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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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2020
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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. |
format | Online Article Text |
id | pubmed-7194032 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
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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