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Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study

BACKGROUND: Attenuated social attention is a key marker of autism spectrum disorder (ASD). Recent neuroimaging findings also emphasize an altered processing of sensory salience in ASD. The locus coeruleus–norepinephrine system (LC-NE) has been established as a modulator of this sensory salience proc...

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Autores principales: Bast, Nico, Mason, Luke, Ecker, Christine, Baumeister, Sarah, Banaschewski, Tobias, Jones, Emily J. H., Murphy, Declan G. M., Buitelaar, Jan K., Loth, Eva, Pandina, Gahan, Freitag, Christine M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9912590/
https://www.ncbi.nlm.nih.gov/pubmed/36759875
http://dx.doi.org/10.1186/s13229-023-00537-6
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author Bast, Nico
Mason, Luke
Ecker, Christine
Baumeister, Sarah
Banaschewski, Tobias
Jones, Emily J. H.
Murphy, Declan G. M.
Buitelaar, Jan K.
Loth, Eva
Pandina, Gahan
Freitag, Christine M.
author_facet Bast, Nico
Mason, Luke
Ecker, Christine
Baumeister, Sarah
Banaschewski, Tobias
Jones, Emily J. H.
Murphy, Declan G. M.
Buitelaar, Jan K.
Loth, Eva
Pandina, Gahan
Freitag, Christine M.
author_sort Bast, Nico
collection PubMed
description BACKGROUND: Attenuated social attention is a key marker of autism spectrum disorder (ASD). Recent neuroimaging findings also emphasize an altered processing of sensory salience in ASD. The locus coeruleus–norepinephrine system (LC-NE) has been established as a modulator of this sensory salience processing (SSP). We tested the hypothesis that altered LC-NE functioning contributes to different SSP and results in diverging social attention in ASD. METHODS: We analyzed the baseline eye-tracking data of the EU-AIMS Longitudinal European Autism Project (LEAP) for subgroups of autistic participants (n = 166, age = 6–30 years, IQ = 61–138, gender [female/male] = 41/125) or neurotypical development (TD; n = 166, age = 6–30 years, IQ = 63–138, gender [female/male] = 49/117) that were matched for demographic variables and data quality. Participants watched brief movie scenes (k = 85) depicting humans in social situations (human) or without humans (non-human). SSP was estimated by gazes on physical and motion salience and a corresponding pupillary response that indexes phasic activity of the LC-NE. Social attention is estimated by gazes on faces via manual areas of interest definition. SSP is compared between groups and related to social attention by linear mixed models that consider temporal dynamics within scenes. Models are controlled for comorbid psychopathology, gaze behavior, and luminance. RESULTS: We found no group differences in gazes on salience, whereas pupillary responses were associated with altered gazes on physical and motion salience. In ASD compared to TD, we observed pupillary responses that were higher for non-human scenes and lower for human scenes. In ASD, we observed lower gazes on faces across the duration of the scenes. Crucially, this different social attention was influenced by gazes on physical salience and moderated by pupillary responses. LIMITATIONS: The naturalistic study design precluded experimental manipulations and stimulus control, while effect sizes were small to moderate. Covariate effects of age and IQ indicate that the findings differ between age and developmental subgroups. CONCLUSIONS: Pupillary responses as a proxy of LC-NE phasic activity during visual attention are suggested to modulate sensory salience processing and contribute to attenuated social attention in ASD. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-023-00537-6.
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spelling pubmed-99125902023-02-11 Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study Bast, Nico Mason, Luke Ecker, Christine Baumeister, Sarah Banaschewski, Tobias Jones, Emily J. H. Murphy, Declan G. M. Buitelaar, Jan K. Loth, Eva Pandina, Gahan Freitag, Christine M. Mol Autism Research BACKGROUND: Attenuated social attention is a key marker of autism spectrum disorder (ASD). Recent neuroimaging findings also emphasize an altered processing of sensory salience in ASD. The locus coeruleus–norepinephrine system (LC-NE) has been established as a modulator of this sensory salience processing (SSP). We tested the hypothesis that altered LC-NE functioning contributes to different SSP and results in diverging social attention in ASD. METHODS: We analyzed the baseline eye-tracking data of the EU-AIMS Longitudinal European Autism Project (LEAP) for subgroups of autistic participants (n = 166, age = 6–30 years, IQ = 61–138, gender [female/male] = 41/125) or neurotypical development (TD; n = 166, age = 6–30 years, IQ = 63–138, gender [female/male] = 49/117) that were matched for demographic variables and data quality. Participants watched brief movie scenes (k = 85) depicting humans in social situations (human) or without humans (non-human). SSP was estimated by gazes on physical and motion salience and a corresponding pupillary response that indexes phasic activity of the LC-NE. Social attention is estimated by gazes on faces via manual areas of interest definition. SSP is compared between groups and related to social attention by linear mixed models that consider temporal dynamics within scenes. Models are controlled for comorbid psychopathology, gaze behavior, and luminance. RESULTS: We found no group differences in gazes on salience, whereas pupillary responses were associated with altered gazes on physical and motion salience. In ASD compared to TD, we observed pupillary responses that were higher for non-human scenes and lower for human scenes. In ASD, we observed lower gazes on faces across the duration of the scenes. Crucially, this different social attention was influenced by gazes on physical salience and moderated by pupillary responses. LIMITATIONS: The naturalistic study design precluded experimental manipulations and stimulus control, while effect sizes were small to moderate. Covariate effects of age and IQ indicate that the findings differ between age and developmental subgroups. CONCLUSIONS: Pupillary responses as a proxy of LC-NE phasic activity during visual attention are suggested to modulate sensory salience processing and contribute to attenuated social attention in ASD. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-023-00537-6. BioMed Central 2023-02-09 /pmc/articles/PMC9912590/ /pubmed/36759875 http://dx.doi.org/10.1186/s13229-023-00537-6 Text en © The Author(s) 2023 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
Bast, Nico
Mason, Luke
Ecker, Christine
Baumeister, Sarah
Banaschewski, Tobias
Jones, Emily J. H.
Murphy, Declan G. M.
Buitelaar, Jan K.
Loth, Eva
Pandina, Gahan
Freitag, Christine M.
Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
title Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
title_full Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
title_fullStr Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
title_full_unstemmed Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
title_short Sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
title_sort sensory salience processing moderates attenuated gazes on faces in autism spectrum disorder: a case–control study
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9912590/
https://www.ncbi.nlm.nih.gov/pubmed/36759875
http://dx.doi.org/10.1186/s13229-023-00537-6
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