Background
Acute bouts of exercise elicit small-moderate beneficial effects on cognitive function in adults [
1], children [
2] and adolescents [
3]. However, the exercise-cognition relationship is a complex phenomenon, affected by a number of factors such as the modality, intensity and duration of the exercise bout, age, physical fitness and the cognitive domain assessed [
4,
5]. Much of the research in the adolescent population has employed traditional continuous lab-based exercise protocols, examining treadmill running/walking [
6‐
8] and cycle ergometry [
9‐
12]. Furthermore, the focus has been primarily on cognitive function immediately post-exercise, including the domains of executive function and working memory [
6,
9,
13]. There is also some evidence that the benefits of an acute bout of exercise persist for up to 45 min [
14‐
16] post-exercise; yet the time-course of exercise-induced cognitive effects beyond this are currently unknown. Only one study has demonstrated acute cognitive benefits up to 60 min post-exercise, with improved inhibitory control found 60 min following moderate intensity circuit exercise [
17]. However, no study has examined the effect of an acute bout of exercise beyond 1 h post-exercise in adolescents.
Furthermore, many of the acute exercise protocols used in previous studies are difficult to incorporate into a school day due to reliance on specialist equipment, such as motorised treadmills and cycle ergometers, which may not be available in a school setting. This is known to be a prominent barrier to exercise participation in this population [
18]. Recent research has attempted to address this issue by utilising acute school-based protocols consisting of sprint intervals [
14], shuttle running [
15,
19], Basketball [
16] and cognitively-engaging exercise [
13,
20]. The use of acute games-based activity, such as Football, is an attractive modality given that the habitual activity patterns of young people are high-intensity and intermittent in nature [
21], as seen in team games [
22]. Furthermore, games-based activity is typically a mode of exercise that young people enjoy; a vital consideration for long-term implementation [
23]. Positive effects of such acute school-based protocols have been demonstrated across a range of domains of cognition, including attention [
13,
15,
20], working memory [
16] and executive function [
14,
16]. Football is the most popular games-based exercise amongst adolescents [
23], with only one study to date examining the acute effects of Football on subsequent cognitive function [
24]. A brief (20 min) bout of high-intensity Football improved inhibitory control performance 20 min post-exercise, compared to walking Football and a resting control [
24]. However, it is unknown how acute Football affects other domains of cognitive function, such as working memory, as well as the duration of the transient improvements post-exercise.
Cross-sectional evidence in adults suggests that those with a higher physical fitness, assessed by V̇O
2max, have quicker response times on a psychomotor speed task [
25]. Similar results have been demonstrated in overweight and sedentary children, using V̇O
2 peak as the fitness criterion [
26]. Hillman et al. [
27] found that both high-fit children and adults, assessed with the PACER, a variation of the multi-stage fitness test, performed better on an executive function task than their low-fit counterparts. Whilst there is strong evidence of a positive relationship between physical fitness and cognitive function in children and adults, there is limited knowledge concerning adolescents. Adelantado-Renau et al. [
28] used a battery of fitness tests, including the multi-stage fitness test, in a group of healthy adolescents and found that higher physical fitness was positively associated with academic performance. In addition, higher physical fitness (assessed by the Andersen intermittent test) was associated with a greater inhibitory control performance in older adolescents (~ 14 y) [
29]. However, it is not known how physical fitness affects key cognitive domains such as executive function and working memory in younger adolescents, where they are of particular importance for academic achievement [
30].
