Brain basis for physical activity levels mediate beta Inhibition to improve cognitive function in elderly based on multimodality monitoring

The efficacy of long-term regular PA in improving CF in older adults has been extensively documented, yet the optimal dosage profile and underlying structural basis in various aspects of CF remain uncertain. While some studies have indicated that the effects of VPA may be superior to other forms of exercise, there is considerable heterogeneity between studies, and the neural mechanisms remain poorly understood. This study builds upon previous research to examine the differential effects of VPA and MPA on cognitive function in older adults, with a focus on the physiological characteristics of intracranial gray matter structures across diverse populations. The objective is to develop a more rational and effective exercise prescription for this age group, with a rationale grounded in physiological mechanisms.
The initial findings of this study indicated that regular PA significantly enhanced CF in older adults. However, the effect of VPA on response inhibition and cognitive flexibility was more pronounced. In this study, the 2-Back and Stroop scores of HG and MG were higher than those of CG, and the response time was shorter than that of the CG. However, the stop-signal and Stroop scores of the HG were higher than those of the MG. This suggests that VPA enhances the efficiency of CF improvement in older adults. Consequently, hypothesis (I) can be accepted, which is consistent with previous results. Anabela conducted a longitudinal study to examine the effects of a short period of time (one week) of moderate-to-vigorous physical activity (MVPA) on executive function in older adults. The results demonstrated that the PA group outperformed the sedentary control group in processing speed and language function after the intervention23. With regard to memory, Wang observed that 12 weeks of MPA (Tai Chi) significantly enhanced older adults’ 2-back task accuracy and reaction time, thereby enhancing their working memory24. To further verify whether PA level leads to differences in CF in older adults, Li analyzed the correlation between PA level and CF. The results indicated a positive correlation between muscle strength, PA level, and memory and cognitive flexibility in older adults25. This also implies that elevating PA levels is an effective way to improve CF. To substantiate this assertion, Wang conducted a cross-sectional survey of 647 older adults aged 60 and above, categorizing them according to their levels of PA in terms of visuospatial, attention, language, abstraction, and delayed recall. The results demonstrated a positive correlation between PA and CF scores, with a saturation effect between the two variables10. In contrast, Paula, after a comprehensive evaluation of 104 studies, found that while PA may mitigate the decline in CF in older adults, all follow-ups of more than 10 years showed no significant association26. In conjunction with the present results, this study hypothesizes that age may have contributed to the gradual attenuation of the long-term regular PA effect. Paula included a large number of studies in which participants were older than 76, a range that exceeds the WHO limit of Very Old27. In contrast, the sample in this study was between 60 and 65 years old, which may have resulted in an underestimation of the effect of PA on CF. Collectively, these findings suggest that age is not only a crucial factor in determining the effectiveness of PA, but also increases the associated risk of exercise. In conclusion, while increasing PA levels can be an effective means of maintaining CF in the retired population, the key factor is to maintain a long-term PA habit in the early years to build a foundation of physical fitness for exercise in old age.
