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A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities

The rapid brain maturation in childhood and adolescence accompanies the development of socio-emotional functioning. However, it is unclear how the maturation of the neural activity drives the development of socio-emotional functioning and individual differences. This study aimed to reflect the age d...

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Autores principales: Xie, Shuqi, Liu, Jingjing, Hu, Yang, Liu, Wenjing, Ma, Changminghao, Jin, Shuyu, Zhang, Lei, Kang, Yinzhi, Ding, Yue, Zhang, Xiaochen, Hu, Zhishan, Cheng, Wenhong, Yang, Zhi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10649363/
https://www.ncbi.nlm.nih.gov/pubmed/37930841
http://dx.doi.org/10.1093/scan/nsad062
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author Xie, Shuqi
Liu, Jingjing
Hu, Yang
Liu, Wenjing
Ma, Changminghao
Jin, Shuyu
Zhang, Lei
Kang, Yinzhi
Ding, Yue
Zhang, Xiaochen
Hu, Zhishan
Cheng, Wenhong
Yang, Zhi
author_facet Xie, Shuqi
Liu, Jingjing
Hu, Yang
Liu, Wenjing
Ma, Changminghao
Jin, Shuyu
Zhang, Lei
Kang, Yinzhi
Ding, Yue
Zhang, Xiaochen
Hu, Zhishan
Cheng, Wenhong
Yang, Zhi
author_sort Xie, Shuqi
collection PubMed
description The rapid brain maturation in childhood and adolescence accompanies the development of socio-emotional functioning. However, it is unclear how the maturation of the neural activity drives the development of socio-emotional functioning and individual differences. This study aimed to reflect the age dependence of inter-individual differences in brain responses to socio-emotional scenarios and to develop naturalistic imaging indicators to assess the maturity of socio-emotional ability at the individual level. Using three independent naturalistic imaging datasets containing healthy participants (n = 111, 21 and 122), we found and validated that age-modulated inter-individual concordance of brain responses to socio-emotional movies in specific brain regions. The similarity of an individual’s brain response to the average response of older participants was defined as response typicality, which predicted an individual’s emotion regulation strategies in adolescence and theory of mind (ToM) in childhood. Its predictive power was not superseded by age, sex, cognitive performance or executive function. We further showed that the movie’s valence and arousal ratings grounded the response typicality. The findings highlight that forming typical brain response patterns may be a neural phenotype underlying the maturation of socio-emotional ability. The proposed response typicality represents a neuroimaging approach to measure individuals’ maturity of cognitive reappraisal and ToM.
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spelling pubmed-106493632023-11-01 A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities Xie, Shuqi Liu, Jingjing Hu, Yang Liu, Wenjing Ma, Changminghao Jin, Shuyu Zhang, Lei Kang, Yinzhi Ding, Yue Zhang, Xiaochen Hu, Zhishan Cheng, Wenhong Yang, Zhi Soc Cogn Affect Neurosci Original Manuscript The rapid brain maturation in childhood and adolescence accompanies the development of socio-emotional functioning. However, it is unclear how the maturation of the neural activity drives the development of socio-emotional functioning and individual differences. This study aimed to reflect the age dependence of inter-individual differences in brain responses to socio-emotional scenarios and to develop naturalistic imaging indicators to assess the maturity of socio-emotional ability at the individual level. Using three independent naturalistic imaging datasets containing healthy participants (n = 111, 21 and 122), we found and validated that age-modulated inter-individual concordance of brain responses to socio-emotional movies in specific brain regions. The similarity of an individual’s brain response to the average response of older participants was defined as response typicality, which predicted an individual’s emotion regulation strategies in adolescence and theory of mind (ToM) in childhood. Its predictive power was not superseded by age, sex, cognitive performance or executive function. We further showed that the movie’s valence and arousal ratings grounded the response typicality. The findings highlight that forming typical brain response patterns may be a neural phenotype underlying the maturation of socio-emotional ability. The proposed response typicality represents a neuroimaging approach to measure individuals’ maturity of cognitive reappraisal and ToM. Oxford University Press 2023-11-01 /pmc/articles/PMC10649363/ /pubmed/37930841 http://dx.doi.org/10.1093/scan/nsad062 Text en © The Author(s) 2023. Published by Oxford University Press. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Manuscript
Xie, Shuqi
Liu, Jingjing
Hu, Yang
Liu, Wenjing
Ma, Changminghao
Jin, Shuyu
Zhang, Lei
Kang, Yinzhi
Ding, Yue
Zhang, Xiaochen
Hu, Zhishan
Cheng, Wenhong
Yang, Zhi
A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
title A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
title_full A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
title_fullStr A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
title_full_unstemmed A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
title_short A normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
title_sort normative model of brain responses to social scenarios reflects the maturity of children and adolescents’ social–emotional abilities
topic Original Manuscript
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10649363/
https://www.ncbi.nlm.nih.gov/pubmed/37930841
http://dx.doi.org/10.1093/scan/nsad062
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