Recent reviews suggest that physical fitness moderates the acute exercise-cognition relationship [
1,
4] – particularly when cognition is measured immediately post-exercise [
1], or with reference to learning and memory [
4]. However, another recent meta-analysis concluded that physical fitness does not moderate the acute exercise response, with respect to aerobic exercise and executive function [
3]. Specifically, it has been shown that adolescents with a higher level of physical fitness, assessed by a multi-stage fitness test [
16] and a continuous-graded maximal exercise test until exhaustion [
11], demonstrate improved response times on an executive function task immediately after cycling [
11] and 45 min after basketball exercise [
16]; whilst in lower fit adolescents error rates were higher [
11] and response times were slower [
16] following exercise. In addition, response times on a working memory task were improved, in the high-fit group only, following basketball exercise [
16]. Overall, the available evidence suggests that higher physical fitness may enhance the post-exercise improvements in cognition. This may also be more applicable to games-based exercise, which has both cognitive and physical demands, whereby those with a higher physical fitness can allocate greater cognitive resources to the activity itself [
3]. The underlying mechanisms behind this relationship remain unclear, although it has been surmised that circulating growth factors – particularly brain-derived neurotrophic factor (BDNF) – may have a role to play [
31,
32].
BDNF is stated to have an instrumental role in the structural formation and function of the brain [
33] and plays an important role in the promotion and maintenance of synaptic connectivity [
34]; which is suggested to be one of the mechanisms through which BDNF may mediate post-exercise improvements in cognitive function [
4]. To date, only resting BDNF has been investigated in relation to objectively measured physical activity in adolescents; whereby physical activity and plasma BDNF were not related [
35] and mean physical activity and serum BDNF were negatively related in adolescent boys only [
36]. Furthermore, no studies have examined the time-course of BDNF concentrations in the hours following an acute bout of exercise in adolescents – which is an important knowledge gap to fill given the suggested role of BDNF in mediating post-exercise cognitive improvements [
31,
33]. The response of BDNF to an acute bout of ecologically valid games-based activity in adolescents, and the moderating role of physical fitness in this exercise-BDNF relationship, is currently unknown.
The aim of the present study was to investigate the effect of an acute bout of outdoor Football on information processing, inhibitory control and working memory and circulating BDNF concentration in adolescents, for up to 2 h post-exercise. A secondary aim of the study was to examine whether there were differences in overall cognitive function performance and BDNF concentration between high and low-fit participants, and whether physical fitness moderates cognitive function and BDNF concentrations following exercise.
Discussion
The findings of the present study show that acute Football activity did not influence subsequent information processing, inhibitory control and working memory response times for this group of adolescents overall. However, response times for the high-fit group were quicker across all levels of cognitive tasks, compared to the low-fit group. When considering the moderating role of fitness on the acute responses to exercise, 60 min of Football was beneficial for working memory in the high-fit group, whereas working memory tended to be unaffected by exercise in the low-fit group. The present study is also the first to measure the time course of BDNF post-exercise in an adolescent population, with serum BDNF unaffected by acute Football activity and fitness.
The current study demonstrates that response times, during information processing, inhibitory control and working memory tasks, are quicker in adolescents with a higher physical fitness, when compared to their low-fit counterparts. This is in support of recent meta-analyses in children and adolescents demonstrating that chronic exercise interventions, which aim to improve physical fitness, lead to improvements in cognitive function [
49,
50]. The findings of the present study extends previous cross-sectional findings in children [
26‐
29] and adults [
25,
32] to three distinct domains of cognitive function (information processing, inhibitory control and working memory) in adolescents. Response times were consistently quicker in the high-fit group across the congruent and incongruent levels of the Stroop Task, as well as across all three levels of the Sternberg Paradigm, compared to the low-fit group. This enhanced cognition in high-fit adolescents may explain the improved academic performance in high-fit young people that has previously been reported [
28,
51,
52] The findings of the current study, along with previous work, highlight the importance of high levels of physical fitness for cognitive function and academic achievement in children and adolescents.