The second finding of the present study was that VPA demonstrated superior efficacy in improving CF, which may be related to higher alpha occupancy in the resting state and suppression of mid-frequency beta with higher high-frequency β-oscillation in the task. Although VPA resulted in greater frontal-to-central ERP amplitude, there was no significant difference in terms of shorter latency compared with MPA. In the present study, exercise intensity was found to be positively associated with resting state alpha occupancy and mid- and high-frequency β-oscillation in the task, and inversely associated with resting state mid-frequency β-band activity and α-oscillation in the task. In contrast, PA resulted in positive and negative potential amplitude in a larger area of frontal, parietal, and central regions in the older adults’ task, significantly shortening the latencies of P300, N200, and N450. Although VPA-mediated individuals exhibited a greater maximal ERP amplitude, the latency was not significantly shorter than that of MPA. Therefore, hypothesis (II) could not be fully accepted. This is consistent with some of the findings of Wang, who found that, compared with MPA, long-term VPA not only significantly elevated individuals’ executive function and suppressed midrange β-band activity during quiet time, but also improved the body’s central tolerance to fatigue and stress stimuli14. Similarly, Numan compared the EEG characteristics of professional dancers and fast-ball sports athletes and found that the fast-ball athlete exhibited a greater alpha band amplitude at rest and a higher level of β-oscillation than the dancer during the task28. Zhang demonstrated that the mediating effect of high β-oscillation in cognitive processes was significant only after prolonged VPA, which may be an important mechanism by which VPA reverses the decline in CF brought about by aging29. In terms of ERP, Patelaki’s findings indicated that long-term PA resulted in individuals exhibiting greater positive amplitude of the P200 and P300 in the frontal and central regions during a memory task. This attenuation pattern was hypothesized to reflect a more diligent recalibration of neural processes following long-term PA30. Furthermore, Chang demonstrated that a single session of PA can have a positive effect on CF. He discovered that individuals exhibited significant improvements in their Stroop scores and reaction times following acute exercise. Moreover, he observed that the N100, N200, and P300 components of the process exhibited the most pronounced changes31. It is noteworthy that Ludyga demonstrated a correlation between negative values of N200 and N450 and participation in open-skill sports. This was evidenced by the observation that individuals who engaged in such PA for an extended period of time exhibited higher Stroop and Stop Signal scores than those who engaged in closed-skill sports17. This effect was also observed in the present study with regard to VPA. Therefore, it can be postulated that incorporating open-skill sports into weekly PA may further enhance the improvement of CF. In contrast to the above evidence, the present study used PA level as a variable for the first time and found that older adults with long-term VPA had higher N200 and P200 amplitude fluctuations than MPA and had shorter latencies. This also shows that VPA improves working memory and cognitive flexibility better than MPA, and the neural mechanism may be related to N200 and P200 amplitude variability with shorter latency.
The third finding of the present study was that regular PA improved gray matter density in older adults, whereas VPA had a more significant stimulatory effect on frontal and temporal lobe regions. In the present study, long-term MPA and VPA resulted in greater amplitude of MFG, RSFG, LCG, LACG, LSMA, RSMG, and PHG densities in older adults. The effects of VPA on RSFG, LCG, LACG, and RSMG areas were greater than those of MPA, in which RSFG and LCG are generally associated with higher cognitive functions and are involved in behaviors such as control of external stimuli, attentional control, and pain perception32, whereas LACG and RSMG play important roles in spatial perception, hand coordination, and language comprehension, and also play an important role in fine motor control33. This also implies that older adults with long-term VPA will have higher levels of executive functioning. Therefore, hypothesis (III) can be accepted. The above phenomenon can be explained in terms of neural mechanisms. Chen’s systematic evaluation demonstrated that at least three months of VPA can optimize the activity status of CF-related brain regions (anterior cingulate gyrus, middle anterior gyrus, and supraparietal lobule, etc.) and increase prefrontal cortical volume in older adults34. To elucidate the mechanisms underlying the beneficial effects of PA on memory function, Steventon observed that, following a single week of PA in older adults, individuals exhibited elevated voxel counts in the corpus callosum, uncinate fasciculus, and parahippocampal cingulum relative to baseline levels, accompanied by selective increases in hippocampal blood flow. This evidence suggests that brief periods of PA can induce alterations in intracranial microstructure and vascular brain35. Similar to the present study, Liu, after comparing the effects of two mind-body exercises (Tai Chi and Baduanjin) on various gray matter structures in older adults from the perspective of resting-state functional connectivity of brain networks, found that the two types of PA significantly increased the resting-state functional connectivity (rsFC) of the posterior cingulate cortex with the right putamen/caudate, but individuals with longer habituation showed greater rsFC between the medial prefrontal cortex (mPFC) and the right putamen/caudate volume. PA levels and rsFC with the orbital prefrontal gyrus were negatively correlated with the Visual Reproduction subscore36. Despite the beneficial effect of PA on gray matter density in older adults, exercise-induced fatigue due to transitioning from one type of PA to another can have a negative impact. Koevoets used the timeliness of PA as a variable and found that six months of PA did not result in an increase in hippocampal subfield and cortical thickness or gray matter volume in older adults, despite improving CF. However, the prevalence of high fatigue in their included sample is a cause for concern37. In the context of the present study, we conducted the first comparison of gray matter density differences between older adults under long-term MPA and VPA by MRI. Our findings indicated that although long-term VPA resulted in greater structural improvement of gray matter in frontal and temporal lobe regions, controlling the amount of exercise is a key factor in exerting this effect. The present study thus indicates that the course of VPA necessitates the implementation of a training program that is continuously adapted to the individual’s subjective level of fatigue, thereby preventing the occurrence of exercise fatigue and exercise-related injury.
