncbi.nlm.nih.gov/pubmed/31213484
http://dx.doi.org/10.1523/JNEUROSCI.2831-18.2019
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