Aerobic fitness, but not physical activity, is associated with grey matter volume in adolescents

Highlights

• We analyzed how both aerobic fitness and physical activity associate with grey matter volumes in adolescents.

• Aerobic fitness was associated with grey matter volume in the left superior frontal cortex and in left pallidum.

• Moderate-to-vigorous intensity physical activity did not associate with any region of interest.

Abstract

Higher levels of aerobic fitness and physical activity are linked to beneficial effects on brain health, especially in older adults. The generalizability of these earlier results to young individuals is not straightforward, because physiological responses (such as cardiovascular responses) to exercise may depend on age. Earlier studies have mostly focused on the effects of either physical activity or aerobic fitness on the brain. Yet, while physical activity indicates the amount of activity, aerobic fitness is an adaptive state or attribute that an individual has or achieves. Here, by measuring both physical activity and aerobic fitness in the same study, we aimed to differentiate the association between these two measures and grey matter volume specifically. Magnetic resonance imaging scans were used to study volumes of 30 regions of interest located in the frontal, motor and subcortical areas of 60 adolescents (12.7–16.2 years old). Moderate-to-vigorous intensity physical activity (MVPA) was measured with hip-worn accelerometers and aerobic fitness was assessed with a 20-m shuttle run. Multiple regression analyses revealed a negative association between aerobic fitness and left superior frontal cortex volume and a positive association between aerobic fitness and the left pallidum volume. No associations were found between MVPA and any brain region of interest. These results demonstrate unequal contribution of physical activity and aerobic fitness on grey matter volumes, with inherent or achieved capacity (aerobic fitness) showing clearer associations than physical activity.

Introduction

Aerobic fitness, also referred to as cardiorespiratory fitness, and physical activity are factors that are known to be associated with brain health. Studies have demonstrated that physical activity and aerobic fitness levels are positively associated with several structural properties of grey matter e.g. [[1], [2], [3]]. However, the majority of the research in this field has focused on older adults, and the generalizability of these results to other age groups is not straightforward. The integrity of the neural network in later life is strongly influenced by the developmental processes during the first decades of life, highlighting the importance of exercise-related effects on the brain during this time period. Importantly, research so far has focused on the influence of either physical fitness or physical activity on brain measures rather than comparing the effects between them. In order to understand the role and significance of exercise-related measures on brain structure, it is crucial to compare the contribution of physical activity behaviour vs. the level of aerobic fitness to grey matter volumes in adolescents.

Physical activity and aerobic fitness are distinct concepts. Caspersen et al. [4] defined physical activity as “any bodily movement produced by skeletal muscles that results in energy expenditure” (p.126). On the other hand, physical fitness is a condition or adaptive state that an individual has or achieves. Aerobic fitness is typically measured either directly by measuring oxygen consumption during maximal exercise test or indirectly by using submaximal tests or field tests, such as the maximal 20-m shuttle run. Physical activity can be determined subjectively using questionnaires or objectively with measurement devices such as accelerometers. However, self-reported physical activity assessments are considered less valid, because they are influenced by recall biases and other factors [5].

Even though measures of physical activity and aerobic fitness provide different information, they are related to each other to a certain extent. There seems to be a dose-response relationship between physical activity and aerobic fitness, concerning both the intensity and the amount of physical activity. In other words, the higher the intensity and amount of exercise training, the larger the improvements in aerobic fitness [[6], [7], [8]]. Importantly however, during adolescence the relationship between objectively measured physical activity and aerobic fitness is suggested to be only low to moderate [[9], [10], [11]]. Besides individual’s own actions, aerobic fitness is influenced by inherent properties, the genotype. More than half of the individual differences in aerobic fitness could be explained by heritability [12,13]. Studying the independent associations of both physical activity and aerobic fitness on grey matter volumes, in the same individuals, will critically extend our understanding of the specific aspects of these measures.

In recent neuroimaging literature, aerobic fitness has been associated with grey matter properties in several brain regions. Surprisingly, only one group has investigated this association in adolescents. Herting et al. studied male adolescents (15–18 years old) and found that the level of aerobic fitness correlated with left hippocampus volume [14] and with right rostral middle frontal cortical volume [15]. In children, aerobic fitness has been demonstrated to associate with several subcortical regions, such as the hippocampus and basal ganglia [[16], [17], [18], [19], [20]]. In addition, exploratory analysis by Chaddock-Heyman et al. [21] proposes that more highly fit children may have decreased cortical thickness in superior frontal cortex, superior temporal areas, and lateral occipital cortex. To the best of our knowledge, only one study investigated the relationship between physical activity and grey matter volumes in youth. Based on self-reported, but not objectively measured physical activity, Herting et al. [15] found that male adolescents in high physical activity group demonstrated larger right medial pericalcarine and left precuneus surface areas than in low activity group.

Given these findings, it is problematic to determine whether it is the regular physical activity or the aerobic fitness level that is more important for brain structures in youth. Animal models using rats bred for their response to exercise training (high vs. low induced change in running capacity) have shed some light on this issue. Nokia et al. [22] observed that high-response rats exhibited larger increases in hippocampal neurogenesis than low-response rats after physical training. However, high-response rats also ran more, so the amount of physical training was not equal between groups. When controlling for amount of physical activity, female high-response rats still showed a higher rate of neurogenesis in hippocampus [23]. Moreover, the training at same intensity levels induced different responses in brain-derived neurotrophic factor (BDNF) in low- and high-response rats [24]. Thus, in animal models, inherent running capacity seemed to affect brain responses even though the exercise was similar between groups. Taken together, these results suggest that neither the amount of physical exercise nor the running capacity can independently explain differential responses to exercise.

Age has been suggested to influence the physiological responses to exercise. Several studies have reported age-related differences in exercise responses [[25], [26], [27], [28]]. Supporting these human studies, animal models also indicate that age-related responses to exercise can be seen in cognition [29,30], in BDNF [30], and in microvascular function [31]. Although the main focus has been on the differences between young and old individuals, distinct responses to exercise have been also observed between adolescents and adults. Interestingly, Hopkins et al. [30] found that exercise enhanced relative levels of BDNF across brain regions and object recognition memory in adolescent rats 2–4 weeks after training intervention, but not in adult rats. Thus, brain responses to exercise can differ depending on age.

Despite the considerable number of studies concerning the effects of aerobic fitness or physical activity on grey matter volume in older adults, the evidence for this relationship in adolescence is inconclusive. To the best of our knowledge, no studies to date have compared objectively measured physical activity and fitness with grey matter volumes in adolescents. Therefore, we investigated how both physical activity and aerobic fitness associates with grey matter volumes in the adolescent brain. We measured physical activity objectively with accelerometers and aerobic fitness with a 20-m shuttle run. Magnetic resonance imaging (MRI) was applied to measure grey matter volumes. Based on the previous literature we hypothesized that both physical activity and aerobic fitness would show positive association with grey matter volumes in the basal ganglia and hippocampus.