The current study also demonstrates that the acute benefits to working memory following exercise were exclusive to the high-fit group only. This is an important finding, given that physical fitness is suggested as a key moderator of the exercise-cognition relationship [
1,
4], yet there are few empirical studies directly investigating this, especially in adolescents. Recent work has investigated this through a 60 min Basketball session [
16] and a 20 min bout of cycling [
11]. Even though the modality and duration of exercise are vastly different, both studies concluded that the improvement in cognition, following an acute bout of exercise, was enhanced in those considered high-fit; in line with the findings of the present study. An explanation for this may be the differences in relative exercise intensity during the Football activity, with the low-fit group working at a higher relative exercise intensity (~ 80% HRmax) compared to the higher fit children (~ 70% HRmax). It is possible that for the low-fit children the exercise was of too high an intensity and thus too demanding. A recent review suggests that enhancements in cognitive function, following exercise, tend to occur under moderate intensities with attenuated effects under light- and high-intensities; which is consistent with an inverted-U theory [
4]. An additional explanation might be under the transient hypofrontality hypothesis, whereby neural activity in the brain – mainly the prefrontal cortex – is reduced as a result of very high-intensity exercise [
53].
The present study also provides novel evidence regarding the effects of Football on subsequent cognitive function (particularly working memory) in adolescents, with only one previous studying investigating the acute effects of Football [
24]. The majority of previous work in adolescents has used traditional forms of exercise; such as continuous running [
6,
7,
19,
20], walking [
8] and cycling [
9,
11,
12]. Whilst traditional exercise protocols are easy to control in a laboratory setting, they do not necessarily reflect the habitual activity patterns of young people [
21]. The use of Football may provide an attractive model; viable for adolescents and thus has real-world applicability. Whilst the cognitive benefits following Football were exclusive to high-fit individuals and the domain of working memory in the present study, there was also no evidence of a decline in performance for the low-fit participants because of exercise. This suggests that games-based exercise, such as Football, can still be a valid mode of activity for young people, given the known health benefits [
54], the popularity [
46] and the ease of access to the equipment needed.
The present study is the first to examine the time-course of circulating BDNF in adolescents following an acute bout of exercise. This is an important knowledge gap, given the potential mediating role of BDNF in the exercise-cognition relationship [
31,
33,
55] and the transient nature of improvements seen in cognitive function following exercise. Whilst peripheral BDNF increases immediately after acute bouts of exercise in adults [
55,
56], data from the current study did not provide evidence of this effect in adolescents. The post-exercise increase in BDNF is positively associated with the intensity and duration of the exercise bout [
55]. The exercise bout in the current study was of a sufficient duration, however the intensity may not have been sufficient enough to elicit increases in BDNF post-exercise. The present study did however demonstrate cognitive improvements post-exercise, despite the lack of change in peripheral BDNF. This may be explained by the fact that central BDNF (in the brain) was not measured in the present study, due to the constraints of such an assessment in adolescents, and arguably central BDNF is more important for the cognitive benefits of exercise. The improvements in response times seen in the present study, without any noticeable change in peripheral BDNF, may be explained by this or suggest that another mechanism is mediating these cognitive benefits.
A potential limitation of the present study is that the socioeconomic status of the participants was not accounted for. It has been reported that socioeconomic status is implicated in the development of attentional processes in young children [
57] and executive function throughout childhood and adolescence [
58]. However, there is evidence suggesting that a lower socioeconomic status is associated with lower levels of physical activity [
59] and physical fitness [
60] in adolescents; which suggests that the effect of socioeconomic status on cognitive function may, in part, be mediated through physical activity and physical fitness. The relationship between physical fitness and cognitive function in the present study is cross-sectional and thus, causation cannot be attributed. However, this is still an important finding as this relationship was evident across all test levels for both the Stroop test and the Sternberg paradigm. Whilst the number of trials used in both the Stroop and Sternberg tests could be seen as a limitation, it was necessary to reduce the amount in order to facilitate the use of both tests within a realistic timeframe. The choice of control condition (seated rest) in the present study could also be seen as a potential limitation, particularly as the exercise session included both physical and cognitive elements. However, it would be difficult to match the social interactions of the exercise session and the use of such a control condition also offers ecological validity. A further potential limitation is the measurement of global response time (rather than reaction time and movement time separately), due to the practicalities of conducting such measurements in field-based studies of this nature.
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