Discussion
To our knowledge, this is the first study to assess the immediate cognitive effects of golf, Nordic walking and walking in older adults without underlying cognitive impairment. Our findings indicate that an acute bout of AE popular in this age group is able to improve cognitive function in older adults. Moreover, Nordic walking and walking also improve more demanding executive functions, which may be related to the higher relative exercise intensity. While no significant increase in cognition-related exerkines was observed immediately after exercise, Nordic walking produced significantly longer-lasting increases in BDNF.
Acute responses to cognitive function
We observed significant improvements in the TMT A test, which measures lower cognitive functions such as psychomotor speed, visuospatial searching and target-director motor tracking,33 with all exercise modalities. In addition, improvements in the TMT B test, which measures high-order processes, executive functions and set-switching ability,33 and these findings were statistically significant after Nordic walking and walking. From previous study, it is known that acute AE can improve task-shifting performance measured by the TMT A and B tests, while low to moderate intensity exercise may provide better results in task-shifting performance.8 Meta-analysis11 proves that moderate and vigorous exercise induces fatigue and dehydration. Longer duration of a cognitively demanding activity may induce more fatigue, cognitive fatigue and other factors (eg, dehydration) that can influence cognition, and this may explain the lack of improvement in the TMT B test results after golf trials as golf is a longer duration activity.
Studies have supported that a subject’s performance on TMT B is influenced by the low-level processes that are also involved in TMT A, such as visual scanning, motor speed, and basic visuomotor tracking. To account for this, we calculated corrected TMT B scores ((TMT B−TMT A) or (TMT B/TMT A)) to provide a more efficient measure of cognitive flexibility and processing speed that isolates the specific demands of set-switching in TMT B.31 32 We observed significant improvements in the total time of both the TMT A and B tests, which describes generally more low-level processes improvements. It is important to highlight that the TMT A test has an impact on both its own time values and those of TMT B, owing to the test protocol’s.31–33 Additionally, the enhancement in overall time following Nordic walking for the TMT B-TMT A test could potentially be attributed to the fact that Nordic walking places higher cognitive demands compared with regular walking. Among all exercise types, the TMT B/TMT A ratio score was between 2 and 3, suggesting essentially equal performance for these tests.32
The TMT-A and TMT-B time of our study participants were approximately 60% faster compared with normative data of TMT tests on older adults, which reported TMT A (53±26 s) and TMT B (137±54 s).9 It appears that our senior golfers may have better cognitive function than matched members of the general population, which could be due to their habitual physical activity and regular participation in cognitively demanding AE (golf),20 although confounding factors could include socio-economic status, education level and other factors, which may mean the baseline of a golf-playing cohort is different to the general population. Based on prior investigations7–9 as well as those of this study, low to moderate intensity physical activity seems to be positively associated with improved acute cognitive function for older healthy adults; this is particularly important as these types of exercise are more popular and perhaps more practical than high-intensity training/ exercise, which may not be feasible for older adults considering their health status, and activities participated in by their friends and peers.
Acute responses of BDNF to AE
BDNF is synthesised primarily in the brain and also in skeletal muscle.6 It has been suggested as a mediator of acute exercise-cognitive performance relationships.34 It is known that a single session of at least 30 min of moderate intensity (> 60% VO2max) AE can increase BDNF concentrations11 in healthy younger adults.34 However, it remains unclear whether acute cognitively demanding exercise has a similar impact on BDNF in healthy older adults.11 35 In our study, we were not able to find an immediate post-exercise effect of acute exercise on BDNF levels. Only one study directly measured the effect of playing an 18-hole golf round on BDNF levels in healthy younger adults (n=9, 31±4 years) and reported a modest but significant increase in BDNF (20%) immediately after the golf round, with levels returning to baseline after 1 hour of recovery.36 However, the duration of their golf round was longer (5 hours) in this past study than in our study (3.5 hours), and participants differed in age and prior exposure, where in our current study, all participants were regular weekly senior golfers.11 Interestingly, BDNF levels have been shown to decrease by about 6% in older women who participated in NW training for the first time after 1 hour of training, but BDNF increased if the person regularly practised Nordic walking.37 In our study, most of the golfers did not regularly practice Nordic walking. However, Nordic walking led to a significant increase in BDNF expression, while golf also produced higher BDNF levels after approximately 35–40 hours after the first exercise; this makes biological sense given that the maximum concentration of BDNF was found 24 hours after blood collection, and this concentration can remain stable up to 42 hours postexercise.38
Some studies have determined that acute AE can lead to a reduction in BDNF concentration.39 40 It has been suggested that this reduction may be due to the utilisation of BDNF in the repair of exercise-induced muscle damage or a reduction of BDNF release by the brain during recovery.40 41 The release of BDNF in response to exercise appears to be intensity-dependent, with higher-intensity exercise resulting in a greater release of BDNF.35 40 However, in our study, the intensity of AE was largely moderate (60%–76% HRmax), which might have affected the immediate lack of BDNF response. In addition, previous studies have indicated that BDNF levels may also vary within individuals over days and that physical fitness, sex, age and body weight can all influence BDNF concentrations.11 28 35
Acute responses of cathepsin-B to AE
In addition to BDNF, we also investigated the effect of acute AE on CTSB. However, CTSB is released from skeletal muscle cells, and we know that CTSB circulation increases in an AE intensity-dependent manner.10 The acute effects of AE on CTSB circulation in humans requires further study, especially since there are conflicting results regarding exercise and CTSB.6 In our study we observed non-significant increases immediately postexercise in this population. A recent past study observed no change in serum CTSB in response to acute low and moderate (40% and 65% VO2max) intensity AE, but there was a 20%±7% (p=0.02) and 30%±18% (p=0.04) increase in CTSB in response to higher intensity (80% of VO2max and VO2max) AEs.10 In another recent study, where acute moderate-intensity (50%–60% of HRR) postexercise effects of open-skill and closed-skill on CTSB were studied in healthy younger (age 18–25 years) athletes (n=45), an increase in CTSB was reported immediately (3 min) postexercise.6
From a clinical perspective, this study’s findings focused on acute changes in cognitive function and cognitive-related exerkines. In keeping with the wider literature on the role of health-enhancing physical activity on cognitive function, our study showed that all types of studied AE produce favourable effects on cognitive function in older adults, regardless of intensity or duration. However, no significant changes were observed in the cognitive-related exerkines. Further research is needed on the exercise dose-response relationship in exerkines, including BDNF and CTSB, based on exercise-specific parameters such as intensity, duration and type in populations including healthy older adults.
Study limitations
We conducted this randomised cross-over study in a real-world environment. This is advantageous for its generalisability to real-life contexts. However, due to the field-test conditions, differences in exercise modulation, such as distance and terrain, may influence the findings. Not all factors could be controlled as precisely as in a laboratory setting. The use of one postexercise measurement for BDNF and CTSB and blood samples taken after 12:00 hours may also impact the interpretation of the study’s findings due to potential biomarker changes over time and BDNF’s circadian rhythm expression. Additionally, it is important to take into consideration the small sample size when evaluating the results.
Considering the trial protocol, we recruited only golfers for the study as it was impossible to assign non-golfers to play a round of golf. Nordic walking was a new type of exercise for most participants, which may have led to poor technique and thereby exercise parameters of the activity. Those who regularly play golf may have better overall health and physical fitness, limiting the generalisability of the results to all older adults or those with chronic conditions.