Widespread Positive Direct and Indirect Effects of Regular Physical Activity on the Developing Functional Connectome in Early Adolescence

Abstract

Adolescence is a period of profound but incompletely understood changes in the brain’s neural circuitry (the connectome), which is vulnerable to risk factors such as unhealthy weight, but may be protected by positive factors such as regular physical activity. In 5955 children (median age = 120 months; 50.86% females) from the Adolescent Brain Cognitive Development (ABCD) cohort, we investigated direct and indirect (through impact on body mass index [BMI]) effects of physical activity on resting-state networks, the backbone of the functional connectome that ubiquitously affects cognitive function. We estimated significant positive effects of regular physical activity on network connectivity, efficiency, robustness and stability (P ≤ 0.01), and on local topologies of attention, somatomotor, frontoparietal, limbic, and default-mode networks (P < 0.05), which support extensive processes, from memory and executive control to emotional processing. In contrast, we estimated widespread negative BMI effects in the same network properties and brain regions (P < 0.05). Additional mediation analyses suggested that physical activity could also modulate network topologies leading to better control of food intake, appetite and satiety, and ultimately lower BMI. Thus, regular physical activity may have extensive positive effects on the development of the functional connectome, and may be critical for improving the detrimental effects of unhealthy weight on cognitive health.

Shorter Duration and Lower Quality Sleep Have Widespread Detrimental Effects on Developing Functional Brain Networks in Early Adolescence

“…The Next-Generation-Neural-Data-Analysis ( NGNDA 2021 ) platform, recently developed for analyses of high-dimensional brain data, was used to further processed the fMRI data, reduce its dimensionality, and denoise it prior to the estimation of the connectome and its properties. FMRI processing using the NGNDA, which uses a combination of widely available and custom-developed computational tools and algorithms, is described in detail in Brooks et al. 2021 and Supplementary Materials .…”

“…Each participant’s fMRI data were first processed for initial frame removal, coregistration to MRI, slice-time correction, and normalization to MNI152 space, followed by time series denoising and artifact suppression. Then, the spatial dimension of the original fMRI time series matrix was reduced through parcellation to 1088 cortical and subcortical regions and the cerebellum, using a combination of three atlases as described in Brooks et al. (2021) .…”

“…Resulting connectivity matrices from the two methods had overall statistically identical spatial patterns. These matrices were subsequently thresholded (as described in Brooks et al. [2021] and Supplemental Materials ) to obtain weighted and binary adjacency matrices, which were used to estimate network properties.…”

“…All models also included an adjustment for percent of motion-censored frames in the analyzed fMRI run. Although, based on the inclusion criteria for fMRI quality, the selected run had a small number of censored frames (median = 1.90%), in prior work this parameter was found to be significant in statistical models, although its inclusion did not alter the overall results ( Brooks et al. 2021 ).…”

“…In a sample of 5566 typically developing children from the ABCD cohort, this study investigated the impact of sleep duration and quality, assessed via the parent-reported Sleep Disturbance Scale for Children (SDSC), on the resting-state functional connectome in early adolescence, and thus brain networks that play a ubiquitous role in cognitive function across domains. These include the DMN, frontoparietal control, and limbic networks, which continue to maturate throughout adolescence and are thus vulnerable to the effects of risk factors (e.g., unhealthy body mass index [BMI]; Brooks et al. 2021 ) and stressors such as unhealthy sleep.…”