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Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study

BACKGROUND: Sensory over-responsivity (SOR) is an impairing sensory processing challenge in autism spectrum disorder (ASD) which shows heterogenous developmental trajectories and appears to improve into adulthood in some but not all autistic individuals. However, the neural mechanisms underlying int...

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Autores principales: Cakar, Melis E., Cummings, Kaitlin K., Bookheimer, Susan Y., Dapretto, Mirella, Green, Shulamite A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10566124/
https://www.ncbi.nlm.nih.gov/pubmed/37817282
http://dx.doi.org/10.1186/s13229-023-00571-4
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author Cakar, Melis E.
Cummings, Kaitlin K.
Bookheimer, Susan Y.
Dapretto, Mirella
Green, Shulamite A.
author_facet Cakar, Melis E.
Cummings, Kaitlin K.
Bookheimer, Susan Y.
Dapretto, Mirella
Green, Shulamite A.
author_sort Cakar, Melis E.
collection PubMed
description BACKGROUND: Sensory over-responsivity (SOR) is an impairing sensory processing challenge in autism spectrum disorder (ASD) which shows heterogenous developmental trajectories and appears to improve into adulthood in some but not all autistic individuals. However, the neural mechanisms underlying interindividual differences in these trajectories are currently unknown. METHODS: Here, we used functional magnetic resonance imaging (fMRI) to investigate the association between age and neural activity linearly and nonlinearly in response to mildly aversive sensory stimulation as well as how SOR severity moderates this association. Participants included 52 ASD (14F) and 41 (13F) typically developing (TD) youth, aged 8.6–18.0 years. RESULTS: We found that in pre-teens, ASD children showed widespread activation differences in sensorimotor, frontal and cerebellar regions compared to TD children, while there were fewer differences between ASD and TD teens. In TD youth, older age was associated with less activation in the prefrontal cortex. In contrast, in ASD youth, older age was associated with more engagement of sensory integration and emotion regulation regions. In particular, orbitofrontal and medial prefrontal cortices showed a nonlinear relationship with age in ASD, with an especially steep increase in sensory-evoked neural activity during the mid-to-late teen years. There was also an interaction between age and SOR severity in ASD youth such that these age-related trends were more apparent in youth with higher SOR. LIMITATIONS: The cross-sectional design limits causal interpretations of the data. Future longitudinal studies will be instrumental in determining how prefrontal engagement and SOR co-develop across adolescence. CONCLUSIONS: Our results suggest that enhanced recruitment of prefrontal regions may underlie age-related decreases in SOR for a subgroup of ASD youth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-023-00571-4.
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spelling pubmed-105661242023-10-12 Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study Cakar, Melis E. Cummings, Kaitlin K. Bookheimer, Susan Y. Dapretto, Mirella Green, Shulamite A. Mol Autism Research BACKGROUND: Sensory over-responsivity (SOR) is an impairing sensory processing challenge in autism spectrum disorder (ASD) which shows heterogenous developmental trajectories and appears to improve into adulthood in some but not all autistic individuals. However, the neural mechanisms underlying interindividual differences in these trajectories are currently unknown. METHODS: Here, we used functional magnetic resonance imaging (fMRI) to investigate the association between age and neural activity linearly and nonlinearly in response to mildly aversive sensory stimulation as well as how SOR severity moderates this association. Participants included 52 ASD (14F) and 41 (13F) typically developing (TD) youth, aged 8.6–18.0 years. RESULTS: We found that in pre-teens, ASD children showed widespread activation differences in sensorimotor, frontal and cerebellar regions compared to TD children, while there were fewer differences between ASD and TD teens. In TD youth, older age was associated with less activation in the prefrontal cortex. In contrast, in ASD youth, older age was associated with more engagement of sensory integration and emotion regulation regions. In particular, orbitofrontal and medial prefrontal cortices showed a nonlinear relationship with age in ASD, with an especially steep increase in sensory-evoked neural activity during the mid-to-late teen years. There was also an interaction between age and SOR severity in ASD youth such that these age-related trends were more apparent in youth with higher SOR. LIMITATIONS: The cross-sectional design limits causal interpretations of the data. Future longitudinal studies will be instrumental in determining how prefrontal engagement and SOR co-develop across adolescence. CONCLUSIONS: Our results suggest that enhanced recruitment of prefrontal regions may underlie age-related decreases in SOR for a subgroup of ASD youth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-023-00571-4. BioMed Central 2023-10-11 /pmc/articles/PMC10566124/ /pubmed/37817282 http://dx.doi.org/10.1186/s13229-023-00571-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Cakar, Melis E.
Cummings, Kaitlin K.
Bookheimer, Susan Y.
Dapretto, Mirella
Green, Shulamite A.
Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
title Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
title_full Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
title_fullStr Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
title_full_unstemmed Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
title_short Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
title_sort age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10566124/
https://www.ncbi.nlm.nih.gov/pubmed/37817282
http://dx.doi.org/10.1186/s13229-023-00571-4
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