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Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism

BACKGROUND: Autism spectrum disorder (ASD) is a complex neurodevelopmental condition, and multiple theories have emerged concerning core social deficits. While the social motivation hypothesis proposes that deficits in the social reward system cause individuals with ASD to engage less in social inte...

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Autores principales: Stavropoulos, Katherine Kuhl-Meltzoff, Carver, Leslie J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789641/
https://www.ncbi.nlm.nih.gov/pubmed/29423131
http://dx.doi.org/10.1186/s13229-018-0189-5
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author Stavropoulos, Katherine Kuhl-Meltzoff
Carver, Leslie J.
author_facet Stavropoulos, Katherine Kuhl-Meltzoff
Carver, Leslie J.
author_sort Stavropoulos, Katherine Kuhl-Meltzoff
collection PubMed
description BACKGROUND: Autism spectrum disorder (ASD) is a complex neurodevelopmental condition, and multiple theories have emerged concerning core social deficits. While the social motivation hypothesis proposes that deficits in the social reward system cause individuals with ASD to engage less in social interaction, the overly intense world hypothesis (sensory over-responsivity) proposes that individuals with ASD find stimuli to be too intense and may have hypersensitivity to social interaction, leading them to avoid these interactions. METHODS: EEG was recorded during reward anticipation and reward processing. Reward anticipation was measured using alpha asymmetry, and post-feedback theta was utilized to measure reward processing. Additionally, we calculated post-feedback alpha suppression to measure attention and salience. Participants were 6- to 8-year-olds with (N = 20) and without (N = 23) ASD. RESULTS: Children with ASD showed more left-dominant alpha suppression when anticipating rewards accompanied by nonsocial stimuli compared to social stimuli. During reward processing, children with ASD had less theta activity than typically developing (TD) children. Alpha activity after feedback showed the opposite pattern: children with ASD had greater alpha suppression than TD children. Significant correlations were observed between behavioral measures of autism severity and EEG activity in both the reward anticipation and reward processing time periods. CONCLUSIONS: The findings provide evidence that children with ASD have greater approach motivation prior to nonsocial (compared to social) stimuli. Results after feedback suggest that children with ASD evidence less robust activity thought to reflect evaluation and processing of rewards (e.g., theta) compared to TD children. However, children with ASD evidence greater alpha suppression after feedback compared to TD children. We hypothesize that post-feedback alpha suppression reflects general cognitive engagement—which suggests that children with ASD may experience feedback as overly intense. Taken together, these results suggest that aspects of both the social motivation hypothesis and the overly intense world hypothesis may be occurring simultaneously.
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spelling pubmed-57896412018-02-08 Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism Stavropoulos, Katherine Kuhl-Meltzoff Carver, Leslie J. Mol Autism Research BACKGROUND: Autism spectrum disorder (ASD) is a complex neurodevelopmental condition, and multiple theories have emerged concerning core social deficits. While the social motivation hypothesis proposes that deficits in the social reward system cause individuals with ASD to engage less in social interaction, the overly intense world hypothesis (sensory over-responsivity) proposes that individuals with ASD find stimuli to be too intense and may have hypersensitivity to social interaction, leading them to avoid these interactions. METHODS: EEG was recorded during reward anticipation and reward processing. Reward anticipation was measured using alpha asymmetry, and post-feedback theta was utilized to measure reward processing. Additionally, we calculated post-feedback alpha suppression to measure attention and salience. Participants were 6- to 8-year-olds with (N = 20) and without (N = 23) ASD. RESULTS: Children with ASD showed more left-dominant alpha suppression when anticipating rewards accompanied by nonsocial stimuli compared to social stimuli. During reward processing, children with ASD had less theta activity than typically developing (TD) children. Alpha activity after feedback showed the opposite pattern: children with ASD had greater alpha suppression than TD children. Significant correlations were observed between behavioral measures of autism severity and EEG activity in both the reward anticipation and reward processing time periods. CONCLUSIONS: The findings provide evidence that children with ASD have greater approach motivation prior to nonsocial (compared to social) stimuli. Results after feedback suggest that children with ASD evidence less robust activity thought to reflect evaluation and processing of rewards (e.g., theta) compared to TD children. However, children with ASD evidence greater alpha suppression after feedback compared to TD children. We hypothesize that post-feedback alpha suppression reflects general cognitive engagement—which suggests that children with ASD may experience feedback as overly intense. Taken together, these results suggest that aspects of both the social motivation hypothesis and the overly intense world hypothesis may be occurring simultaneously. BioMed Central 2018-01-30 /pmc/articles/PMC5789641/ /pubmed/29423131 http://dx.doi.org/10.1186/s13229-018-0189-5 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Stavropoulos, Katherine Kuhl-Meltzoff
Carver, Leslie J.
Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
title Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
title_full Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
title_fullStr Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
title_full_unstemmed Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
title_short Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
title_sort oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789641/
https://www.ncbi.nlm.nih.gov/pubmed/29423131
http://dx.doi.org/10.1186/s13229-018-0189-5
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