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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-04-01
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| Series: | Frontiers in Psychiatry |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpsyt.2020.00343/full |
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| author | Leanna M. Hernandez Leanna M. Hernandez Shulamite A. Green Shulamite A. Green Katherine E. Lawrence Katherine E. Lawrence Marisa Inada Janelle Liu Janelle Liu Susan Y. Bookheimer Susan Y. Bookheimer Mirella Dapretto Mirella Dapretto |
| author_facet | Leanna M. Hernandez Leanna M. Hernandez Shulamite A. Green Shulamite A. Green Katherine E. Lawrence Katherine E. Lawrence Marisa Inada Janelle Liu Janelle Liu Susan Y. Bookheimer Susan Y. Bookheimer Mirella Dapretto Mirella Dapretto |
| author_sort | Leanna M. Hernandez |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-12T20:32:34Z |
| format | Article |
| id | doaj.art-6ae2e2dfa8a4472dbd30119f612225ee |
| institution | Directory Open Access Journal |
| issn | 1664-0640 |
| language | English |
| last_indexed | 2024-12-12T20:32:34Z |
| publishDate | 2020-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Psychiatry |
| spelling | doaj.art-6ae2e2dfa8a4472dbd30119f612225ee2022-12-22T00:12:59ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402020-04-011110.3389/fpsyt.2020.00343517323Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social InformationLeanna M. Hernandez0Leanna M. Hernandez1Shulamite A. Green2Shulamite A. Green3Katherine E. Lawrence4Katherine E. Lawrence5Marisa Inada6Janelle Liu7Janelle Liu8Susan Y. Bookheimer9Susan Y. Bookheimer10Mirella Dapretto11Mirella Dapretto12Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, United StatesAhmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, United StatesAhmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, United StatesAhmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesAhmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, United StatesAhmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesStaglin IMHRO Center for Cognitive Neuroscience, University of California, Los Angeles, Los Angeles, CA, United StatesAhmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, United StatesAutism 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.https://www.frontiersin.org/article/10.3389/fpsyt.2020.00343/fullspeechautismvoice-selectiveattentionconversationnoise |
| spellingShingle | Leanna M. Hernandez Leanna M. Hernandez Shulamite A. Green Shulamite A. Green Katherine E. Lawrence Katherine E. Lawrence Marisa Inada Janelle Liu Janelle Liu Susan Y. Bookheimer Susan Y. Bookheimer Mirella Dapretto Mirella Dapretto Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information Frontiers in Psychiatry speech autism voice-selective attention conversation noise |
| 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 | speech autism voice-selective attention conversation noise |
| url | https://www.frontiersin.org/article/10.3389/fpsyt.2020.00343/full |
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