Effects of ambient fine particulates, nitrogen dioxide, and ozone on maturation of functional brain networks across early adolescence

Devyn L. Cotter; Claire E. Campbell; Kirthana Sukumaran; Rob McConnell; Kiros Berhane; Joel Schwartz; Daniel A. Hackman; Hedyeh Ahmadi; Jiu-Chiuan Chen; Megan M. Herting

Environment International (Jul 2023)

Effects of ambient fine particulates, nitrogen dioxide, and ozone on maturation of functional brain networks across early adolescence

Devyn L. Cotter,
Claire E. Campbell,
Kirthana Sukumaran,
Rob McConnell,
Kiros Berhane,
Joel Schwartz,
Daniel A. Hackman,
Hedyeh Ahmadi,
Jiu-Chiuan Chen,
Megan M. Herting

Affiliations

Devyn L. Cotter: Neuroscience Graduate Program, University of Southern California, Los Angeles, CA, USA; Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Claire E. Campbell: Neuroscience Graduate Program, University of Southern California, Los Angeles, CA, USA; Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Kirthana Sukumaran: Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Rob McConnell: Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Kiros Berhane: Department of Biostatistics, Columbia University Mailman School of Public Health, New York, NY, USA
Joel Schwartz: Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Daniel A. Hackman: USC Suzanne Dworak-Peck School of Social Work, University of Southern California, Los Angeles, CA, USA
Hedyeh Ahmadi: Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Jiu-Chiuan Chen: Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA; Department of Neurology, Keck School of Medicine of University of Southern California, Los Angeles, CA, USA
Megan M. Herting: Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA; Children’s Hospital Los Angeles, Los Angeles, CA, USA; Corresponding author at: Department of Population and Public Health Sciences, University of Southern California, 1845 N. Soto Street, Room 225N, Los Angeles, CA 90089, USA.

Journal volume & issue: Vol. 177
p. 108001

Abstract

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Background: Air pollution is linked to neurodevelopmental delays, but its association with longitudinal changes in brain network development has yet to be investigated. We aimed to characterize the effect of PM2.5, O3, and NO2 exposure at ages 9–10 years on changes in functional connectivity (FC) over a 2-year follow-up period, with a focus on the salience (SN), frontoparietal (FPN), and default-mode (DMN) brain networks as well as the amygdala and hippocampus given their importance in emotional and cognitive functioning. Methods: A sample of children (N = 9,497; with 1–2 scans each for a total of 13,824 scans; 45.6% with two brain scans) from the Adolescent Brain Cognitive Development (ABCD) Study® were included. Annual averages of pollutant concentrations were assigned to the child’s primary residential address using an ensemble-based exposure modeling approach. Resting-state functional MRI was collected on 3T MRI scanners. First, developmental linear mixed-effect models were performed to characterize typical FC development within our sample. Next, single- and multi-pollutant linear mixed-effect models were constructed to examine the association between exposure and intra-network, inter-network, and subcortical-to-network FC change over time, adjusting for sex, race/ethnicity, income, parental education, handedness, scanner type, and motion. Results: Developmental profiles of FC over the 2-year follow-up included intra-network integration within the DMN and FPN as well as inter-network integration between the SN-FPN; along with intra-network segregation in the SN as well as subcortical-to-network segregation more broadly. Higher PM2.5 exposure resulted in greater inter-network and subcortical-to-network FC over time. In contrast, higher O3 concentrations resulted in greater intra-network, but less subcortical-to-network FC over time. Lastly, higher NO2 exposure led to less inter-network and subcortical-to-network FC over the 2-year follow-up period. Conclusion: Taken together, PM2.5, O3, and NO2 exposure in childhood relate to distinct changes in patterns of network maturation over time. This is the first study to show outdoor ambient air pollution during childhood is linked to longitudinal changes in brain network connectivity development.

Published in Environment International

ISSN: 0160-4120 (Print)
Publisher: Elsevier
Country of publisher: United Kingdom
LCC subjects: Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/environment-international

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