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Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information

Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by lack of attention to social cues in the environment, including speech. Hypersensitivity to sensory stimuli, such as loud noises, is also extremely common in youth with ASD. While a link between sensory hypersensitivity...

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Autores principales: Hernandez, Leanna M., Green, Shulamite A., Lawrence, Katherine E., Inada, Marisa, Liu, Janelle, Bookheimer, Susan Y., Dapretto, Mirella
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7194032/
https://www.ncbi.nlm.nih.gov/pubmed/32390890
http://dx.doi.org/10.3389/fpsyt.2020.00343
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author Hernandez, Leanna M.
Green, Shulamite A.
Lawrence, Katherine E.
Inada, Marisa
Liu, Janelle
Bookheimer, Susan Y.
Dapretto, Mirella
author_facet Hernandez, Leanna M.
Green, Shulamite A.
Lawrence, Katherine E.
Inada, Marisa
Liu, Janelle
Bookheimer, Susan Y.
Dapretto, Mirella
author_sort Hernandez, Leanna M.
collection PubMed
description Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by lack of attention to social cues in the environment, including speech. Hypersensitivity to sensory stimuli, such as loud noises, is also extremely common in youth with ASD. While a link between sensory hypersensitivity and impaired social functioning has been hypothesized, very little is known about the neural mechanisms whereby exposure to distracting sensory stimuli may interfere with the ability to direct attention to socially-relevant information. Here, we used functional magnetic resonance imaging (fMRI) in youth with and without ASD (N=54, age range 8–18 years) to (1) examine brain responses during presentation of brief social interactions (i.e., two-people conversations) shrouded in ecologically-valid environmental noises, and (2) assess how brain activity during encoding might relate to later accuracy in identifying what was heard. During exposure to conversation-in-noise (vs. conversation or noise alone), both neurotypical youth and youth with ASD showed robust activation of canonical language networks. However, the extent to which youth with ASD activated temporal language regions, including voice-selective cortex (i.e., posterior superior temporal sulcus), predicted later discriminative accuracy in identifying what was heard. Further, relative to neurotypical youth, ASD youth showed significantly greater activity in left-hemisphere speech-processing cortex (i.e., angular gyrus) while listening to conversation-in-noise (vs. conversation or noise alone). Notably, in youth with ASD, increased activity in this region was associated with higher social motivation and better social cognition measures. This heightened activity in voice-selective/speech-processing regions may serve as a compensatory mechanism allowing youth with ASD to hone in on the conversations they heard in the context of non-social distracting stimuli. These findings further suggest that focusing on social and non-social stimuli simultaneously may be more challenging for youth with ASD requiring the recruitment of additional neural resources to encode socially-relevant information.
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spelling pubmed-71940322020-05-08 Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information Hernandez, Leanna M. Green, Shulamite A. Lawrence, Katherine E. Inada, Marisa Liu, Janelle Bookheimer, Susan Y. Dapretto, Mirella Front Psychiatry Psychiatry Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by lack of attention to social cues in the environment, including speech. Hypersensitivity to sensory stimuli, such as loud noises, is also extremely common in youth with ASD. While a link between sensory hypersensitivity and impaired social functioning has been hypothesized, very little is known about the neural mechanisms whereby exposure to distracting sensory stimuli may interfere with the ability to direct attention to socially-relevant information. Here, we used functional magnetic resonance imaging (fMRI) in youth with and without ASD (N=54, age range 8–18 years) to (1) examine brain responses during presentation of brief social interactions (i.e., two-people conversations) shrouded in ecologically-valid environmental noises, and (2) assess how brain activity during encoding might relate to later accuracy in identifying what was heard. During exposure to conversation-in-noise (vs. conversation or noise alone), both neurotypical youth and youth with ASD showed robust activation of canonical language networks. However, the extent to which youth with ASD activated temporal language regions, including voice-selective cortex (i.e., posterior superior temporal sulcus), predicted later discriminative accuracy in identifying what was heard. Further, relative to neurotypical youth, ASD youth showed significantly greater activity in left-hemisphere speech-processing cortex (i.e., angular gyrus) while listening to conversation-in-noise (vs. conversation or noise alone). Notably, in youth with ASD, increased activity in this region was associated with higher social motivation and better social cognition measures. This heightened activity in voice-selective/speech-processing regions may serve as a compensatory mechanism allowing youth with ASD to hone in on the conversations they heard in the context of non-social distracting stimuli. These findings further suggest that focusing on social and non-social stimuli simultaneously may be more challenging for youth with ASD requiring the recruitment of additional neural resources to encode socially-relevant information. Frontiers Media S.A. 2020-04-24 /pmc/articles/PMC7194032/ /pubmed/32390890 http://dx.doi.org/10.3389/fpsyt.2020.00343 Text en Copyright © 2020 Hernandez, Green, Lawrence, Inada, Liu, Bookheimer and Dapretto http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Psychiatry
Hernandez, Leanna M.
Green, Shulamite A.
Lawrence, Katherine E.
Inada, Marisa
Liu, Janelle
Bookheimer, Susan Y.
Dapretto, Mirella
Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information
title Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information
title_full Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information
title_fullStr Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information
title_full_unstemmed Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information
title_short Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information
title_sort social attention in autism: neural sensitivity to speech over background noise predicts encoding of social information
topic Psychiatry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7194032/
https://www.ncbi.nlm.nih.gov/pubmed/32390890
http://dx.doi.org/10.3389/fpsyt.2020.00343
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