Adolescent brain maturation associated with environmental factors: a multivariate analysis

Front Neuroimaging. 2024 Nov 19:3:1390409. doi: 10.3389/fnimg.2024.1390409. eCollection 2024.

Abstract

Human adolescence marks a crucial phase of extensive brain development, highly susceptible to environmental influences. Employing brain age estimation to assess individual brain aging, we categorized individuals (N = 7,435, aged 9-10 years old) from the Adolescent Brain and Cognitive Development (ABCD) cohort into groups exhibiting either accelerated or delayed brain maturation, where the accelerated group also displayed increased cognitive performance compared to their delayed counterparts. A 4-way multi-set canonical correlation analysis integrating three modalities of brain metrics (gray matter density, brain morphological measures, and functional network connectivity) with nine environmental factors unveiled a significant 4-way canonical correlation between linked patterns of neural features, air pollution, area crime, and population density. Correlations among the three brain modalities were notably strong (ranging from 0.65 to 0.77), linking reduced gray matter density in the middle temporal gyrus and precuneus to decreased volumes in the left medial orbitofrontal cortex paired with increased cortical thickness in the right supramarginal and bilateral occipital regions, as well as increased functional connectivity in occipital sub-regions. These specific brain characteristics were significantly more pronounced in the accelerated brain aging group compared to the delayed group. Additionally, these brain regions exhibited significant associations with air pollution, area crime, and population density, where lower air pollution and higher area crime and population density were correlated to brain variations more prominently in the accelerated brain aging group.

Keywords: adolescence; brain development; environmental factors; functional MRI; multi-set canonical correlation analysis; multivariate; structural MRI.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Institutes of Health (NIH; R01DA049238) and the National Science Foundation of the USA (NSF; 2112455) to VC and JL.