Fetal network controllability co-develops with synaptic density and synchronizes with maternal network controllability during pregnancy

White matter undergoes rapid changes during the fetal period that are foundational for later cognition. However, how these changes contribute to the brain's capacity for dynamic state transitions-its controllability-remains largely unknown. Here, we apply network control theory (NCT) to investigate the developmental trajectory of controllability from the second trimester through the first postnatal month. We analyzed structural connectivity data from 217 fetuses, 448 term infants, and 194 preterm infants as part of the developing Human Connectome Project. We identified a robust, nonlinear U-shaped developmental curve of whole-brain controllability across the perinatal period, with a minimum at approximately 35 gestational weeks. Preterm birth disrupted these trajectories, leading to greater controllability and earlier minimums compared to age-matched fetuses. We used positron emission tomography in seven pregnant rhesus macaques to quantify changes in fetal synaptic density. Increased synaptic density in non-human primates (NHPs) co-occurred with periods of reduced controllability in humans, suggesting that changes in controllability may be driven by synaptogenesis. Finally, using longitudinal scans of a pregnant woman, we mapped the trajectory of changes in maternal controllability during pregnancy. This trajectory exhibited a U-shaped pattern that inversely correlated with the fetal trajectory and reached a maximum around 36 weeks. Together, fetal controllability follows a nonlinear trajectory that co-develops with synaptic density in NHPs and synchronizes with maternal changes in controllability during pregnancy.