Typical and disrupted small-world architecture and regional communication in full-term and preterm infants

Understanding the emergence of complex cognition in the neonate is one of the great frontiers of cognitive neuroscience. In the adult brain, small-world organization enables efficient information segregation and integration and dynamic adaptability to cognitive demands. It remains unknown, however, when functional small-world architecture emerges in development, whether it is present by birth and how prematurity affects it. We leveraged the world's largest fMRI neonatal dataset-Developing Human Connectome Project-to include full-term neonates (n = 278), and preterm neonates scanned at term-equivalent age (TEA; n = 72), or before TEA (n = 70), and the Human Connectome Project for a reference adult group (n = 176). Although different from adults', the small-world architecture was developed in full-term neonates at birth. The key novel finding was that premature neonates before TEA showed dramatic underdevelopment of small-world organization and regional communication in 9/11 networks, with disruption in 32% of brain nodes. The somatomotor and dorsal attention networks carry the largest spatial effect, and visual network the smallest. Significant prematurity-related disruption of small-world architecture and reduced efficiency of regional communication in networks related to high-order cognition, including language, persisted at TEA. Critically, at full-term birth or by TEA, infants exhibited functional small-world architecture, which facilitates differentiated and integrated neural processes that support complex cognition. Conversely, this brain infrastructure is significantly underdeveloped before infants reach TEA. These findings improve understanding of the ontogeny of functional small-world architecture and efficiency of neural communication, and of their disruption by premature birth.