Chronic effects of different exercise types on brain activity in healthy older adults and those with Parkinson’s disease: A systematic review

Abstract

Objective: This study aimed to compare the regulation of brain activity by different kinds of long-term exercises (Tai Chi, treadmill training, and dancing) in healthy older adults and those with PD.

Methods: From January 2000 to October 2021, the electronic databases PubMed, Web of Science, and Scopus were searched. All articles were screened throughout the inclusion and exclusion criteria, which was followed by PICOS criteria. Finally, all articles were systematically reviewed with analyses.

Results: 29 studies were identified for this review, 24 of which were finally included in a group of healthy older adults, and five of which in a group of people with PD. All studies showed that significant changes were showed on people with PD and healthy older adults’ brain activity after three terms of the exercises we chose. An inverse change trend on the functional connectivity in people with PD was observed after treadmill training, whereas increased brain activity, cognitive function, memory, and emotion were noticed in healthy older adults.

Conclusion: Our findings suggest that different patterns of brain activity were also observed between healthy older adults and people with PD after treadmill training. However, more robust evidence and comprehensive studies are needed to determine if there is a difference between healthy older adults and people with PD.

1 Introduction

Parkinson’s disease (PD) has become the second-most common neurodegenerative disorder that typically affects older adults (Hirtz et al., 2007; Wirdefeldt et al., 2011). The main characteristic clinical hallmarks are the degeneration and loss of primarily dopaminergic neurons in the substantia nigra, and the accumulation of misfolded intracellular alpha-synuclein (α-syn) within Lewy bodies (Balestrino and Schapira, 2020). PD leads to the reduction of dopamine secretion and degeneration of the nigrostriatal pathway. With disease progression, the “Lewy body disease” will spread to the neocortex and cortical areas (Tysnes and Storstein, 2017). Recent research shows that the risk of developing PD is associated with genetic factors, consumption of dairy products, history of melanoma, and traumatic brain injury (Ascherio and Schwarzschild, 2016). Meanwhile, pollution due to pesticides and heavy metals resulting from industrialization is also a potential factor (Li et al., 2021). The classical clinical signs of PD are divided as follows: motor symptoms (i.e., bradykinesia, tremor, and rigidity); and non-motor symptom (i.e., cognitive impairment, sleep disorders, and depression). These co-occurring and prevalent symptoms of PD will induce serious psychological or medical pathology and incur a huge burden on society due to deterioration of physical health and loss of productivity (Silva De Lima et al., 2019). Globally, approximately 1% of all older adults aged 65 years old or above suffers from PD, and this percentage is predicted to increase with the growth of the aging population (Moore et al., 2005; Kasten et al., 2007; Lees et al., 2009). Current regimens in the treatment of PD are conventional and permanent, including drug treatment (especially levodopa) and surgical treatment (Ashoori et al., 2015; Mico-Amigo et al., 2017). Mainly, the motor symptoms of the disease are alleviated by these treatment approaches. However, the long-term use of drugs can lead to severe side effects, such as drug dependence and loss of efficacy.

Physical exercise can be used as an important supplementary treatment to improve these symptoms in people with PD. For example, treadmill walking exercise (Herman et al., 2007; Fisher et al., 2008) or progressive resistance training (Brienesse and Emerson, 2013; Lima et al., 2013) can improve these motor symptoms (i.e., muscle strength and endurance, mobility, and spatial parameters); and mindfulness yoga (Kwok et al., 2019) or resistance training reduces depressive, anxiety symptoms and improves the quality of life and functionality of older adults with PD (de Lima et al., 2019). Furthermore, many studies have also reported the benefits of exercise for others; it can enhance the plasticity of the nervous system for older adults (Cotman and Berchtold, 2002; Erickson et al., 2007) and people with brain injury (Betker et al., 2007), mild cognitive impairment (Hemmeter and Ngamsri, 2022), and Alzheimer’s disease (Zhou et al., 2022).

Different exercise modalities, such as endurance training, Tai Chi, whole-body vibration (Dincher et al., 2019), water exercises (Loureiro et al., 2022; Peyre-Tartaruga et al., 2022), and dancing, are feasible for healthy older adults and those with PD. For instance, long-term endurance training may even increase the cortical volume of the prefrontal area and the connectivity between brain regions, resulting in better emotion, memory, attention, and executive control abilities (Weng et al., 2017). Similarly, the research finding supports the Tai Chi group which demonstrated stronger frontostriatal functional connectivity in trials (Liu et al., 2020). Moreover, Rektorova et al. (2020) found that changes in the brain structure were observed after dance training compared with the control group; moreover, the executive functions slightly improved.

