Physical activity, aerobic fitness and brain white matter: their role for executive functions in adolescence

Abstract

Highlights:· Aerobic fitness level, but not physical activity, is associated with white matter properties in several white matter tracts in the brain.· The relationship between aerobic fitness and working memory was moderated by fractional anisotropy of the body of corpus callosum and in the right superior corona radiata.· The relationship between physical activity and working memory was moderated by fractional anisotropy of the body and genu of corpus callosum. Declarations of interest: noneAbbreviations: CANTAB = Cambridge Neuropsychological Automated Test Battery, DWI = diffusionweighted imaging, FA = fractional anisotropy, MD = mean diffusivity, MRI = magnetic resonance imaging, MVPA = moderate-to-vigorous intensity physical activity, RD = radial diffusivity, RVP = rapid visual information processing, SWM = spatial working memory, TBSS = Tract-Based Spatial Statistics, TFCE = threshold-free cluster enhancement Abstract Physical activity and exercise beneficially link to brain properties and cognitive functions in older adults, but it is unclear how these results generalise to other age groups. During adolescence, the brain undergoes significant changes, which are especially pronounced in white matter. Existing studies provide contradictory evidence regarding the influence of physical activity or aerobic-exercise on executive functions in youth. Little is also known about the link between both aerobic fitness and physical activity with white matter during puberty. For this reason, we investigated the connection between both aerobic fitness (20-m shuttle run) and physical activity (moderate-to-vigorous intensity physical activity) with white matter in 59 adolescents (12.7-16.2 years). We further determined whether white matter interacts with the connection of fitness or physical activity with three core executive functions (sustained attention, spatial working memory and response inhibition). Our results showed that only the level of aerobic fitness, but not of physical activity was related to white matter properties. Furthermore, the white matter of specific tracts also moderated the links of aerobic fitness and physical activity with working memory. Our results suggest that aerobic fitness and physical activity have an unequal contribution to the properties of white matter in adolescent brains. We propose that the differences in white matter properties could underlie the variations in the relationship between either physical activity or aerobic fitness with working memory.

Physical activity and aerobic fitness show different associations with brain processes underlying anticipatory selective visuospatial attention in adolescents

“…Nevertheless, they showed different associations with executive control and its underlying brain processes. Although the aerobic fitness has been shown to be more strongly associated with brain structural measures than physical activity (Ruotsalainen et al, 2019;Ruotsalainen et al, 2020), we did not find any relationship between aerobic fitness and brain oscillatory dynamics underlying anticipatory attention allocation. However, in behavioral measures higher aerobic fitness was related to higher drift rate values in the selective attention/inhibition task.…”

“…The dynamic interaction between hemispheres, modulating the processing capacity of the brain, is proposed to occur via the corpus callosum (Banich, 1998;Qin et al, 2016). A recent study by our group (Ruotsalainen et al, 2020) investigated the connection between both aerobic fitness and physical activity with the white matter in adolescents using MRI and fractional anisotropy (assessing microstructural changes in the brain's white matter). Although the main results in this study showed that only the level of aerobic fitness was related to white matter properties, it was also described that the level of fractional anisotropy in the body of the corpus callosum could moderate the relationship between physical activity and working memory.…”

“…On the other hand, AF is conceived as an achieved condition and it is usually directly measured by obtaining the maximal oxygen uptake (VO2max) during maximal effort tasks. Very few studies have investigated the effect of both PA and AF on cognition in humans in the same study (but see Haapala et al, 2014;Iuliano et al, 2015;Ruotsalainen et al, 2020), especially in adolescents (Tee et al, 2018). A recent study using structural MRI reported the associations of AF, but not accelerometer-measured PA, with grey matter volume in the adolescent's brain (Ruotsalainen et al, 2019), indicating that the level of PA alone is not directly associated with structural modifications in the brain.…”

Physical activity and aerobic fitness in relation to local and interhemispheric functional connectivity in adolescents’ brains

“…First, we studied the association of both aerobic fitness (estimated using a 20‐m shuttle run test [SRT]) and moderate‐to‐vigorous physical activity (measured with accelerometers) with voxel‐wise homotopic connectivity. Based on our previous findings showing an association between aerobic fitness and corpus callosum microstructure (Ruotsalainen et al., 2020), we hypothesized that aerobic fitness, but not physical activity, would be associated with 13–16‐year‐old adolescents’ homotopic connectivity. Further, in contrast to longer range functional connections, we studied the associations of physical activity and aerobic fitness with the brain's local functional connectivity using ReHo.…”

“…Studies of structural connectivity have shown that physical activity and aerobic fitness are related to the white matter structure connecting the brain's hemispheres, namely the corpus callosum, in children (Chaddock‐Heyman et al., 2014, 2018) and adolescents (Ruotsalainen et al., 2020). Although functional connectivity cannot be explained solely by considering the brain's structural connectivity, many studies have demonstrated that functional connectivity at least partly reflects underlying structural connections (Mollink et al., 2019; Shah et al., 2018; Van Den Heuvel et al., 2009).…”