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Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study

AIMS: Increasing evidence indicates that major neurodevelopmental disorders have potential links to abnormal cerebellar development. However, the developmental trajectories of cerebellar subregions from childhood to adolescence are lacking, and it is not clear how emotional and behavioral problems a...

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Autores principales: Wang, Yanpei, Ma, Leilei, Chen, Rui, Liu, Ningyu, Zhang, Haibo, Li, Yuanyuan, Wang, Jiali, Hu, Mingming, Zhao, Gai, Men, Weiwei, Tan, Shuping, Gao, Jia‐Hong, Qin, Shaozheng, He, Yong, Dong, Qi, Tao, Sha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580368/
https://www.ncbi.nlm.nih.gov/pubmed/37287420
http://dx.doi.org/10.1111/cns.14286
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author Wang, Yanpei
Ma, Leilei
Chen, Rui
Liu, Ningyu
Zhang, Haibo
Li, Yuanyuan
Wang, Jiali
Hu, Mingming
Zhao, Gai
Men, Weiwei
Tan, Shuping
Gao, Jia‐Hong
Qin, Shaozheng
He, Yong
Dong, Qi
Tao, Sha
author_facet Wang, Yanpei
Ma, Leilei
Chen, Rui
Liu, Ningyu
Zhang, Haibo
Li, Yuanyuan
Wang, Jiali
Hu, Mingming
Zhao, Gai
Men, Weiwei
Tan, Shuping
Gao, Jia‐Hong
Qin, Shaozheng
He, Yong
Dong, Qi
Tao, Sha
author_sort Wang, Yanpei
collection PubMed
description AIMS: Increasing evidence indicates that major neurodevelopmental disorders have potential links to abnormal cerebellar development. However, the developmental trajectories of cerebellar subregions from childhood to adolescence are lacking, and it is not clear how emotional and behavioral problems affect them. We aim to map the developmental trajectories of gray matter volume (GMV), cortical thickness (CT), and surface area (SA) in cerebellar subregions from childhood to adolescence and examine how emotional and behavioral problems change the cerebellar development trajectory in a longitudinal cohort study. METHOD: This population‐based longitudinal cohort study used data on a representative sample of 695 children. Emotional and behavioral problems were assessed at baseline and at three annual follow‐ups with the Strengths and Difficulties Questionnaire (SDQ). RESULTS: Using an innovative automated image segmentation technique, we quantified the GMV, CT, and SA of the whole cerebellum and 24 subdivisions (lobules I‐VI, VIIB, VIIIA&B, and IX‐X plus crus I‐II) with 1319 MRI scans from a large longitudinal sample of 695 subjects aged 6–15 years and mapped their developmental trajectories. We also examined sex differences and found that boys showed more linear growth, while girls showed more nonlinear growth. Boys and girls showed nonlinear growth in the cerebellar subregions; however, girls reached the peak earlier than boys. Further analysis found that emotional and behavioral problems modulated cerebellar development. Specifically, emotional symptoms impede the expansion of the SA of the cerebellar cortex, and no gender differences; conduct problems lead to inadequate cerebellar GMV development only in girls, but not boys; hyperactivity/inattention delays the development of cerebellar GMV and SA, with left cerebellar GMV, right VIIIA GMV and SA in boys and left V GMV and SA in girls; peer problems disrupt CT growth and SA expansion, resulting in delayed GMV development, with bilateral IV, right X CT in boys and right Crus I GMV, left V SA in girls; and prosocial behavior problems impede the expansion of the SA and lead to excessive CT growth, with bilateral IV, V, right VI CT, left cerebellum SA in boys and right Crus I GMV in girls. CONCLUSIONS: This study maps the developmental trajectories of GMV, CT, and SA in cerebellar subregions from childhood to adolescence. In addition, we provide the first evidence for how emotional and behavioral problems affect the dynamic development of GMV, CT, and SA in the cerebellum, which provides an important basis and guidance for the prevention and intervention of cognitive and emotional behavioral problems in the future.
