Neuronal Coupling Modes Show Differential Development in the Early Cortical Activity Networks of Human Newborns

The third trimester is a critical period for the development of functional networks that support the lifelong neurocognitive performance, yet the emergence of neuronal coupling in these networks is poorly understood. Here, we used longitudinal high-density electroencephalographic recordings from preterm infants during the period from 33 to 45 weeks of conceptional age (CA) to characterize early spatiotemporal patterns in the development of local cortical function and the intrinsic coupling modes [ICMs; phase- phase (PPCs), amplitude-amplitude (AACs), and phase-amplitude correlations (PACs)]. Absolute local power showed a robust increase with CA across the full frequency spectrum, while local PACs showed sleep state-specific, biphasic development that peaked a few weeks before normal birth. AACs and distant PACs decreased globally at nearly all frequencies. In contrast, the PPCs showed frequency- and region-selective development, with an increase of coupling strength with CA between frontal, central, and occipital regions at low-delta and alpha frequencies together with a wider-spread decrease at other frequencies. Our findings together present the spectrally and spatially differential development of the distinct ICMs during the neonatal period and provide their developmental templates for future basic and clinical research.