skip to main content

Title: 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 more » health. « less
Authors:
; ;
Award ID(s):
1940096 1649865 1451480 1658414
Publication Date:
NSF-PAR ID:
10228266
Journal Name:
Cerebral Cortex
ISSN:
1047-3211
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Sleep is critical for cognitive health, especially during complex developmental periods such as adolescence. However, its effects on maturating brain networks that support cognitive function are only partially understood. We investigated the impact of shorter duration and reduced quality sleep, common stressors during development, on functional network properties in early adolescence—a period of significant neural maturation, using resting-state functional magnetic resonance imaging from 5566 children (median age = 120.0 months; 52.1% females) in the Adolescent Brain Cognitive Development cohort. Decreased sleep duration, increased sleep latency, frequent waking up at night, and sleep-disordered breathing symptoms were associated with lower topological efficiency, flexibility, and robustness of visual, sensorimotor, attention, fronto-parietal control, default-mode and/or limbic networks, and with aberrant changes in the thalamus, basal ganglia, hippocampus, and cerebellum (P < 0.05). These widespread effects, many of which were body mass index-independent, suggest that unhealthy sleep in early adolescence may impair neural information processing and integration across incompletely developed networks, potentially leading to deficits in their cognitive correlates, including attention, reward, emotion processing and regulation, memory, and executive control. Shorter sleep duration, frequent snoring, difficulty waking up, and daytime sleepiness had additional detrimental network effects in nonwhite participants, indicating racial disparities in the influence of sleep metrics.
  2. Abstract

    Convergent research identifies a general factor (“P factor”) that confers transdiagnostic risk for psychopathology. Large-scale networks are key organizational units of the human brain. However, studies of altered network connectivity patterns associated with the P factor are limited, especially in early adolescence when most mental disorders are first emerging. We studied 11,875 9- and 10-year olds from the Adolescent Brain and Cognitive Development (ABCD) study, of whom 6593 had high-quality resting-state scans. Network contingency analysis was used to identify altered interconnections associated with the P factor among 16 large-scale networks. These connectivity changes were then further characterized with quadrant analysis that quantified the directionality of P factor effects in relation to neurotypical patterns of positive versus negative connectivity across connections. The results showed that the P factor was associated with altered connectivity across 28 network cells (i.e., sets of connections linking pairs of networks);pPERMUTATIONvalues < 0.05 FDR-corrected for multiple comparisons. Higher P factor scores were associated with hypoconnectivity within default network and hyperconnectivity between default network and multiple control networks. Among connections within these 28 significant cells, the P factor was predominantly associated with “attenuating” effects (67%;pPERMUTATION < 0.0002), i.e., reduced connectivity at neurotypically positive connections and increased connectivity at neurotypically negative connections.more »These results demonstrate that the general factor of psychopathology produces attenuating changes across multiple networks including default network, involved in spontaneous responses, and control networks involved in cognitive control. Moreover, they clarify mechanisms of transdiagnostic risk for psychopathology and invite further research into developmental causes of distributed attenuated connectivity.

    « less
  3. Abstract

    Context.Large multi-site neuroimaging datasets have significantly advanced our quest to understand brain-behavior relationships and to develop biomarkers of psychiatric and neurodegenerative disorders. Yet, such data collections come at a cost, as the inevitable differences across samples may lead to biased or erroneous conclusions.Objective.We aim to validate the estimation of individual brain network dynamics fingerprints and appraise sources of variability in large resting-state functional magnetic resonance imaging (rs-fMRI) datasets by providing a novel point of view based on data-driven dynamical models.Approach.Previous work has investigated this critical issue in terms of effects on static measures, such as functional connectivity and brain parcellations. Here, we utilize dynamical models (hidden Markov models—HMM) to examine how diverse scanning factors in multi-site fMRI recordings affect our ability to infer the brain’s spatiotemporal wandering between large-scale networks of activity. Specifically, we leverage a stable HMM trained on the Human Connectome Project (homogeneous) dataset, which we then apply to an heterogeneous dataset of traveling subjects scanned under a multitude of conditions.Main Results.Building upon this premise, we first replicate previous work on the emergence of non-random sequences of brain states. We next highlight how these time-varying brain activity patterns are robust subject-specific fingerprints. Finally, we suggest these fingerprintsmore »may be used to assess which scanning factors induce high variability in the data.Significance.These results demonstrate that we can (i) use large scale dataset to train models that can be then used to interrogate subject-specific data, (ii) recover the unique trajectories of brain activity changes in each individual, but also (iii) urge caution as our ability to infer such patterns is affected by how, where and when we do so.

    « less
  4. Abstract Neural activity coordinated across different scales from neuronal circuits to large-scale brain networks gives rise to complex cognitive functions. Bridging the gap between micro- and macro-scale processes, we present a novel framework based on the maximum entropy model to infer a hybrid resting state structural connectome, representing functional interactions constrained by structural connectivity. We demonstrate that the structurally informed network outperforms the unconstrained model in simulating brain dynamics; wherein by constraining the inference model with the network structure we may improve the estimation of pairwise BOLD signal interactions. Further, we simulate brain network dynamics using Monte Carlo simulations with the new hybrid connectome to probe connectome-level differences in excitation-inhibition balance between apolipoprotein E (APOE)-ε4 carriers and noncarriers. Our results reveal sex differences among APOE-ε4 carriers in functional dynamics at criticality; specifically, female carriers appear to exhibit a lower tolerance to network disruptions resulting from increased excitatory interactions. In sum, the new multimodal network explored here enables analysis of brain dynamics through the integration of structure and function, providing insight into the complex interactions underlying neural activity such as the balance of excitation and inhibition.
  5. Abstract

    Listening to pleasurable music is known to engage the brain’s reward system. This has motivated many cognitive-behavioral interventions for healthy aging, but little is known about the effects of music-based intervention (MBI) on activity and connectivity of the brain’s auditory and reward systems. Here we show preliminary evidence that brain network connectivity can change after receptive MBI in cognitively unimpaired older adults. Using a combination of whole-brain regression, seed-based connectivity analysis, and representational similarity analysis (RSA), we examined fMRI responses during music listening in older adults before and after an 8-week personalized MBI. Participants rated self-selected and researcher-selected musical excerpts on liking and familiarity. Parametric effects of liking, familiarity, and selection showed simultaneous activation in auditory, reward, and default mode network (DMN) areas. Functional connectivity within and between auditory and reward networks was modulated by participant liking and familiarity ratings. RSA showed significant representations of selection and novelty at both time-points, and an increase in striatal representation of musical stimuli following intervention. An exploratory seed-based connectivity analysis comparing pre- and post-intervention showed significant increase in functional connectivity between auditory regions and medial prefrontal cortex (mPFC). Taken together, results show how regular music listening can provide an auditory channel towardsmore »the mPFC, thus offering a potential neural mechanism for MBI supporting healthy aging.

    « less