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spelling pubmed-105803682023-10-18 Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study Wang, Yanpei Ma, Leilei Chen, Rui Liu, Ningyu Zhang, Haibo Li, Yuanyuan Wang, Jiali Hu, Mingming Zhao, Gai Men, Weiwei Tan, Shuping Gao, Jia‐Hong Qin, Shaozheng He, Yong Dong, Qi Tao, Sha CNS Neurosci Ther Original Articles AIMS: Increasing evidence indicates that major neurodevelopmental disorders have potential links to abnormal cerebellar development. However, the developmental trajectories of cerebellar subregions from childhood to adolescence are lacking, and it is not clear how emotional and behavioral problems affect them. We aim to map the developmental trajectories of gray matter volume (GMV), cortical thickness (CT), and surface area (SA) in cerebellar subregions from childhood to adolescence and examine how emotional and behavioral problems change the cerebellar development trajectory in a longitudinal cohort study. METHOD: This population‐based longitudinal cohort study used data on a representative sample of 695 children. Emotional and behavioral problems were assessed at baseline and at three annual follow‐ups with the Strengths and Difficulties Questionnaire (SDQ). RESULTS: Using an innovative automated image segmentation technique, we quantified the GMV, CT, and SA of the whole cerebellum and 24 subdivisions (lobules I‐VI, VIIB, VIIIA&B, and IX‐X plus crus I‐II) with 1319 MRI scans from a large longitudinal sample of 695 subjects aged 6–15 years and mapped their developmental trajectories. We also examined sex differences and found that boys showed more linear growth, while girls showed more nonlinear growth. Boys and girls showed nonlinear growth in the cerebellar subregions; however, girls reached the peak earlier than boys. Further analysis found that emotional and behavioral problems modulated cerebellar development. Specifically, emotional symptoms impede the expansion of the SA of the cerebellar cortex, and no gender differences; conduct problems lead to inadequate cerebellar GMV development only in girls, but not boys; hyperactivity/inattention delays the development of cerebellar GMV and SA, with left cerebellar GMV, right VIIIA GMV and SA in boys and left V GMV and SA in girls; peer problems disrupt CT growth and SA expansion, resulting in delayed GMV development, with bilateral IV, right X CT in boys and right Crus I GMV, left V SA in girls; and prosocial behavior problems impede the expansion of the SA and lead to excessive CT growth, with bilateral IV, V, right VI CT, left cerebellum SA in boys and right Crus I GMV in girls. CONCLUSIONS: This study maps the developmental trajectories of GMV, CT, and SA in cerebellar subregions from childhood to adolescence. In addition, we provide the first evidence for how emotional and behavioral problems affect the dynamic development of GMV, CT, and SA in the cerebellum, which provides an important basis and guidance for the prevention and intervention of cognitive and emotional behavioral problems in the future. John Wiley and Sons Inc. 2023-06-08 /pmc/articles/PMC10580368/ /pubmed/37287420 http://dx.doi.org/10.1111/cns.14286 Text en © 2023 The Authors. CNS Neuroscience & Therapeutics published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Wang, Yanpei
Ma, Leilei
Chen, Rui
Liu, Ningyu
Zhang, Haibo
Li, Yuanyuan
Wang, Jiali
Hu, Mingming
Zhao, Gai
Men, Weiwei
Tan, Shuping
Gao, Jia‐Hong
Qin, Shaozheng
He, Yong
Dong, Qi
Tao, Sha
Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study
title Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study
title_full Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study
title_fullStr Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study
title_full_unstemmed Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study
title_short Emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: A longitudinal cohort study
title_sort emotional and behavioral problems change the development of cerebellar gray matter volume, thickness, and surface area from childhood to adolescence: a longitudinal cohort study
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580368/
https://www.ncbi.nlm.nih.gov/pubmed/37287420
http://dx.doi.org/10.1111/cns.14286
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