Development of segregation and integration of functional connectomes during the first 1,000 days

Highlights•Brain hubs shift from primary to association regions during the first 1,000 days of life•Functional segregation and integration develop along an anterior-posterior axis•Neonatal connectomes predict cognitive and language outcomes at 1.5 years of age•Network growth is regulated by genes involved in neurodevelopment and metabolismSummaryThe first 1,000 days of human life lay the foundation for brain development and later cognitive growth. However, the developmental rules of the functional connectome during this critical period remain unclear. Using high-resolution, longitudinal, task-free functional magnetic resonance imaging data from 930 scans of 665 infants aged 28 postmenstrual weeks to 3 years, we report the early maturational process of connectome segregation and integration. We show the dominant development of local connections alongside a few global connections, the shift of brain hubs from primary regions to high-order association cortices, the developmental divergence of network segregation and integration along the anterior-posterior axis, the prediction of neurocognitive outcomes, and their associations with gene expression signatures of microstructural development and neuronal metabolic pathways. These findings advance our understanding of the principles of connectome remodeling during early life and its neurobiological underpinnings and have implications for studying typical and atypical development.