In parallel, previous works showed that changes in the brain structure and connectivity with ageing and PD impact cognitive processes, walking, and balance (Seidler et al., 2010; Tian et al., 2017), likely due to the involvement of common neural centers (Stuart et al., 2018). Specifically, some changes in certain brain areas (such as gray matter atrophy, changes in brain function connections, etc.) may cause movement disorders (Yogev-Seligmann et al., 2008; Agosta et al., 2014; Sehm et al., 2014; Hoffstaedter et al., 2015). Therefore, these three forms of exercises (Tai Chi, treadmill training, and dancing) may improve motor and non-motor symptoms by changing brain activity and structure.

Recent studies on the brain activity of exercises have not generally focused on neurological mechanisms, but those which did have mainly utilized electroencephalography (EEG), functional magnetic resonance imaging (fMRI), and functional near-infrared spectroscopy (fNIRS) (Chang et al., 2017). Innovations in non-invasive neuroimaging have been able to make remarkable advances in rapidly assessing cortical activity for healthy older adults and patients with PD.

Although evidence supporting the use of Tai Chi, treadmill training, and dancing to improve clinical measures of motor and cognitive functions exists, most studies were limited to focusing on the effects of exercise intervention and lacked the comparison between some exercise interventions. To the best of our knowledge, several systematic reviews have systematically investigated the effect of single exercise interventions, such as dancing, endurance training, and Tai Chi (Halloway et al., 2017; Pan et al., 2018; Pereira et al., 2019; Muinos and Ballesteros, 2021). However, it is unclear if the effects between these three types of exercises, healthy older adults, and people with PD are different. Therefore, this review aimed to compare the effects of the different kinds of exercises (Tai Chi, treadmill training, and dancing) on brain activity in healthy older adults and patients with PD.

2 Methods

2.1 Search strategy

The PubMed, Web of Science, and Scopus database were searched from January 2000 to October 2021 in this study. Then, the keywords, synonyms, search strategies, and Boolean logic operators were used for retrieval by the reviewer (LW), including four fields (connected with “AND”) with independent search terms (Table 1). The first search field focused on the participants, who were categorized according to the population of interest (i.e., older adults, healthy older adults, and older adults with PD). The second search field included possible synonyms for the forms of exercise, i.e., Tai Chi (Tai Chi Chuan), treadmill (walking) exercise, and dancing (dance). The third search field comprised synonyms for the brain function and included “brain,” “neural,” and “neuronal.” The fourth search field focused on the measurement device of interest to assess the cortical activity (i.e., EEG, fNIRS, and fMRI), these three kinds of detection devices are commonly used for detecting brain activity. All key search terms were matched and explored with medical subject headings (MeSH). Moreover, the reference lists of the included studies were also searched. The PRISMA flow chart of study design, which includes the search information at each stage of the study process, is presented (Figure 1).

FIGURE 1

2.2 Eligibility criteria

The inclusion and exclusion criteria were created by two reviewers (LW and FL). Studies were included if 1) it was printed in full English text; 2) the aim of the study was to examine the chronic effects of three terms of exercises on brain activity in healthy older adults and people with PD; 3) the target population: healthy older adults and people with PD with a mean age of 60 years or above; 4) the studies included at least distinct exercise interventions or one exercise intervention (Tai Chi, treadmill training, and dancing) with a no-exercise controlled intervention (NE) or other types compared in each trial; 5) the studies included at least one measurement device (EEG, fMRI, or fNIRS). The searches included in this review were restricted to exercise intervention trials, which were published from January 2000 to October 2021.

2.3 Quality assessment of studies

The methodological quality was independently assessed according to the physiotherapy evidence database (PEDro) scale (ranging from 0 to 10 points). To reduce the risk of bias in assessment, the work was performed by two reviewers (LW and LT). Any disagreements in scores between reviewers were judged after discussing with the third reviewer.

2.4 Data extraction

Data were extracted by the reviewer (LW), synthesized into table format, and confirmed by another reviewer (LT), according to the information strategy. The data extracted included authors, the year of publication, demographic, experimental protocol, measurement device, regions of interest, signal pre-processing, data outcomes, and conclusion.

