AUTHOR=Invernizzi Azzurra , Renzetti Stefano , Rechtman Elza , Ambrosi Claudia , Mascaro Lorella , Corbo Daniele , Gasparotti Roberto , Tang Cheuk Y. , Smith Donald R. , Lucchini Roberto G. , Wright Robert O. , Placidi Donatella , Horton Megan K. , Curtin Paul TITLE=Neuro-environmental interactions: a time sensitive matter JOURNAL=Frontiers in Computational Neuroscience VOLUME=17 YEAR=2024 URL=https://www.frontiersin.org/journals/computational-neuroscience/articles/10.3389/fncom.2023.1302010 DOI=10.3389/fncom.2023.1302010 ISSN=1662-5188 ABSTRACT=Introduction

The assessment of resting state (rs) neurophysiological dynamics relies on the control of sensory, perceptual, and behavioral environments to minimize variability and rule-out confounding sources of activation during testing conditions. Here, we investigated how temporally-distal environmental inputs, specifically metal exposures experienced up to several months prior to scanning, affect functional dynamics measured using rs functional magnetic resonance imaging (rs-fMRI).

Methods

We implemented an interpretable XGBoost-shapley additive explanation (SHAP) model that integrated information from multiple exposure biomarkers to predict rs dynamics in typically developing adolescents. In 124 participants (53% females, ages, 13–25 years) enrolled in the public health impact of metals exposure (PHIME) study, we measured concentrations of six metals (manganese, lead, chromium, copper, nickel, and zinc) in biological matrices (saliva, hair, fingernails, toenails, blood, and urine) and acquired rs-fMRI scans. Using graph theory metrics, we computed global efficiency (GE) in 111 brain areas (Harvard Oxford atlas). We used a predictive model based on ensemble gradient boosting to predict GE from metal biomarkers, adjusting for age and biological sex.

Results

Model performance was evaluated by comparing predicted versus measured GE. SHAP scores were used to evaluate feature importance. Measured versus predicted rs dynamics from our model utilizing chemical exposures as inputs were significantly correlated (p < 0.001, r = 0.36). Lead, chromium, and copper contributed most to the prediction of GE metrics.

Discussion

Our results indicate that a significant component of rs dynamics, comprising approximately 13% of observed variability in GE, is driven by recent metal exposures. These findings emphasize the need to estimate and control for the influence of past and current chemical exposures in the assessment and analysis of rs functional connectivity.