Early Development and Co-Evolution of Microstructural and Functional Brain Connectomes: A Multi-Modal MRI Study in Preterm and Full-Term Infants

Abstract

Functional networks characterized by coherent neural activity across distributed brain regions have been observed to emerge early in neurodevelopment. Synchronized maturation across regions that relate to functional connectivity (FC) could be partially reflected in the developmental changes in underlying microstructure. Nevertheless, covariation of regional microstructural properties, termed “microstructural connectivity” (MC), and its relationship to the emergence of functional specialization during the early neurodevelopmental period remain poorly understood. We investigated the evolution of MC and FC postnatally across a set of cortical and subcortical regions, focusing on 45 preterm infants scanned longitudinally, and compared to 45 matched full-term neonates as part of the developing Human Connectome Project (dHCP) using direct comparisons of grey-matter connectivity strengths as well as network-based analyses. Our findings revealed a global strengthening of both MC and FC with age, with connection-specific variability influenced by the connection maturational stage. Prematurity at term-equivalent age was associated with significant connectivity disruptions, particularly in FC. During the preterm period, direct comparisons of MC and FC strength showed a positive linear relationship, which seemed to weaken with development. On the other hand, overlaps between MC- and FC-derived networks (estimated with Mutual Information) increased with age, suggesting a potential convergence towards a shared underlying network structure that may support the co-evolution of microstructural and functional systems. Our study offers novel insights into the dynamic interplay between microstructural and functional brain development and highlights the potential of MC as a complementary descriptor for characterizing brain network development and alterations due to perinatal insults such as premature birth.