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

Abstract

One fundamental property of conscious experiences is that they are both differentiated and integrated. Adult functional brain networks exhibit an elegant "small-world" architecture. This optimal architecture enables efficient and cost-effective localized information processing and information integration between long-distance regions across the brain. It remains unclear whether the functional small-world architecture is developed in neonates at birth and how this development may be altered by premature birth. To address this gap, we investigated the development of small-world architecture in neonates. To understand the effect of early neonate age on small-world architecture, we also assessed neonates born prematurely or before term-equivalent age (TEA). We used the Developing Human Connectome Project (dHCP), a large neonatal functional magnetic resonance imaging (MRI) dataset with high temporal and spatial resolution. Resting-state functional MRI data for full- term neonates (N = 278, age 41.2 weeks {+/-} 12.2 days) and preterm neonates scanned at TEA (N = 72, 40.9 weeks {+/-} 14.6 days), or before TEA (N = 70, 34.7 weeks {+/-} 12.7 days), were obtained from the dHCP, and for a reference adult group (N = 176, 22-36 years), from the Human Connectome Project. Whole-brain functional network properties were evaluated with comprehensive spatial resolution using graph theoretical analyses. Although different from the adults, small-world architecture was developed in full-term born neonates at birth. Premature neonates before TEA showed dramatic underdevelopment of small-world architecture and regional communication in 9/11 brain networks, with disruption in 32% of nodes primarily distributed within the somatomotor, dorsal attention, cingulo-opercular, and frontoparietal control network. By TEA, premature neonates showed large-scale recuperation of regional communication, with 1.4% of nodes, distributed in the frontoparietal, salience, and visual networks remaining significantly underdeveloped. Our results suggest that, at full- term birth or by term-equivalent age, infants possess well-developed small-world architecture, which facilitates differentiated and integrated neural processes that give rise to conscious experiences. Conversely, they suggest that this brain infrastructure is significantly underdeveloped before infants reach term-equivalent age. These findings improve understanding of the ontogeny of functional small-world architecture and efficiency of neural communication across distinct brain networks in infants at birth.