Patterns of sociocognitive stratification and perinatal risk in the child brain

Abstract

The expanding behavioral repertoire of the developing brain during childhood and adolescence is shaped by complex brain-environment interactions and flavored by unique life experiences. The transition into young adulthood offers opportunities for adaptation and growth but also increased susceptibility to environmental perturbations, such as the characteristics of social relationships, family environment, quality of schools and activities, financial security, urbanization and pollution, drugs, cultural practices, and values, that all act in concert with our genetic architecture and biology. Our multivariate brain-behavior mapping in 7,577 children aged 9 to 11 y across 585 brain imaging phenotypes and 617 cognitive, behavioral, psychosocial, and socioeconomic measures revealed three population modes of brain covariation, which were robust as assessed by cross-validation and permutation testing, taking into account siblings and twins, identified using genetic data. The first mode revealed traces of perinatal complications, including preterm and twin birth, eclampsia and toxemia, shorter period of breastfeeding, and lower cognitive scores, with higher cortical thickness and lower cortical areas and volumes. The second mode reflected a pattern of sociocognitive stratification, linking lower cognitive ability and socioeconomic status to lower cortical thickness, area, and volumes. The third mode captured a pattern related to urbanicity, with particulate matter pollution (PM²⁵) inversely related to home value, walkability, and population density, associated with diffusion properties of white matter tracts. These results underscore the importance of a multidimensional and interdisciplinary understanding, integrating social, psychological, and biological sciences, to map the constituents of healthy development and to identify factors that may precede maladjustment and mental illness.

Keywords: childhood/adolescence; neurodevelopment; neuroscience; population imaging; psychology.

Fig. 1.

Rows represent CCA–ICA modes 1–3. Each mode represents an association between a linear combination of behavioral measures (Left) with a separate combination of imaging features (Right). x axes represent the numbered behavioral measures/imaging features. Behavioral measures legend shows starting location on x axis for each measure (in parentheses). y axes show the correlation between each included variable with the CCA–ICA subject weights. DWI measures abbreviations: fractional anisotropy (FA); mean diffusivity (MD); axial diffusivity (AD); radial diffusivity (RD); neurite density (ND).

Fig. 2.

Mode 1 links obstetric and perinatal complications to cortical area, volume, and thickness. Numbers on the left are correlations between each participant measure and MRI feature with mode 1 CCA–ICA subject weights. Hot and cold colors represent positive and negative correlations, respectively. Text on the right represents the participant measures (black) and imaging features (orange). The top 35 items are shown; for a full list of all measures and their respective correlations, see SI Appendix, Table S3.

Fig. 3.

Variables with the highest correlations with CCA–ICA mode 2 subject weights are shown, forming a dimension of sociocognitive stratification, which is associated with total intracranial volume and regional cortical volumes and thickness. Numbers on the left are correlations; hot and cold colors represent positive and negative correlations, respectively; and arrows indicate increasing positive/negative correlations. Text on the right represents the behavioral measures (black) and imaging features (orange). The top 35 items are shown; for a full list of all measures and associated correlations, see SI Appendix, Table S4.

Fig. 4.

The variables with the highest correlations with CCA–ICA mode 3 subject weights, linking air pollution, area deprivation, walkability, and population density to brain white matter indices. Numbers on the left are correlations; hot and cold colors represent positive and negative correlations, respectively; and arrows indicate increasing positive/negative correlations. Text on the right represents the behavioral measures (black) and imaging features (orange). The top 35 items are shown; for a full list of all measures and associated correlations, see SI Appendix, Table S5.