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.

Keywords: first year; functional connectivity; functional networks; resting state.

© The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.

Figures

Figure 1.

The distribution of gestational ages for all included pediatric subjects whose image quality passed the quality control procedures. Each dot represents one successful rsfMRI scan from one subject and dots along each line represent all available longitudinal scans of a subject.

Figure 2.

Development of the 9 brain cortical functional networks. Thresholded maps (P < 0.05 after FDR correction) evaluated at each of the 5 time points were shown from the first to the fifth rows and the corresponding adult maps were shown at the bottom row (green dots show the locations of seeds). Color bar indicates correlation strength. The images are in radiological convention (the right side of the brain is on the left side of image).

Figure 3.

Detailed development trends of the 9 functional networks during the first year of life. (A) The comparisons between 6 months and neonates, 12 and 6 months, 12 months and neonates are shown from the first to the third rows, respectively. The adult functional network structures are presented in the bottom row for comparisons. (B) Comparisons of the amount of significant changes between 0 and 6 months (labeled as 1) and 6 and 12 months (labeled as 2) are shown. Top row: Percentages of voxels showing a significant increase in functional connectivity for all networks (normalized against the number of voxels showing a significant increase during the whole year). Bottom row: Percentages of voxels showing a significant decrease in functional connectivity for all networks (normalized against the number of voxels showing a significant decrease during the whole year). (C) More detailed development trends of 9 functional networks during the first year of life. The comparisons across every 3-month periods are shown from the first to the fourth row, respectively. The images are in radiological convention (the right side of the brain is on the left side of image).

Figure 4.

Longitudinal growth trajectory of the network matching scores (NMS) for each functional network. (A) NMS growth curves. Bold red lines indicate the group trend while the underlying gray lines are spaghetti plots representing curves from individual subjects. Significant age-dependent group-level growths (log-linear, P < 0.05, FDR corrected) are shown in solid lines, whereas non-significant ones are in dashed lines. (B) Bar plots of the growth rates [per log(day)] from different functional networks. The groupings of different groups are based on Table 2.

Figure 5.

SES correlations with network functional connectivity measures. (A) The relationship between income and network matching score (NMS) of the SM network (first panel); income and within-network functional connectivity (WNC) of the SM network (second panel); maternal education and network matching score of the SM network (third panel), maternal education and within-network connectivity of the SM network (fourth panel) at 6 months of age. (B) The relationship between maternal education and DMN network outside-network connectivity (ONC) at 6 months of age. Note the residual values of both SES parameters and functional connectivity measures after regressing out the covariates of no-interest (see Materials and Methods section, indicated by _R) are plotted to visualize their partial correlations. Black dots represent individual subjects and red lines are the fitted regression lines to show the linear trend. The histograms of correlations based on 1000 times bootstrapping were visualized below each correlation scatter plot with red vertical lines, indicating the confidence intervals of each correlation estimate.