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Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis

Organizing sensory information into coherent perceptual objects is fundamental to everyday perception and communication. In the visual domain, indirect evidence from cortical responses suggests that children with autism spectrum disorder (ASD) have anomalous figure–ground segregation. While auditory...

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Autores principales: Bharadwaj, Hari, Mamashli, Fahimeh, Khan, Sheraz, Singh, Ravinderjit, Joseph, Robert M., Losh, Ainsley, Pawlyszyn, Stephanie, McGuiggan, Nicole M., Graham, Steven, Hämäläinen, Matti S., Kenet, Tal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8884487/
https://www.ncbi.nlm.nih.gov/pubmed/35167585
http://dx.doi.org/10.1371/journal.pbio.3001541
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author Bharadwaj, Hari
Mamashli, Fahimeh
Khan, Sheraz
Singh, Ravinderjit
Joseph, Robert M.
Losh, Ainsley
Pawlyszyn, Stephanie
McGuiggan, Nicole M.
Graham, Steven
Hämäläinen, Matti S.
Kenet, Tal
author_facet Bharadwaj, Hari
Mamashli, Fahimeh
Khan, Sheraz
Singh, Ravinderjit
Joseph, Robert M.
Losh, Ainsley
Pawlyszyn, Stephanie
McGuiggan, Nicole M.
Graham, Steven
Hämäläinen, Matti S.
Kenet, Tal
author_sort Bharadwaj, Hari
collection PubMed
description Organizing sensory information into coherent perceptual objects is fundamental to everyday perception and communication. In the visual domain, indirect evidence from cortical responses suggests that children with autism spectrum disorder (ASD) have anomalous figure–ground segregation. While auditory processing abnormalities are common in ASD, especially in environments with multiple sound sources, to date, the question of scene segregation in ASD has not been directly investigated in audition. Using magnetoencephalography, we measured cortical responses to unattended (passively experienced) auditory stimuli while parametrically manipulating the degree of temporal coherence that facilitates auditory figure–ground segregation. Results from 21 children with ASD (aged 7–17 years) and 26 age- and IQ-matched typically developing children provide evidence that children with ASD show anomalous growth of cortical neural responses with increasing temporal coherence of the auditory figure. The documented neurophysiological abnormalities did not depend on age, and were reflected both in the response evoked by changes in temporal coherence of the auditory scene and in the associated induced gamma rhythms. Furthermore, the individual neural measures were predictive of diagnosis (83% accuracy) and also correlated with behavioral measures of ASD severity and auditory processing abnormalities. These findings offer new insight into the neural mechanisms underlying auditory perceptual deficits and sensory overload in ASD, and suggest that temporal-coherence-based auditory scene analysis and suprathreshold processing of coherent auditory objects may be atypical in ASD.
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spelling pubmed-88844872022-03-01 Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis Bharadwaj, Hari Mamashli, Fahimeh Khan, Sheraz Singh, Ravinderjit Joseph, Robert M. Losh, Ainsley Pawlyszyn, Stephanie McGuiggan, Nicole M. Graham, Steven Hämäläinen, Matti S. Kenet, Tal PLoS Biol Short Reports Organizing sensory information into coherent perceptual objects is fundamental to everyday perception and communication. In the visual domain, indirect evidence from cortical responses suggests that children with autism spectrum disorder (ASD) have anomalous figure–ground segregation. While auditory processing abnormalities are common in ASD, especially in environments with multiple sound sources, to date, the question of scene segregation in ASD has not been directly investigated in audition. Using magnetoencephalography, we measured cortical responses to unattended (passively experienced) auditory stimuli while parametrically manipulating the degree of temporal coherence that facilitates auditory figure–ground segregation. Results from 21 children with ASD (aged 7–17 years) and 26 age- and IQ-matched typically developing children provide evidence that children with ASD show anomalous growth of cortical neural responses with increasing temporal coherence of the auditory figure. The documented neurophysiological abnormalities did not depend on age, and were reflected both in the response evoked by changes in temporal coherence of the auditory scene and in the associated induced gamma rhythms. Furthermore, the individual neural measures were predictive of diagnosis (83% accuracy) and also correlated with behavioral measures of ASD severity and auditory processing abnormalities. These findings offer new insight into the neural mechanisms underlying auditory perceptual deficits and sensory overload in ASD, and suggest that temporal-coherence-based auditory scene analysis and suprathreshold processing of coherent auditory objects may be atypical in ASD. Public Library of Science 2022-02-15 /pmc/articles/PMC8884487/ /pubmed/35167585 http://dx.doi.org/10.1371/journal.pbio.3001541 Text en © 2022 Bharadwaj 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 (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Short Reports
Bharadwaj, Hari
Mamashli, Fahimeh
Khan, Sheraz
Singh, Ravinderjit
Joseph, Robert M.
Losh, Ainsley
Pawlyszyn, Stephanie
McGuiggan, Nicole M.
Graham, Steven
Hämäläinen, Matti S.
Kenet, Tal
Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
title Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
title_full Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
title_fullStr Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
title_full_unstemmed Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
title_short Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
title_sort cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis
topic Short Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8884487/
https://www.ncbi.nlm.nih.gov/pubmed/35167585
http://dx.doi.org/10.1371/journal.pbio.3001541
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