Delayed brain network energy development in preterm youth impairs cognitive function: evidence from the longitudinal ABCD study

Preterm birth disrupts early brain development, increasing the risk of cognitive difficulties. However, its long-term effects on functional brain network energy, a metric of large-scale network stability and adaptability, remain poorly understood. Using resting-state fMRI data from the Adolescent Brain Cognitive Development (ABCD) study, we examined how prematurity influences brain network energy across late childhood and early adolescence. Our sample included 818 preterm-born youth and 2,149 matched full-term controls. Compared to full-term adolescents, preterm individuals exhibited altered multiscale functional connectivity and persistent reductions in functional network energy, specifically within the sensorimotor (SM) and higher-cognitive temporoparietal (HC-TP) networks, at both baseline and 2-year follow-up. These findings suggest diminished functional flexibility and network integration in preterm-born individuals. To further contextualize these results, we incorporated data from 1,633 participants in the Human Connectome Project (HCP) and HCP-Development studies, confirming that network energy increases with age in typically developing youth and is consistently reduced in preterm individuals. Notably, lower energy in the HC-TP network was specifically associated with deficits in crystallized cognition, but not with behavioral problems. Meta-analytic decoding further linked the HC-TP network to language and social cognition, providing a mechanistic explanation for its relationship with crystallized cognitive abilities. These findings highlight the persistence of neurodevelopmental alterations in preterm individuals, particularly affecting higher-order cognitive functions, and position network energy as a potential marker of altered neurodevelopment following preterm birth.