Neurodevelopmental benefits of increased gestation have not been fully characterized in terms of network organization. Since brain function can be understood as an integrated network of neural information from distributed brain regions, investigation of the effects of gestational length on network properties is a critical goal of human developmental neuroscience. Using diffusion tensor imaging and fiber tractography, we investigated the effects of gestational length on the small-world attributes and rich club organization of 147 preadolescent children, whose gestational length ranged from 29 to 42 weeks. Higher network efficiency was positively associated with longer gestation. The longer gestation was correlated with increased local efficiency in the posterior medial cortex, including the precuneus, cuneus, and superior parietal regions. Rich club organization was also observed indicating the existence of highly interconnected structural hubs formed in preadolescent children. Connectivity among rich club members and from rich club regions was positively associated with the length of gestation, indicating the higher level of topological benefits of structural connectivity from longer gestation in the predominant regions of brain networks. The findings provide evidence that longer gestation is associated with improved topological organization of the preadolescent brain, characterized by the increased communication capacity of the brain network and enhanced directional strength of brain connectivity with central hub regions.

Socioeconomic disadvantage is associated with atypical development in specific brain regions, yet the relation between poverty and whole brain network organization (i.e., the connectome, a set of brain regions connected with neuronal pathways) has not been characterized. Developmental studies indicate that the connectome undergoes rapid change during childhood and is consequently likely to be highly sensitive to both salutary and detrimental influences. We investigated associations between the socioeconomic disparities measured by the income-to-needs ratio (INR) in childhood and structural brain network organization with 144 healthy children between 6 and 11 years of age (mean age = 8 years). INR of girls was positively and logarithmically associated with the extent to which brain networks were efficiently organized, suggesting that girls in more impoverished environments had less efficient brain network organization. Lower INR was associated with network inefficiency in multiple cortical regions including prefrontal cortex, cingulate, and insula, and in subcortical regions including the hippocampus and amygdala. These findings suggest that childhood poverty may result in wide-spread disruptions of the brain connectome among girls, particularly at the lowest INR levels, and are differentially expressed in females and males.

Elevated maternal cortisol concentrations have the potential to alter fetal development in a sex-specific manner. Female brains are known to show adaptive behavioral and anatomical flexibility in response to early-life exposure to cortisol, but it is not known how these sex-specific effects manifest at the whole-brain structural networks. A prospective longitudinal study of 49 mother child dyads was conducted with serial assessments of maternal cortisol levels from 15 to 37 gestational weeks. We modeled the structural network of typically developing children (aged 6-9 years) and examined its global connectome properties, rich-club organization, and modular architecture. Network segregation was susceptible only for girls to variations in exposure to maternal cortisol during pregnancy. Girls generated more connections than boys to maintain topologically capable and efficient neural circuits, and this increase in neural cost was associated with higher levels of internalizing problems. Maternal cortisol concentrations at 31 gestational weeks gestation were most strongly associated with altered neural connectivity in girls, suggesting a sensitive period for the maternal cortisol-offspring brain associations. Our data suggest that girls exhibit an adaptive response by increasing the neural network connectivity necessary for maintaining homeostasis and efficient brain function across the lifespan.