Functional Network Development During the First Year: Relative Sequence and Socioeconomic Correlations

Abstract

The first postnatal year is characterized by the most dramatic functional network development of the human lifespan. Yet, the relative sequence of the maturation of different networks and the impact of socioeconomic status (SES) on their development during this critical period remains poorly characterized. Leveraging a large, normally developing infant sample with multiple longitudinal resting-state functional magnetic resonance imaging scans during the first year (N = 65, scanned every 3 months), we aimed to delineate the relative maturation sequence of 9 key brain functional networks and examine their SES correlations. Our results revealed a maturation sequence from primary sensorimotor/auditory to visual to attention/default-mode, and finally to executive control networks. Network-specific critical growth periods were also identified. Finally, marginally significant positive SES-brain correlations were observed at 6 months of age for both the sensorimotor and default-mode networks, indicating interesting SES effects on functional brain maturation. To the best of our knowledge, this is the first study delineating detailed longitudinal growth trajectories of all major functional networks during the first year of life and their SES correlations. Insights from this study not only improve our understanding of early brain development, but may also inform the critical periods for SES expression during infancy.

The emergence of functional architecture during early brain development

“…Comparable functional network architecture has been revealed in the neonatal brain, albeit in an immature state (Doria et al, 2010a;Fransson et al, 2009;Gao et al, 2014aGao et al, , 2014bGao et al, , 2013Gao et al, , 2009Lin et al, 2008;Smyser et al, 2010) (Figure 3). Primary networks can be clearly depicted in newborn infants and display a mature configuration whilst higher-order networks are largely fragmented (Doria et al, 2010a;Fransson et al, 2009;Gao et al, 2014aGao et al, , 2014bSmyser et al, 2010).…”

“…A number of studies have focused on the emergence of resting-state networks in fetuses and newborn infants (Alcauter et al, 2015a;Arichi et al, 2010;Fransson et al, 2009, Gao et al, 2014a, 2014b, 2009Lin et al, 2008;Schöpf et al, 2012;Smyser et al, 2010;Thomason et al, 2015). In healthy adults, a distinct set of resting-state networks has been described encompassing brain regions involved in primary functions (i.e.…”

“…Primary networks can be clearly depicted in newborn infants and display a mature configuration whilst higher-order networks are largely fragmented (Doria et al, 2010a;Fransson et al, 2009;Gao et al, 2014aGao et al, , 2014bSmyser et al, 2010). These higher order networks are merely restricted to their core regions in the newborn brain, exhibiting relatively limited functional connections with spatially distant homologues.…”

“…The default mode network for instance -that has been associated with self-awareness, future planning, mind wandering and conceiving the perspectives of others ('theory of mind') in healthy adult brain functioning -, extends the posterior cingulate cortex, ventral and dorsal medial prefrontal cortex, inferior parietal lobule, lateral temporal cortex and the hippocampus regions in the adult human brain (Buckner et al, 2008;Buckner and Carroll, 2007;Raichle et al, 2001). In neonates, the default mode network is immature and incomplete, encompassing frontal and association cortices including the medial prefrontal cortex and posterior cingulate cortex (Doria et al, 2010a;Gao et al, 2014aGao et al, , 2009Smyser et al, 2010) (Figure 4). A fragmented precursor of the default mode network, comprising the medial prefrontal cortex and posterior cingulate cortex, was recently also identified in the developing fetal brain from 35 PCW (Thomason et al, 2015).…”

“…approximately 30 PCW in healthy fetuses (n=32) (Thomason et al, 2015). A recent study elegantly mapped the maturational trajectories of resting state networks in the first postnatal year at three-month intervals in 65 typically developing infants (Gao et al, 2014a). The sensorimotor network, visual processing network and auditory/language network demonstrated adult-like topology at birth and showed minimal topological changes during the first postnatal year.…”