3 Results

3.1 Study selection

The search strategy fielded 3,649 articles according to the key terms from three publication databases (Moher et al., 2009). Following the screening of the title and abstract and removal of duplicates, 29 articles were included according to the inclusion and exclusion criteria, 24 of which were finally included in the group of healthy older adults, and five of which were in the group of people with PD. Fourteen of the twenty-four reported Tai Chi (Fong et al., 2014; Tao et al., 2016; Tao et al., 2017a; Tao et al., 2017b; Liu et al., 2018; Port et al., 2018; Wu et al., 2018; Liu et al., 2019; Mei et al., 2019; Yang et al., 2019; Yue et al., 2020a; Yue et al., 2020b; Yue et al., 2020c; Liu et al., 2020), four studies investigated treadmill training (Smith et al., 2013; Chuang et al., 2015; Chirles et al., 2017; Won et al., 2021), and seven studies included dancing (Chuang et al., 2015; Eggenberger et al., 2016; Azman et al., 2017; Ji et al., 2018; Zilidou et al., 2018; Voss et al., 2019; Balazova et al., 2021). Five studies reported treadmill training in people with PD (Carvalho et al., 2015; Maidan et al., 2017; Maidan et al., 2018; Calabro et al., 2019; Droby et al., 2020). Articles on healthy older adults were more in number than those on patients with PD. Tables 2, 3 summarize the essential characteristics of these studies in healthy older adults and people with PD.

3.2 Characteristics of included studies

The participants included healthy older adults and patients with PD with average ages of 69.7 ± 6.3 and 65.3 ± 4.2 years of age in the selected articles, respectively. The range of disease severity of PD was assessed by using the Hoehn and Yahr scale (Hoehn and Yahr, 2001), from 1 to 2 (mild to moderate level).

The duration and frequency of Tai Chi intervention ranged from 6 weeks to 10 years, 2–7 sessions/week, and 30–90 min/session; the duration and frequency in treadmill training included 12 weeks, 3–4 sessions/week, and 30 min/session; the training intensity gradually increased and was maintained at 50–60% of heart rate reserve (HRR); the duration and frequency of dancing intervention ranged from 6 to 24 weeks, 2–4 sessions/week, and 20–60 min/session in healthy older adults, while the duration and frequency of treadmill training ranged from 6 to 12 weeks, 2–5 sessions/week, 30–45 min/session in people with PD.

Of the 29 studies, 14 studies reported that brain activity was assessed by use of different types of tasks (e.g., N-back task, Flanker task, walking, etc.) while participants were acquiring data pre- and the post-training, namely, 11 studies in healthy older adults (Smith et al., 2013; Fong et al., 2014; Chuang et al., 2015; Eggenberger et al., 2016; Azman et al., 2017; Ji et al., 2018; Port et al., 2018; Wu et al., 2018; Mei et al., 2019; Yang et al., 2019; Liu et al., 2020) and three studies in people with PD (Maidan et al., 2017; Maidan et al., 2018; Calabro et al., 2019). On the other hand, many regions of interest such as prefrontal cortex (PFC), anterior cingulate cortex (ACC), and bilateral hippocampal (BHPC) were included in healthy older adults and people with PD.

3.3 Methodological quality

The scores for each criterion using the PEDro scale are presented in Table 4. The mean score for all 29 trials was 5.52 ± 1.33. Across the 29 studies, neither the participants nor the therapists administering the program were blinded to the intervention. Only two studies, which were separately derived from the group of healthy older adults and people with PD, concealed the allocation of all participants, reported blinded assessors, and used intention-to-treat analysis (Maidan et al., 2018; Wu et al., 2018). Several studies recruited and allocated participants based on exercise-related experiences, and thus failed to meet the requirement of random allocation (Fong et al., 2014; Liu et al., 2018; Port et al., 2018; Mei et al., 2019; Yue et al., 2020a; Yue et al., 2020b; Yue et al., 2020c; Liu et al., 2020), leading to the lower score.

3.4 Key findings of healthy older adults

The key findings and conclusions of the studies are reported in Table 5. In Tai Chi group, many benefits in cognitive function, memory, and emotion were observed after healthy older adults receiving different types of exercise interventions. Increased activation during the task (i.e., switch task and flanker task) were found in PFC, left superior frontal, bilateral cerebellum, and right posterior cingulate cortex after Tai Chi practice, suggesting that it can improve inhibitory control ability and emotion (Wu et al., 2018; Yang et al., 2019; Liu et al., 2020). Similarly, changes in regional homogeneity (ReHo), amplitude of low-frequency fluctuations (fALFF) were observed in the left medial temporal lobe, para hippocampus, left fusiform gyrus, and dorsolateral prefrontal cortex (DLPFC), and it was related to improvement of memory (Tao et al., 2017b; Mei et al., 2019; Yue et al., 2020a). Increased functional connectivity between the bilateral hippocampus and medial PFC substantiated this result (Tao et al., 2016). However, some studies reported that the functional connectivity between DLPFC and left superior frontal gyrus, DLPFC and middle frontal gyrus was decreased, implying that a negative relationship between emotion regulation and functional connectivity (Tao et al., 2017a; Liu et al., 2018). Both studies showed that Tai Chi contributed to enhanced brain activity in correlation to improved memory, emotion, and cognitive functions.

