Emergence of long- and short-range functional connectivity parallels the development of neonatal brain gradients

Abstract

The emergence of macroscale brain organisation during the perinatal period represents a critical but poorly understood process. Using resting-state fMRI in 325 term-born neonates within the first month of postnatal life, we characterised the early emergence of macroscale brain organisation with functional gradients. Neonatal functional gradients showed a distinct pattern compared with the canonical adult gradients: the principal gradient in neonates, separating the primary sensorimotor and visual networks, broadly corresponded to the secondary gradient in adults (sensorimotor-visual axis), whereas the secondary gradient in neonates, spanning from primary visual to association networks, aligned with the principal gradient in adults (sensorimotor-association axis). We found that the perinatal emergence of distance-dependent functional connectivity paralleled the development of neonatal functional gradients, potentially underlying the protracted development of the sensorimotor-association hierarchy in neonates. Regions with a higher proportion of short-range functional connectivity were more strongly associated with the sensorimotor-visual gradient in neonates, while regions with a greater proportion of middle- to long-range functional connectivity were more strongly associated with the sensorimotor-association hierarchy. Together, these findings highlight the critical role of short- and long-range functional connectivity, which showed a close correspondence with neonatal macroscale functional hierarchy. Disruptions to this process during the perinatal period may alter macroscale brain organisation and contribute to the early origins of neurodevelopmental conditions.