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

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.

Fig. 1

Study design. (A) Structural (i) and functional connectivity (ii) ROIs, specifically the nucleus accumbens (green), orbito-frontal cortex (blue), and accumbofrontal tract (yellow). Structure-function coupling (iii) was derived from correlating structural and functional connectivity. (B) Study data was collected at different time points (age 4.5 years to 8.5 years). Three connectivity measures (blue) were collected – structural connectivity, functional connectivity, and structure-function coupling. Subject numbers (N) represent the number of subjects who have complete data for both neuroimaging measures and the specified task/questionnaire. BRIEF, Behavior Rating Inventory for Executive Function; SPSRQ, Sensitivity to Punishment and Sensitivity to Reward Questionnaire; WASI-II, Wechsler Abbreviated Scale of Intelligence – Second Edition; SC-FC Coupling, Spearman correlation between structural connectivity and functional connectivity.

Fig. 2

Residual plots showing NAc-OFC structural connectivity ranks (Y-axis) and functional connectivity ranks (X-axis), where subjects are divided into groups based on reward sensitivity scores and ranked within each group. Each plot represents connectivity in a hemisphere – left and right. Residuals are calculated after taking the effects of sex, fMRI motion parameters (outliers removed, mean motion, max motion) and DTI parameters (motion, volume of NAc and OFC) into account. The spearman correlation (ρ) and significance (p) are displayed.

Fig. 3

Residual plots showing left NAc-OFC structural connectivity ranks (Y-axis) and functional connectivity ranks (X-axis), where subjects are divided into groups based on task/questionnaire performance and ranked within each group. Residuals are calculated after taking the effects of sex, fMRI motion parameters (outliers removed, mean motion, max motion) and DTI parameters (motion, volume of NAc and OFC) into account. The spearman correlation (ρ) and significance (p) are displayed. Note: BRIEF-GEC, Behavior Rating Inventory for Executive Function Global Executive Composite; WASI-II, Wechsler Abbreviated Scale of Intelligence – Second Edition Perceptual Reasoning; WCST, Wisconsin Card Sorting Test.