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Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children

BACKGROUND: Elevated or reduced responses to sensory stimuli, known as sensory features, are common in autistic individuals and often impact quality of life. Little is known about the neurobiological basis of sensory features in autistic children. However, the brainstem may offer critical insights a...

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Autores principales: Surgent, Olivia, Riaz, Ali, Ausderau, Karla K., Adluru, Nagesh, Kirk, Gregory R., Guerrero-Gonzalez, Jose, Skaletski, Emily C., Kecskemeti, Steven R., Dean III, Douglas C, Weismer, Susan Ellis, Alexander, Andrew L., Travers, Brittany G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9762648/
https://www.ncbi.nlm.nih.gov/pubmed/36536467
http://dx.doi.org/10.1186/s13229-022-00524-3
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author Surgent, Olivia
Riaz, Ali
Ausderau, Karla K.
Adluru, Nagesh
Kirk, Gregory R.
Guerrero-Gonzalez, Jose
Skaletski, Emily C.
Kecskemeti, Steven R.
Dean III, Douglas C
Weismer, Susan Ellis
Alexander, Andrew L.
Travers, Brittany G.
author_facet Surgent, Olivia
Riaz, Ali
Ausderau, Karla K.
Adluru, Nagesh
Kirk, Gregory R.
Guerrero-Gonzalez, Jose
Skaletski, Emily C.
Kecskemeti, Steven R.
Dean III, Douglas C
Weismer, Susan Ellis
Alexander, Andrew L.
Travers, Brittany G.
author_sort Surgent, Olivia
collection PubMed
description BACKGROUND: Elevated or reduced responses to sensory stimuli, known as sensory features, are common in autistic individuals and often impact quality of life. Little is known about the neurobiological basis of sensory features in autistic children. However, the brainstem may offer critical insights as it has been associated with both basic sensory processing and core features of autism. METHODS: Diffusion-weighted imaging (DWI) and parent-report of sensory features were acquired from 133 children (61 autistic children with and 72 non-autistic children, 6–11 years-old). Leveraging novel DWI processing techniques, we investigated the relationship between sensory features and white matter microstructure properties (free-water-elimination-corrected fractional anisotropy [FA] and mean diffusivity [MD]) in precisely delineated brainstem white matter tracts. Follow-up analyses assessed relationships between microstructure and sensory response patterns/modalities and analyzed whole brain white matter using voxel-based analysis. RESULTS: Results revealed distinct relationships between brainstem microstructure and sensory features in autistic children compared to non-autistic children. In autistic children, more prominent sensory features were generally associated with lower MD. Further, in autistic children, sensory hyporesponsiveness and tactile responsivity were strongly associated with white matter microstructure in nearly all brainstem tracts. Follow-up voxel-based analyses confirmed that these relationships were more prominent in the brainstem/cerebellum, with additional sensory-brain findings in the autistic group in the white matter of the primary motor and somatosensory cortices, the occipital lobe, the inferior parietal lobe, and the thalamic projections. LIMITATIONS: All participants communicated via spoken language and acclimated to the sensory environment of an MRI session, which should be considered when assessing the generalizability of this work to the whole of the autism spectrum. CONCLUSIONS: These findings suggest unique brainstem white matter contributions to sensory features in autistic children compared to non-autistic children. The brainstem correlates of sensory features underscore the potential reflex-like nature of behavioral responses to sensory stimuli in autism and have implications for how we conceptualize and address sensory features in autistic populations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-022-00524-3.
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spelling pubmed-97626482022-12-20 Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children Surgent, Olivia Riaz, Ali Ausderau, Karla K. Adluru, Nagesh Kirk, Gregory R. Guerrero-Gonzalez, Jose Skaletski, Emily C. Kecskemeti, Steven R. Dean III, Douglas C Weismer, Susan Ellis Alexander, Andrew L. Travers, Brittany G. Mol Autism Research BACKGROUND: Elevated or reduced responses to sensory stimuli, known as sensory features, are common in autistic individuals and often impact quality of life. Little is known about the neurobiological basis of sensory features in autistic children. However, the brainstem may offer critical insights as it has been associated with both basic sensory processing and core features of autism. METHODS: Diffusion-weighted imaging (DWI) and parent-report of sensory features were acquired from 133 children (61 autistic children with and 72 non-autistic children, 6–11 years-old). Leveraging novel DWI processing techniques, we investigated the relationship between sensory features and white matter microstructure properties (free-water-elimination-corrected fractional anisotropy [FA] and mean diffusivity [MD]) in precisely delineated brainstem white matter tracts. Follow-up analyses assessed relationships between microstructure and sensory response patterns/modalities and analyzed whole brain white matter using voxel-based analysis. RESULTS: Results revealed distinct relationships between brainstem microstructure and sensory features in autistic children compared to non-autistic children. In autistic children, more prominent sensory features were generally associated with lower MD. Further, in autistic children, sensory hyporesponsiveness and tactile responsivity were strongly associated with white matter microstructure in nearly all brainstem tracts. Follow-up voxel-based analyses confirmed that these relationships were more prominent in the brainstem/cerebellum, with additional sensory-brain findings in the autistic group in the white matter of the primary motor and somatosensory cortices, the occipital lobe, the inferior parietal lobe, and the thalamic projections. LIMITATIONS: All participants communicated via spoken language and acclimated to the sensory environment of an MRI session, which should be considered when assessing the generalizability of this work to the whole of the autism spectrum. CONCLUSIONS: These findings suggest unique brainstem white matter contributions to sensory features in autistic children compared to non-autistic children. The brainstem correlates of sensory features underscore the potential reflex-like nature of behavioral responses to sensory stimuli in autism and have implications for how we conceptualize and address sensory features in autistic populations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-022-00524-3. BioMed Central 2022-12-19 /pmc/articles/PMC9762648/ /pubmed/36536467 http://dx.doi.org/10.1186/s13229-022-00524-3 Text en © The Author(s) 2022 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
Surgent, Olivia
Riaz, Ali
Ausderau, Karla K.
Adluru, Nagesh
Kirk, Gregory R.
Guerrero-Gonzalez, Jose
Skaletski, Emily C.
Kecskemeti, Steven R.
Dean III, Douglas C
Weismer, Susan Ellis
Alexander, Andrew L.
Travers, Brittany G.
Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
title Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
title_full Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
title_fullStr Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
title_full_unstemmed Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
title_short Brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
title_sort brainstem white matter microstructure is associated with hyporesponsiveness and overall sensory features in autistic children
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9762648/
https://www.ncbi.nlm.nih.gov/pubmed/36536467
http://dx.doi.org/10.1186/s13229-022-00524-3
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