Four studies examined the change of brain activity in healthy older adults throughout the treadmill exercise from several sides. The brain electric activity—event-related potential (ERP) including N2 and P3, were shortened on the latency after exercise intervention (Chuang et al., 2015). Furthermore, one study identified an increase in the functional connectivity between the frontal and parietal regions, the posterior hippocampi, and regions within the left cuneus and left precuneus, whereas reduced activation which is related to semantic memory was observed in another study (Chirles et al., 2017; Won et al., 2021). The results of the three studies provided the evidence of treadmill exercise-induced benefits in improving cognitive performance and memory.

The effects of dancing exercise on brain activity in healthy older adults were showed in six studies. The functional connectivity between brain regions and the latency of N2 and P3 were utilized to assess the brain activity for healthy older adults after dancing training. The findings revealed that N2 and P3 latency were shortened (Smith et al., 2013) and the functional connectivity between insulo-opercular and right frontoparietal control networks, visual and language/DMN networks were increased, confirming the benefits of dancing exercise in the improvement of cognitive function (Chuang et al., 2015; Balazova et al., 2021). Eggenberger et al. (2016) investigated the oxygenation of older adults during walking. The participants showed reduced oxygenation during the acceleration of walking in PFC throughout the training. This study suggested that the exercise training induced the change of PFC oxygenation correlated with the executive functions to improve the mobility and help in prevention. Ji et al. (2018) analyzed the involvement of the brain region during memory tasks by using the fMRI data, and it observed that the involvement in motor cortices and the cerebellum during the task was increased during post-training. This study found that the dancing exercise can improve gait speed and cognitive function by increasing the involvement of motor-related networks.

3.5 Key findings of people with PD

Table 6 summarizes the key findings and conclusions of each study about people with PD. In the treadmill-training group, motor ability is the core index that researchers care about. Maidan et al. (2018) investigated the change in cortex activation during walking after treadmill practice and found a reduced activation in the prefrontal area compared to the baseline, suggesting that the pattern of cortex activation in PFC can be altered by treadmill training to reduce fall risk. The mean frequency (MF) and α, β belonged to the brain’s electric activity were used to study effects of exercise intervention on the brain activity in people with PD. Two studies showed that MF was higher in the left cerebral area and significant changes in α, β within the frontal and centroparietal electrodes were also observed, which might be associated with the improvement of physical ability and gait (Carvalho et al., 2015; Calabro et al., 2019). Additionally, increased activation in Brodmann area 10, inferior frontal gyrus, and functional connectivity in executive control network were observed after training, whereas the activation in the left cerebellum, middle temporal gyrus, and the functional connectivity in sensory-motor network (SMN) were decreased (Maidan et al., 2017; Droby et al., 2020). The findings of these two studies suggested that treadmill exercise may reduce the reliance on the frontal region and enhance the neural plasticity to improve gait and reduce falls. Enhanced brain activity is the evidence of improvement of motor ability throughout treadmill training.

4 Discussion

To the best of our knowledge, this study is the first to cohesively present the effects of three training modalities on brain activity of healthy older adults and people with PD. Our systematic review of the literature found limited robust evidence for the effects of exercise on the brain activity of older adults and people with PD. Of all the trials included in our review, the objectives, and protocols of study are not comprehensive enough to definitely compare the differences between healthy older adults and people with PD after treadmill-training intervention. Therefore, while our systematic review showed that the improvement of cognitive function, memory, and emotion might be associated with modified brain activity, functional connectivity in healthy older adults through Tai Chi, treadmill training, and dancing, and revealed that treadmill exercise may improve the motor ability of people with PD by changing brain activity, it remained largely unknown if the difference was true.

In the group of healthy older adults, most studies included all exercise interventions (Tai Chi, treadmill training, and dancing) found that exercise can affect brain activity and functional connectivity to improve cognitive function, memory, or emotion, despite variability in types and dosages of the intervention used. An explanation for this could derive from their respective objectives and study protocols, 11 of the 24 studies utilized the cognitive or memory tasks in the experiment (such as N-back, flanker task, etc.), especially two of which were included in the treadmill exercise group (Smith et al., 2013; Chuang et al., 2015). Motor tasks, however, have yet to be incorporated into the study of the exercise intervention in healthy older adults.

