First-year development of modules and hubs in infant brain functional networks

Abstract

The human brain develops rapidly in the first postnatal year, in which rewired functional brain networks could shape later behavioral and cognitive performance. Resting-state functional magnetic resonances imaging (rs-fMRI) and complex network analysis have been widely used for characterizing the developmental brain functional connectome. Yet, such studies focusing on the first year of postnatal life are still very limited. Leveraging normally developing longitudinal infant rs-fMRI scans from neonate to one year of age, we investigated how brain functional networks develop at a fine temporal scale (every 3 months). Considering challenges in the infant fMRIbased network analysis, we developed a novel algorithm to construct the robust, temporally consistent and modular structure augmented group-level network based on which functional modules were detected at each age. Our study reveals that the brain functional network is gradually subdivided into an increasing number of functional modules accompanied by the strengthened intra-and inter-modular connectivities. Based on the developing modules, we found connector hubs (the high-centrality regions connecting different modules) emerging and increasing, while provincial hubs (the high-centrality regions connecting regions in the same module) diminishing. Further region-wise longitudinal analysis validates that different hubs have distinct developmental trajectories of the intra-and inter-modular connections suggesting different types of role transitions in network, such as non-hubs to hubs or provincial hubs to connector hubs

Hub distribution of the brain functional networks of newborns prenatally exposed to maternal depression and SSRI antidepressants

“…Also, symptom severity (reported using HAM-D) was positively correlated with modularity (Ye et al, 2015). As modularity has been shown to gradually increase in the first year of life (Wen et al, 2018), it might be that alterations in global modularity do not exist in the neonatal brain but might develop over time. Also, mothers in our cohort showed only mild-depressive symptoms (see Table 1).…”

“…A multivariate GLM analysis corrected for sex, age at the MRI, and PES revealed group differences between the depressed-only and control groups for the amygdala, and between SSRI and depressed-only for the right frontal orbital and left Heschl gyrus corrected for multiple comparisons, Bonferroni (also see Table S4a,b). As modularity has been shown to gradually increase in the first year of life (Wen et al, 2018), it might be that alterations in global modularity do not exist in the neonatal brain but might develop over time. Dark green circles represent provincial hubs, and red circles represent connector hubs.…”

“…GTA applied to resting-state functional magnetic resonance imaging (rs-fMRI) has been used to characterize the functional topography of the human brain from the fetal period through to adulthood (Bathelt, O'Reilly, Clayden, Cross, & De Haan, 2013;De Asis-Cruz, Bouyssi-Kobar, Evangelou, Vezina, & Limperopoulos, 2015;Gao et al, 2015;Thomason et al, 2017;van den Heuvel et al, 2018). Wen et al (2018) have shown that during the first year of life the modular organization of the brain functional network is progressively increasing and subdividing into an increasing number of functional modules together with stabilizing intramodular connection and clustering and intermodular connections. Patterns of gradual increase in intermodular connectivity have also been demonstrated in fetuses with increasing gestational age (Thomason et al, 2014).…”

Development of Dynamic Functional Architecture during Early Infancy

“…Different functional sub-networks are developed with diverse developmental trajectories, with primary systems mature earlier than high-order function-related systems Gao et al, 2015). From the local level, our recent findings suggest that more association regions gradually emerge as connector hubs facilitating information exchange and integration among functional sub-networks, while many primary regions become less centralized (Gao et al, 2011;Wen et al, 2019). Although providing valuable insights, these studies all investigate FC from a "static" point of view, ignoring its essential "temporal dynamics".…”

“…Based on this method, existing studies have revealed the brain functional network development at multiple levels, including global (i.e., whole brain) (Gao et al, 2011;Wen et al, 2019), mesoscale (i.e., functional sub-networks) (Gao and Lin, 2012b;Gao et al, 2014;Gao et al, 2015;) and local levels (i.e., brain regions) (Wen et al, 2019). Generally, the brain network is globally reconfigured to be more efficiently balanced between local and global information communications from neonates to two years of age (Gao et al, 2011;Wen et al, 2019). Different functional sub-networks are developed with diverse developmental trajectories, with primary systems mature earlier than high-order function-related systems Gao et al, 2015).…”