Triple Interactions Between the Environment, Brain, and Behavior in Children: An ABCD Study

Dongmei Zhi; Rongtao Jiang; Godfrey Pearlson; Zening Fu; Shile Qi; Weizheng Yan; Aichen Feng; Ming Xu; Vince Calhoun; Jing Sui

doi:10.1016/j.biopsych.2023.12.019

Triple Interactions Between the Environment, Brain, and Behavior in Children: An ABCD Study

Biol Psychiatry. 2024 May 1;95(9):828-838. doi: 10.1016/j.biopsych.2023.12.019. Epub 2023 Dec 25.

Authors

Dongmei Zhi¹, Rongtao Jiang², Godfrey Pearlson³, Zening Fu⁴, Shile Qi⁵, Weizheng Yan⁶, Aichen Feng⁷, Ming Xu⁷, Vince Calhoun⁸, Jing Sui⁹

Affiliations

¹ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China.
² Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, Connecticut.
³ Department of Psychiatry and Neurobiology, Yale School of Medicine, New Haven, Connecticut.
⁴ Tri-institutional Center for Translational Research in Neuroimaging and Data Science, Georgia Institute of Technology, Emory University, and Georgia State University, Atlanta, Georgia.
⁵ College of Computer Science and Technology, Nanjing University of Aeronautics and Astronautics, Nanjing, China.
⁶ National Institute on Alcohol Abuse and Alcoholism, Lab of Neuroimaging, National Institutes of Health, Bethesda, Maryland.
⁷ Brainnetome Center and National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China; School of Artificial Intelligence, University of Chinese Academy of Sciences, Beijing, China.
⁸ Tri-institutional Center for Translational Research in Neuroimaging and Data Science, Georgia Institute of Technology, Emory University, and Georgia State University, Atlanta, Georgia. Electronic address: vince.calhoun@ece.gatech.edu.
⁹ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China; Tri-institutional Center for Translational Research in Neuroimaging and Data Science, Georgia Institute of Technology, Emory University, and Georgia State University, Atlanta, Georgia. Electronic address: kittysj@gmail.com.

PMID: 38151182
PMCID: PMC11006588 (available on 2025-05-01)
DOI: 10.1016/j.biopsych.2023.12.019

Abstract

Background: Environmental exposures play a crucial role in shaping children's behavioral development. However, the mechanisms by which these exposures interact with brain functional connectivity and influence behavior remain unexplored.

Methods: We investigated the comprehensive environment-brain-behavior triple interactions through rigorous association, prediction, and mediation analyses, while adjusting for multiple confounders. Particularly, we examined the predictive power of brain functional network connectivity (FNC) and 41 environmental exposures for 23 behaviors related to cognitive ability and mental health in 7655 children selected from the Adolescent Brain Cognitive Development (ABCD) Study at both baseline and follow-up.

Results: FNC demonstrated more predictability for cognitive abilities than for mental health, with cross-validation from the UK Biobank study (N = 20,852), highlighting the importance of thalamus and hippocampus in longitudinal prediction, while FNC+environment demonstrated more predictive power than FNC in both cross-sectional and longitudinal prediction of all behaviors, especially for mental health (r = 0.32-0.63). We found that family and neighborhood exposures were common critical environmental influencers on cognitive ability and mental health, which can be mediated by FNC significantly. Healthy perinatal development was a unique protective factor for higher cognitive ability, whereas sleep problems, family conflicts, and adverse school environments specifically increased risk of poor mental health.

Conclusions: This work revealed comprehensive environment-brain-behavior triple interactions based on the ABCD Study, identified cognitive control and default mode networks as the most predictive functional networks for a wide repertoire of behaviors, and underscored the long-lasting impact of critical environmental exposures on childhood development, in which sleep problems were the most prominent factors affecting mental health.

Keywords: ABCD; Cognition; Environmental exposure; Functional network connectivity; Individualized prediction; Mediation analysis; Mental health.

MeSH terms

Adolescent
Brain
Child
Cognition*
Cross-Sectional Studies
Humans
Magnetic Resonance Imaging
Mental Health
Sleep Wake Disorders*

Abstract

MeSH terms

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