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Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum

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 se...

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Autores principales: Knight, Emily J., Freedman, Edward G., Myers, Evan J., Berruti, Alaina S., Oakes, Leona A., Cao, Cody Zhewei, Molholm, Sophie, Foxe, John J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10072299/
https://www.ncbi.nlm.nih.gov/pubmed/36859306
http://dx.doi.org/10.1523/JNEUROSCI.1192-22.2023
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author Knight, Emily J.
Freedman, Edward G.
Myers, Evan J.
Berruti, Alaina S.
Oakes, Leona A.
Cao, Cody Zhewei
Molholm, Sophie
Foxe, John J.
author_facet Knight, Emily J.
Freedman, Edward G.
Myers, Evan J.
Berruti, Alaina S.
Oakes, Leona A.
Cao, Cody Zhewei
Molholm, Sophie
Foxe, John J.
author_sort Knight, Emily J.
collection PubMed
description 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.
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spelling pubmed-100722992023-04-05 Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum Knight, Emily J. Freedman, Edward G. Myers, Evan J. Berruti, Alaina S. Oakes, Leona A. Cao, Cody Zhewei Molholm, Sophie Foxe, John J. J Neurosci Research Articles 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. Society for Neuroscience 2023-03-29 /pmc/articles/PMC10072299/ /pubmed/36859306 http://dx.doi.org/10.1523/JNEUROSCI.1192-22.2023 Text en Copyright © 2023 Knight et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (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
Knight, Emily J.
Freedman, Edward G.
Myers, Evan J.
Berruti, Alaina S.
Oakes, Leona A.
Cao, Cody Zhewei
Molholm, Sophie
Foxe, John J.
Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum
title Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum
title_full Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum
title_fullStr Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum
title_full_unstemmed Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum
title_short Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum
title_sort severely attenuated visual feedback processing in children on the autism spectrum
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10072299/
https://www.ncbi.nlm.nih.gov/pubmed/36859306
http://dx.doi.org/10.1523/JNEUROSCI.1192-22.2023
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