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Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study

BACKGROUND: Social interaction often occurs in noisy environments with many extraneous sensory stimuli. This is especially relevant for youth with autism spectrum disorders (ASD) who commonly experience sensory over-responsivity (SOR) in addition to social challenges. However, the relationship betwe...

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Autores principales: Patterson, Genevieve, Cummings, Kaitlin K., Jung, Jiwon, Okada, Nana J., Tottenham, Nim, Bookheimer, Susan Y., Dapretto, Mirella, Green, Shulamite A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8461948/
https://www.ncbi.nlm.nih.gov/pubmed/34556059
http://dx.doi.org/10.1186/s11689-021-09391-0
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author Patterson, Genevieve
Cummings, Kaitlin K.
Jung, Jiwon
Okada, Nana J.
Tottenham, Nim
Bookheimer, Susan Y.
Dapretto, Mirella
Green, Shulamite A.
author_facet Patterson, Genevieve
Cummings, Kaitlin K.
Jung, Jiwon
Okada, Nana J.
Tottenham, Nim
Bookheimer, Susan Y.
Dapretto, Mirella
Green, Shulamite A.
author_sort Patterson, Genevieve
collection PubMed
description BACKGROUND: Social interaction often occurs in noisy environments with many extraneous sensory stimuli. This is especially relevant for youth with autism spectrum disorders (ASD) who commonly experience sensory over-responsivity (SOR) in addition to social challenges. However, the relationship between SOR and social difficulties is still poorly understood and thus rarely addressed in interventions. This study investigated the effect of auditory sensory distracters on neural processing of emotion identification in youth with ASD and the effects of increasing attention to social cues by priming participants with their own emotional faces. METHODS: While undergoing functional magnetic resonance imaging (fMRI), 30 youth with ASD and 24 typically developing (TD) age-matched controls (ages 8–17 years) identified faces as happy or angry with and without simultaneously hearing aversive environmental noises. Halfway through the task, participants also viewed videos of their own emotional faces. The relationship between parent-rated auditory SOR and brain responses during the task was also examined. RESULTS: Despite showing comparable behavioral performance on the task, ASD and TD youth demonstrated distinct patterns of neural activity. Compared to TD, ASD youth showed greater increases in amygdala, insula, and primary sensory regions when identifying emotions with noises compared to no sounds. After viewing videos of their own emotion faces, ASD youth showed greater increases in medial prefrontal cortex activation compared to TD youth. Within ASD youth, lower SOR was associated with reduced increased activity in subcortical regions after the prime and greater increased activity in the ventromedial prefrontal cortex after the prime, particularly in trials with noises. CONCLUSIONS: The results suggest that the sensory environment plays an important role in how ASD youth process social information. Additionally, we demonstrated that increasing attention to relevant social cues helps ASD youth engage frontal regions involved in higher-order social cognition, a mechanism that could be targeted in interventions. Importantly, the effect of the intervention may depend on individual differences in SOR, supporting the importance of pre-screening youth for sensory challenges prior to social interventions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s11689-021-09391-0.
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spelling pubmed-84619482021-09-24 Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study Patterson, Genevieve Cummings, Kaitlin K. Jung, Jiwon Okada, Nana J. Tottenham, Nim Bookheimer, Susan Y. Dapretto, Mirella Green, Shulamite A. J Neurodev Disord Research BACKGROUND: Social interaction often occurs in noisy environments with many extraneous sensory stimuli. This is especially relevant for youth with autism spectrum disorders (ASD) who commonly experience sensory over-responsivity (SOR) in addition to social challenges. However, the relationship between SOR and social difficulties is still poorly understood and thus rarely addressed in interventions. This study investigated the effect of auditory sensory distracters on neural processing of emotion identification in youth with ASD and the effects of increasing attention to social cues by priming participants with their own emotional faces. METHODS: While undergoing functional magnetic resonance imaging (fMRI), 30 youth with ASD and 24 typically developing (TD) age-matched controls (ages 8–17 years) identified faces as happy or angry with and without simultaneously hearing aversive environmental noises. Halfway through the task, participants also viewed videos of their own emotional faces. The relationship between parent-rated auditory SOR and brain responses during the task was also examined. RESULTS: Despite showing comparable behavioral performance on the task, ASD and TD youth demonstrated distinct patterns of neural activity. Compared to TD, ASD youth showed greater increases in amygdala, insula, and primary sensory regions when identifying emotions with noises compared to no sounds. After viewing videos of their own emotion faces, ASD youth showed greater increases in medial prefrontal cortex activation compared to TD youth. Within ASD youth, lower SOR was associated with reduced increased activity in subcortical regions after the prime and greater increased activity in the ventromedial prefrontal cortex after the prime, particularly in trials with noises. CONCLUSIONS: The results suggest that the sensory environment plays an important role in how ASD youth process social information. Additionally, we demonstrated that increasing attention to relevant social cues helps ASD youth engage frontal regions involved in higher-order social cognition, a mechanism that could be targeted in interventions. Importantly, the effect of the intervention may depend on individual differences in SOR, supporting the importance of pre-screening youth for sensory challenges prior to social interventions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s11689-021-09391-0. BioMed Central 2021-09-23 /pmc/articles/PMC8461948/ /pubmed/34556059 http://dx.doi.org/10.1186/s11689-021-09391-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Patterson, Genevieve
Cummings, Kaitlin K.
Jung, Jiwon
Okada, Nana J.
Tottenham, Nim
Bookheimer, Susan Y.
Dapretto, Mirella
Green, Shulamite A.
Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
title Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
title_full Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
title_fullStr Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
title_full_unstemmed Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
title_short Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
title_sort effects of sensory distraction and salience priming on emotion identification in autism: an fmri study
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8461948/
https://www.ncbi.nlm.nih.gov/pubmed/34556059
http://dx.doi.org/10.1186/s11689-021-09391-0
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