Structure-function coupling within the reward network in preschool children predicts executive functioning in later childhood

Shi Yu Chan; Zi Yan Ong; Zhen Ming Ngoh; Yap Seng Chong; Juan H Zhou; Marielle V Fortier; Lourdes M Daniel; Anqi Qiu; Michael J Meaney; Ai Peng Tan

doi:10.1016/j.dcn.2022.101107

Structure-function coupling within the reward network in preschool children predicts executive functioning in later childhood

Dev Cogn Neurosci. 2022 Jun:55:101107. doi: 10.1016/j.dcn.2022.101107. Epub 2022 Mar 30.

Authors

Affiliations

¹ Singapore Institute for Clinical Sciences (SICS), A⁎STAR Research Entities (ARES), Singapore.
² Singapore Institute for Clinical Sciences (SICS), A⁎STAR Research Entities (ARES), Singapore; Yong Loo Lin School of Medicine, National University of Singapore (NUS), Singapore; Department of Obstetrics and Gynaecology, National University Health System, Singapore.
³ Yong Loo Lin School of Medicine, National University of Singapore (NUS), Singapore; Department of Electrical and Computer Engineering, National University of Singapore (NUS), Singapore.
⁴ Department of Diagnostic and Interventional Imaging, KK Women's and Children's Hospital, Singapore.
⁵ Department of Child Development, KK Women's and Children's Hospital, Singapore.
⁶ Department of Biomedical Engineering, National University of Singapore (NUS), Singapore; The N.1 Institute for Health, National University of Singapore (NUS), Singapore; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, USA.
⁷ Singapore Institute for Clinical Sciences (SICS), A⁎STAR Research Entities (ARES), Singapore; Yong Loo Lin School of Medicine, National University of Singapore (NUS), Singapore; Department of Psychiatry and Douglas Mental Health University Institute, McGill University, Montreal, Canada.
⁸ Singapore Institute for Clinical Sciences (SICS), A⁎STAR Research Entities (ARES), Singapore; Yong Loo Lin School of Medicine, National University of Singapore (NUS), Singapore; Department of Diagnostic Imaging, National University Health System, Singapore. Electronic address: ai_peng_tan@nuhs.edu.sg.

Abstract

Early differences in reward behavior have been linked to executive functioning development. The nucleus accumbens (NAc) and orbitofrontal cortex (OFC) are activated by reward-related tasks and identified as key nodes of the brain circuit that underlie reward processing. We aimed to investigate the relation between NAc-OFC structural and functional connectivity in preschool children, as well as associations with future reward sensitivity and executive function. We showed that NAc-OFC structural and functional connectivity were not significantly associated in preschool children, but both independently predicted sensitivity to reward in males in a left-lateralized manner. Moreover, significant NAc-OFC structure-function coupling was only found in individuals who performed poorly on executive function tasks in later childhood, but not in the middle- and high-performing groups. As structure-function coupling is proposed to measure functional specialization, this finding suggests premature functional specialization within the reward network, which may impede dynamic communication with other regions, affects executive function development. Our study also highlights the utility of multimodal imaging data integration when studying the effects of reward network functional flexibility in the preschool age, a critical period in brain and executive function development.

Keywords: Accumbofrontal tract; Executive functioning; Functional connectivity; Preschool children; Reward processing; Structure-function coupling.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain
Child
Child, Preschool
Executive Function*
Humans
Magnetic Resonance Imaging* / methods
Male
Nucleus Accumbens
Reward