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Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits

Sensory atypicalities are particularly common in autism spectrum disorders (ASD). Nevertheless, our knowledge about the divergent functioning of the underlying somatosensory region and its association with ASD phenotype features is limited. We applied a data-driven approach to map the fine-grained v...

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Autores principales: Isakoglou, Christina, Haak, Koen V., Wolfers, Thomas, Floris, Dorothea L., Llera, Alberto, Oldehinkel, Marianne, Forde, Natalie J., Oakley, Bethany F. M., Tillmann, Julian, Holt, Rosemary J., Moessnang, Carolin, Loth, Eva, Bourgeron, Thomas, Baron-Cohen, Simon, Charman, Tony, Banaschewski, Tobias, Murphy, Declan G. M., Buitelaar, Jan K., Marquand, Andre F., Beckmann, Christian F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10374902/
https://www.ncbi.nlm.nih.gov/pubmed/37500630
http://dx.doi.org/10.1038/s41398-023-02559-3
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author Isakoglou, Christina
Haak, Koen V.
Wolfers, Thomas
Floris, Dorothea L.
Llera, Alberto
Oldehinkel, Marianne
Forde, Natalie J.
Oakley, Bethany F. M.
Tillmann, Julian
Holt, Rosemary J.
Moessnang, Carolin
Loth, Eva
Bourgeron, Thomas
Baron-Cohen, Simon
Charman, Tony
Banaschewski, Tobias
Murphy, Declan G. M.
Buitelaar, Jan K.
Marquand, Andre F.
Beckmann, Christian F.
author_facet Isakoglou, Christina
Haak, Koen V.
Wolfers, Thomas
Floris, Dorothea L.
Llera, Alberto
Oldehinkel, Marianne
Forde, Natalie J.
Oakley, Bethany F. M.
Tillmann, Julian
Holt, Rosemary J.
Moessnang, Carolin
Loth, Eva
Bourgeron, Thomas
Baron-Cohen, Simon
Charman, Tony
Banaschewski, Tobias
Murphy, Declan G. M.
Buitelaar, Jan K.
Marquand, Andre F.
Beckmann, Christian F.
author_sort Isakoglou, Christina
collection PubMed
description Sensory atypicalities are particularly common in autism spectrum disorders (ASD). Nevertheless, our knowledge about the divergent functioning of the underlying somatosensory region and its association with ASD phenotype features is limited. We applied a data-driven approach to map the fine-grained variations in functional connectivity of the primary somatosensory cortex (S1) to the rest of the brain in 240 autistic and 164 neurotypical individuals from the EU-AIMS LEAP dataset, aged between 7 and 30. We estimated the S1 connection topography (‘connectopy’) at rest and during the emotional face-matching (Hariri) task, an established measure of emotion reactivity, and accessed its association with a set of clinical and behavioral variables. We first demonstrated that the S1 connectopy is organized along a dorsoventral axis, mapping onto the S1 somatotopic organization. We then found that its spatial characteristics were linked to the individuals’ adaptive functioning skills, as measured by the Vineland Adaptive Behavior Scales, across the whole sample. Higher functional differentiation characterized the S1 connectopies of individuals with higher daily life adaptive skills. Notably, we detected significant differences between rest and the Hariri task in the S1 connectopies, as well as their projection maps onto the rest of the brain suggesting a task-modulating effect on S1 due to emotion processing. All in all, variation of adaptive skills appears to be reflected in the brain’s mesoscale neural circuitry, as shown by the S1 connectivity profile, which is also differentially modulated during rest and emotional processing.
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spelling pubmed-103749022023-07-29 Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits Isakoglou, Christina Haak, Koen V. Wolfers, Thomas Floris, Dorothea L. Llera, Alberto Oldehinkel, Marianne Forde, Natalie J. Oakley, Bethany F. M. Tillmann, Julian Holt, Rosemary J. Moessnang, Carolin Loth, Eva Bourgeron, Thomas Baron-Cohen, Simon Charman, Tony Banaschewski, Tobias Murphy, Declan G. M. Buitelaar, Jan K. Marquand, Andre F. Beckmann, Christian F. Transl Psychiatry Article Sensory atypicalities are particularly common in autism spectrum disorders (ASD). Nevertheless, our knowledge about the divergent functioning of the underlying somatosensory region and its association with ASD phenotype features is limited. We applied a data-driven approach to map the fine-grained variations in functional connectivity of the primary somatosensory cortex (S1) to the rest of the brain in 240 autistic and 164 neurotypical individuals from the EU-AIMS LEAP dataset, aged between 7 and 30. We estimated the S1 connection topography (‘connectopy’) at rest and during the emotional face-matching (Hariri) task, an established measure of emotion reactivity, and accessed its association with a set of clinical and behavioral variables. We first demonstrated that the S1 connectopy is organized along a dorsoventral axis, mapping onto the S1 somatotopic organization. We then found that its spatial characteristics were linked to the individuals’ adaptive functioning skills, as measured by the Vineland Adaptive Behavior Scales, across the whole sample. Higher functional differentiation characterized the S1 connectopies of individuals with higher daily life adaptive skills. Notably, we detected significant differences between rest and the Hariri task in the S1 connectopies, as well as their projection maps onto the rest of the brain suggesting a task-modulating effect on S1 due to emotion processing. All in all, variation of adaptive skills appears to be reflected in the brain’s mesoscale neural circuitry, as shown by the S1 connectivity profile, which is also differentially modulated during rest and emotional processing. Nature Publishing Group UK 2023-07-27 /pmc/articles/PMC10374902/ /pubmed/37500630 http://dx.doi.org/10.1038/s41398-023-02559-3 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Isakoglou, Christina
Haak, Koen V.
Wolfers, Thomas
Floris, Dorothea L.
Llera, Alberto
Oldehinkel, Marianne
Forde, Natalie J.
Oakley, Bethany F. M.
Tillmann, Julian
Holt, Rosemary J.
Moessnang, Carolin
Loth, Eva
Bourgeron, Thomas
Baron-Cohen, Simon
Charman, Tony
Banaschewski, Tobias
Murphy, Declan G. M.
Buitelaar, Jan K.
Marquand, Andre F.
Beckmann, Christian F.
Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits
title Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits
title_full Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits
title_fullStr Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits
title_full_unstemmed Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits
title_short Fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with ASD traits
title_sort fine-grained topographic organization within somatosensory cortex during resting-state and emotional face-matching task and its association with asd traits
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10374902/
https://www.ncbi.nlm.nih.gov/pubmed/37500630
http://dx.doi.org/10.1038/s41398-023-02559-3
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