In conclusion, increasing weekly PA levels can enhance CF to a greater extent in older adults, and its neural mechanisms are more complex. With regard to endogenous mechanisms, the VPA group demonstrated greater α-band activity during quiet than controls, which was more significant than the high β-oscillation of MPA. On a structural basis, PA significantly enhanced gray matter density in older adults, but greater gray matter volume in frontal and temporal regions was observed in the VPA population. Consequently, VPA was superior to MPA in the promotion of CF. However, given that the focus is on older adults, it is important to consider the physiological limitations of this group. Excessive or inappropriate training programs may increase the probability of injury and fatigue. Therefore, based on Principle of Appropriate Load38 and Principle of Motivation in Sports39, it is recommended that older adults use the rating of perceived exertion (RPE) to quantify their own exercise sensation, with the aim of improving as much as possible within the limited scope of the PA level. Furthermore, the Feeling Scale (FS) can be employed to assess the psychological state at different points in time, thereby enabling the program to be adapted in a timely manner in order to optimize exercise motivation.
Limitations and suggestions for future research
The present study aimed to investigate the effects of long-term PA on CF in older adults from the perspectives of working memory, response inhibition, and cognitive flexibility. Additionally, the study sought to elucidate the underlying neural mechanisms and structural bases of these effects through ERP and MRI techniques. Furthermore, the differences in the effects of MPA and VPA on CF were also compared. The objective was to identify more efficient exercise prescriptions to enhance exercise efficiency in older adults. Although this study employed a cross-sectional design to compare the characteristics of the three populations in terms of CF, EEG, ERP, and MRI, through a cohort study, and evaluated them according to the results, several limitations remain.
Firstly, it is necessary to define the age range of the participants. In this study, 68 older adults were included as subjects, all of whom were between the ages of 60 and 65. This age range is qualified by the WHO as the stage of initial aging. Older adults in this age group are in better physical condition relative to those over 70 years of age, thus supporting the implementation of different levels of PA. However, the probability of risk for PA increases with age. Consequently, if the study is focused on older adults, it is important to consider the reality of implementing PA in the 70 + age group. Future research should therefore address the uncertainty of PA with age.
Secondly, the issue of analyzing methods of MRI must be addressed. In general, conventional MRI and fMRI studies should establish a prediction model for the effect of different elements on gray matter volume by singular value decomposition (SVD), latent vector (LV), and structural covariance network analysis based on the number of voxels of different variables with MRI. However, this method has certain characteristics, such as only being able to compare the differences between two groups of variables. However, the present study included three groups of variables, and the difference between the effects of MPA and VPA on gray matter density was minimal, allowing for clear observation of the difference in volume from the MRI images. This phenomenon can also be seen in Table 3 of this study. Consequently, in this study, the MRI results section did not include images of the difference in gray matter structure between MPA and VPA. Instead, these differences were enumerated in Table 3.
In future studies, we will therefore focus primarily on heterogeneous variations for older adults across the age range. Furthermore, we will divide the PA forms based on intensity, program, or open/closed characteristics, such as HIIT vs. MICT or basketball or running. Concurrently, the fMRI method will be incorporated into the study, which will permit a more intuitive comprehension of the activity and volume characteristics of individual brain regions under different conditions, and will provide more accurate and authoritative exercise prescriptions for the cognitive health of the elderly.
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