Structural Brain Co-Maturation in the Neonatal Period

Abstract

Background The neonatal period is characterized by neurodevelopmental processes coinciding with rapid physiological transitions, however, spatial patterns of brain expansion in early life remain incompletely characterized. Here, we leverage grey matter structural covariance in term- and preterm-born neonates to study the interregional synchrony of neonatal brain maturation along principal brain organizational axes. Methods We used structural MRI data from the developing Human Connectome Project (n=525; 435 term-born) scanned at 37-44 weeks postmenstrual age (PMA)), stratifying the sample by term status and PMA. Based on cortical thickness (CT) and surface area (SA) metrics, we computed age group-(CVg) and individual-level (CVi) structural covariance matrices. Applying surface-based linear models, we identified changes in interregional covariance with postmenstrual age (PMA) and gestational age at birth (GAB), and contextualized alterations to neonatal functional networks. Using gradient decomposition, we identified major trajectories of cortical expansion on individual and group levels, and determined their correlation to archetypal geometric, evolutionary, and functional axes. Results We found age-related changes reflecting cortical expansion and an increased structural differentiation with age. Gradient decomposition of group-level covariance revealed that primary components followed both an posterior-anterior distribution, anchored in the visual cortex, and a sensorimotor-association gradient. Individual-level covariance gradients adhered most to geometric axes, and diverged from a sensorimotor-association pattern with increasing PMA. Term-born neonates exhibited a higher spatial correlation to functional and geometric axes than preterm-born neonates, overall pointing to different expansion patterns in neonates of the same PMA. Conclusion We found trajectories of structural maturation in the neonatal period that appear coordinated along geometric and functional axes. On an age group level, term-born neonates appear to follow archetypal axes more than preterm-borns at term-equivalent age, underlining differential expansion patterns in preterm-born neonates.