Exposure to early-life adversity (ELA) is a risk factor for behavioral and emotional problems in childhood as well as long-term health consequences. Neuroimaging studies provide a wealth of evidence for the association of perinatal adversity with neurodevelopmental outcomes. These findings include alterations in structure and connectivity in brain regions that are implicated in common mental disorders. The association of ELA with structural and functional development of the brain is now thought to represent adversity-related adaptations rather than stress-induced damage. ELA serves as a signal of the prevailing environmental conditions that influence the pace of brain development as an adaptive response to match the demands of unfavorable developmental conditions, at the potential cost to adult well-being. In a compromised environment, accelerating development to achieve independence may be prioritized over extended neuroplasticity that benefits the development of higher brain function. The ‘stress acceleration’ hypothesis proposes that exposure to ELA accelerates development, especially in fear/stress-related domains and emotion circuits. Rodents raised in stressful environments show accelerated development of fear learning and memory retention8. In humans, children exposed to maternal distress and deprivation show adult-like limbic brain features (for example, larger amygdala volumes, functional connectivity patterns typically observed in adults). Moreover, children exposed to early-life stress show accelerated biological age measured via either telomere length or DNA methylation-derived epigenetic age.
The current literature on ELA and neurodevelopmental trajectories is limited by a lack of longitudinal neuroimaging data during childhood that are required for a within-subject assessment of the developmental acceleration hypothesis. Most adversity-related studies with large neuroimaging datasets are retrospective cross-sectional studies where the neuroimaging data are collected in adults reporting on adverse childhood experiences (ACE). Therefore, developmental trajectories are not assessed directly but are inferred based on adult data. In addition, existing neurodevelopmental cohorts (for example, the Adolescent Brain Cognitive Development (ABCD), Human Connectome Project Development (HCP-D) and Pediatric Imaging, Neurocognition, and Genetics (PING) studies) cover large age ranges with few subjects below age 7 years, possibly due to the challenges of collecting high-quality neuroimaging data in preschool children. Thus, there is a critical gap in the literature on neurodevelopmental trajectories from early to late childhood, making it difficult (1) to assess the effect of high ELA exposure on brain development and (2) to identify sensitive time windows for intervention during childhood.
Recent studies on neurodevelopmental trajectories have focused on the correlation between structural and functional connectivity, that is, structure–function coupling (SC–FC), as a measure to capture changes in brain organization and maturation. Between the ages of 8 and 22 years, SC–FC changes in a functional-network-specific manner, with decreases in highly conserved motor regions and increases in transmodal cortices. In adults, SC–FC is highest in unimodal cortical regions and lowest in transmodal cortices. Whereas high SC–FC implies functional communication supported directly by local white matter pathways, low SC–FC suggests that functional communication relies on polysynaptic indirect pathways (circuit-level modulation) and a greater capacity for plasticity. The extent of SC–FC is linked to behavioral outcomes, such as executive function and higher cognitive abilities. Notably, significant SC–FC in the reward network is associated with poor performance on executive function tasks in later childhood. Therefore, SC–FC captures information on age and the current state of plasticity (highly conserved unimodal regions versus transmodal regions with increased potential for plasticity).