In comparison to cognitive task in the healthy older adults group, of the five trials in group of people with PD, there were three trials including the motor task during the data collecting (i.e., walking, imaged walking) (Maidan et al., 2017; Maidan et al., 2018; Calabro et al., 2019). Therefore, we speculated that inconsistencies between oddball paradigms might lead to different performances between healthy older adults and patients with PD throughout treadmill training.

Only four studies from the group of healthy older adults and people with PD did not use the oddball paradigm during the data recording through treadmill training. Droby et al. (2020) found that an inverse change trend (such as increased or decreased) in functional connectivity between different brain regions was observed in people with PD after treadmill practice. This finding is consistent with previous studies which reported reduced hemispheric asymmetry in movement patterns due to age-related deficits in neural connectivity (Cabeza, 2002; Przybyla et al., 2011). Interestingly, there were two studies in healthy older adults suggesting an increased functional connectivity between some regions at post-training (Chirles et al., 2017; Won et al., 2021). The difference in change of functional connectivity was observed between three studies. To provide some explanations, three trials did not differ in the baseline demographic characteristics including age, education, sex, and the number of participants in the expected type of population. Three studies adopted the comparison between pre- and post-training within the treadmill training group or the healthy older adults group. Furthermore, the participants in a study by Chirles and Won underwent a 12-week treadmill training intervention including four sessions per week, while the duration of study by Droby was half of that amount of time including three sessions per week. Therefore, the inconsistency in the type of population and the intervention duration provided a sound reason for the disparate results.

In light of our findings about people with PD, we speculated the following. The study reported that cortical activity abnormally increases during walking in people with PD, and it might reflect a cortical compensation phenomenon (Stuart et al., 2018). Decreased cortical activation after training suggests that gait training improves the automaticity of walking and provides more stimuli, which in turn lowers the reliance on cognitive resources and a reflection of better utilization for motor networks during walking or during a task in patients with PD. This was similar to that found in people with PD (Maidan et al., 2016). As indicated from animal and human models, exercise can, to some degree, enhance neuroplasticity that promotes angiogenesis (growth of new blood vessels), neurogenesis (new functional neurons), and synaptogenesis (new synapses). All the processes are consistent with our findings, which reported that functional connectivity was increased (Bherer et al., 2013). Additionally, externally guided rhythmic movements may also account for the augmentation of these changes in PD participants (Rochester et al., 2005; Yogev et al., 2005; Herman et al., 2007; Maidan et al., 2017). Therefore, treadmill training might provide an external setting conducive to improving the gait in PD.

The use of measurement devices included fMRI and EEG presents a limitation in the current exercise intervention literature studies. In comparison to the fNIRS detection which allows moderate physical activity, fMRI and EEG require participants to possibly maintain a resting state. Even small motions may produce artifacts and noise during scanning (Power et al., 2012; Satterthwaite et al., 2012; Lin et al., 2020), affecting the final data analysis and results. Furthermore, most studies utilized the EEG and fMRI and adopted some tasks related to cognitive, memory, and inhibitory control. The type of task might be related to the limitation of EEG or fMRI. To explore the motor ability-related knowledge in people with PD, more feasible motor tasks should be developed and employed for fNIRS scanning.

The average score of PEDro in this review was 5.52, which suggested that the studies included were of moderate methodological quality (Moseley et al., 2002). A lack of some factors included random allocation, double blinding, and intention-to-treat analysis can be regarded as limitations of the methodology of all trials in this review. Furthermore, non-English studies, MRI-related articles were excluded and only three kinds of exercises were included here, which illustrate other limitations in this review. Additionally, only five of the studies and one exercise intervention (treadmill training) included targeted people with PD. Resultantly, our findings may not be representative in people with PD. There is a need for more robust and comprehensive studies on the exercise intervention for people with PD. For example, motor tasks are employed into the study of healthy older adults throughout the exercise, and more studies of people with PD adopt cognitive tasks during fNIRS, EEG, and fMRI scanning.

5 Conclusion

Our systematic review demonstrated that three terms of exercises (Tai Chi, treadmill training, and dancing) can modify brain activity, functional connectivity to improve cognitive function, memory, and emotion in healthy older adults, and treadmill exercise can improve the motor ability of people with PD, which was related to changes in the brain activity. However, with the current available studies, the differences of brain activity and performance between healthy older adults and patients with PD cannot be sufficiently confirmed in this review. In the future, more randomized controlled trials (RCTs) including cognitive and motor tasks are needed to provide the evidence on the effect of exercise intervention on brain activity in healthy older adults and people with PD. Furthermore, applying fNIRS to these RCTs is worth investigating, which reduces the effect of noise and allows researchers to explore the motor ability of people with PD and healthy older adults.

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