Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study
Abstract 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 relationsh...
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doaj-4dcaa019de20415b8645dac7016d9c1f2021-09-26T11:05:07ZengBMCJournal of Neurodevelopmental Disorders1866-19471866-19552021-09-0113111510.1186/s11689-021-09391-0Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI studyGenevieve Patterson0Kaitlin K. Cummings1Jiwon Jung2Nana J. Okada3Nim Tottenham4Susan Y. Bookheimer5Mirella Dapretto6Shulamite A. Green7Department of Psychology, University of DenverJane and Terry Semel Institute of Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California Los AngelesJane and Terry Semel Institute of Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California Los AngelesJane and Terry Semel Institute of Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California Los AngelesDepartment of Psychology, Columbia UniversityJane and Terry Semel Institute of Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California Los AngelesJane and Terry Semel Institute of Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California Los AngelesJane and Terry Semel Institute of Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California Los AngelesAbstract 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.https://doi.org/10.1186/s11689-021-09391-0AutismEmotionfMRISensory processingSensory over-responsivity |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Genevieve Patterson Kaitlin K. Cummings Jiwon Jung Nana J. Okada Nim Tottenham Susan Y. Bookheimer Mirella Dapretto Shulamite A. Green |
spellingShingle |
Genevieve Patterson Kaitlin K. Cummings Jiwon Jung Nana J. Okada Nim Tottenham Susan Y. Bookheimer Mirella Dapretto Shulamite A. Green Effects of sensory distraction and salience priming on emotion identification in autism: an fMRI study Journal of Neurodevelopmental Disorders Autism Emotion fMRI Sensory processing Sensory over-responsivity |
author_facet |
Genevieve Patterson Kaitlin K. Cummings Jiwon Jung Nana J. Okada Nim Tottenham Susan Y. Bookheimer Mirella Dapretto Shulamite A. Green |
author_sort |
Genevieve Patterson |
title |
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_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_sort |
effects of sensory distraction and salience priming on emotion identification in autism: an fmri study |
publisher |
BMC |
series |
Journal of Neurodevelopmental Disorders |
issn |
1866-1947 1866-1955 |
publishDate |
2021-09-01 |
description |
Abstract 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. |
topic |
Autism Emotion fMRI Sensory processing Sensory over-responsivity |
url |
https://doi.org/10.1186/s11689-021-09391-0 |
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