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Social attention during object engagement: toward a cross-species measure of preferential social orienting

BACKGROUND: A central challenge in preclinical research investigating the biology of autism spectrum disorder (ASD) is the translation of ASD-related social phenotypes across humans and animal models. Social orienting, an observable, evolutionarily conserved behavior, represents a promising cross-sp...

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Autores principales: Weichselbaum, Claire, Hendrix, Nicole, Albright, Jordan, Dougherty, Joseph D., Botteron, Kelly N., Constantino, John N., Marrus, Natasha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9749210/
https://www.ncbi.nlm.nih.gov/pubmed/36517753
http://dx.doi.org/10.1186/s11689-022-09467-5
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author Weichselbaum, Claire
Hendrix, Nicole
Albright, Jordan
Dougherty, Joseph D.
Botteron, Kelly N.
Constantino, John N.
Marrus, Natasha
author_facet Weichselbaum, Claire
Hendrix, Nicole
Albright, Jordan
Dougherty, Joseph D.
Botteron, Kelly N.
Constantino, John N.
Marrus, Natasha
author_sort Weichselbaum, Claire
collection PubMed
description BACKGROUND: A central challenge in preclinical research investigating the biology of autism spectrum disorder (ASD) is the translation of ASD-related social phenotypes across humans and animal models. Social orienting, an observable, evolutionarily conserved behavior, represents a promising cross-species ASD phenotype given that disrupted social orienting is an early-emerging ASD feature with evidence for predicting familial recurrence. Here, we adapt a competing-stimulus social orienting task from domesticated dogs to naturalistic play behavior in human toddlers and test whether this approach indexes decreased social orienting in ASD. METHODS: Play behavior was coded from the Autism Diagnostic Observation Schedule (ADOS) in two samples of toddlers, each with and without ASD. Sample 1 (n = 16) consisted of community-ascertained research participants, while Sample 2 involved a prospective study of infants at a high or low familial liability for ASD (n = 67). Coding quantified the child’s looks towards the experimenter and caregiver, a social stimulus, while playing with high-interest toys, a non-social stimulus. A competing-stimulus measure of “Social Attention During Object Engagement” (SADOE) was calculated by dividing the number of social looks by total time spent playing with toys. SADOE was compared based on ASD diagnosis and differing familial liability for ASD. RESULTS: In both samples, toddlers with ASD exhibited significantly lower SADOE compared to toddlers without ASD, with large effect sizes (Hedges’ g ≥ 0.92) driven by a lower frequency of child-initiated spontaneous looks. Among toddlers at high familial likelihood of ASD, toddlers with ASD showed lower SADOE than toddlers without ASD, while SADOE did not differ based on presence or absence of familial ASD risk alone. SADOE correlated negatively with ADOS social affect calibrated severity scores and positively with the Communication and Symbolic Behavior Scales social subscale. In a binary logistic regression model, SADOE alone correctly classified 74.1% of cases, which rose to 85.2% when combined with cognitive development. CONCLUSIONS: This work suggests that a brief behavioral measure pitting a high-interest nonsocial stimulus against the innate draw of social partners can serve as a feasible cross-species measure of social orienting, with implications for genetically informative behavioral phenotyping of social deficits in ASD and other neurodevelopmental disorders.
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spelling pubmed-97492102022-12-15 Social attention during object engagement: toward a cross-species measure of preferential social orienting Weichselbaum, Claire Hendrix, Nicole Albright, Jordan Dougherty, Joseph D. Botteron, Kelly N. Constantino, John N. Marrus, Natasha J Neurodev Disord Research BACKGROUND: A central challenge in preclinical research investigating the biology of autism spectrum disorder (ASD) is the translation of ASD-related social phenotypes across humans and animal models. Social orienting, an observable, evolutionarily conserved behavior, represents a promising cross-species ASD phenotype given that disrupted social orienting is an early-emerging ASD feature with evidence for predicting familial recurrence. Here, we adapt a competing-stimulus social orienting task from domesticated dogs to naturalistic play behavior in human toddlers and test whether this approach indexes decreased social orienting in ASD. METHODS: Play behavior was coded from the Autism Diagnostic Observation Schedule (ADOS) in two samples of toddlers, each with and without ASD. Sample 1 (n = 16) consisted of community-ascertained research participants, while Sample 2 involved a prospective study of infants at a high or low familial liability for ASD (n = 67). Coding quantified the child’s looks towards the experimenter and caregiver, a social stimulus, while playing with high-interest toys, a non-social stimulus. A competing-stimulus measure of “Social Attention During Object Engagement” (SADOE) was calculated by dividing the number of social looks by total time spent playing with toys. SADOE was compared based on ASD diagnosis and differing familial liability for ASD. RESULTS: In both samples, toddlers with ASD exhibited significantly lower SADOE compared to toddlers without ASD, with large effect sizes (Hedges’ g ≥ 0.92) driven by a lower frequency of child-initiated spontaneous looks. Among toddlers at high familial likelihood of ASD, toddlers with ASD showed lower SADOE than toddlers without ASD, while SADOE did not differ based on presence or absence of familial ASD risk alone. SADOE correlated negatively with ADOS social affect calibrated severity scores and positively with the Communication and Symbolic Behavior Scales social subscale. In a binary logistic regression model, SADOE alone correctly classified 74.1% of cases, which rose to 85.2% when combined with cognitive development. CONCLUSIONS: This work suggests that a brief behavioral measure pitting a high-interest nonsocial stimulus against the innate draw of social partners can serve as a feasible cross-species measure of social orienting, with implications for genetically informative behavioral phenotyping of social deficits in ASD and other neurodevelopmental disorders. BioMed Central 2022-12-14 /pmc/articles/PMC9749210/ /pubmed/36517753 http://dx.doi.org/10.1186/s11689-022-09467-5 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
Weichselbaum, Claire
Hendrix, Nicole
Albright, Jordan
Dougherty, Joseph D.
Botteron, Kelly N.
Constantino, John N.
Marrus, Natasha
Social attention during object engagement: toward a cross-species measure of preferential social orienting
title Social attention during object engagement: toward a cross-species measure of preferential social orienting
title_full Social attention during object engagement: toward a cross-species measure of preferential social orienting
title_fullStr Social attention during object engagement: toward a cross-species measure of preferential social orienting
title_full_unstemmed Social attention during object engagement: toward a cross-species measure of preferential social orienting
title_short Social attention during object engagement: toward a cross-species measure of preferential social orienting
title_sort social attention during object engagement: toward a cross-species measure of preferential social orienting
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9749210/
https://www.ncbi.nlm.nih.gov/pubmed/36517753
http://dx.doi.org/10.1186/s11689-022-09467-5
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