The Effects of Anodal tDCS Combined with a Selected Balance Exercise Program on Balance Performance and Working Memory in Older Adults

Abstract

Background

Transcranial direct current stimulation (tDCS) has recently drawn attention as an inexpensive, painless, safe, and effective technique to improve motor performance and cognitive function in older adults. This quasi-experimentstudy examined the effects of a selected balance exercise combined with anodal tDCS on balance performance in older adults.

Methods

Twenty-four older adults (Mean age M±SD= 69.79±5.50) participated in this study. The participants were randomly assigned into a real tDCS or sham tDCS groups. The participants in the real tDCS group received 2 mA anodal tDCS over the left primary motor cortex (M1) for 20 min. The participants performed a selected balance exercise program for 50 min following tDCS. Training was conducted 2 sessions per week for 8 weeks (16 sessions). Berg balance scale (BBS), timed up and go test (TUG) and working memory test (2-back task) were measured before (baseline), after 8 weeks of the training, and 4 weeks of follow-up.

Results

Compared to sham tDCS group, BBS and TUG were significantly improved in real tDCS group after the training and 4 weeks of follow-up, however, this intervention could not effect of working memory.

Conclusions

In sum, these results indicate that the selected balance exercise program combined with anodal tDCS can improve balance performance but not working memory in older adults.

1. Introduction

Lower extremity functional ability involves basic tasks that are essential in carrying out daily activities and includes walking, lower extremity strength, balance, and postural control [1]. There exist several sets of evidence indicating that aging is associated with reduced lower extremity functional ability reflected in reduced muscle performance [2], reduced strength [3], loss of motor coordination [4], and poor balance and walking [5]. In other words, deteriorated balance performance and lower extremity functions are among the issues related to lower quality of life for the elderly which sometimes may even lead to falls or other motor problems [6, 7].

In the process of aging, the brain’s overall size naturally begins to shrink [8] with age-related changes developing in different areas of the motor cortex. These changes are said to be associated with reduced motor control, impaired walking performance, and poor balance [4]. One area of the brain cortex that plays an essential role in proper activation of muscles and controlling voluntary movements [9] is the primary motor area (M1) [10]. Previous studies offered evidence suggesting that M1 importantly contributes to some aspects of lower extremity functions. Some have shown that during the gait cycle, M1 communicates with the subcortical region (responsible for gait control) [ 11] as well as the supplementary motor area (SMA) that contributes to motor control [12]. M1 also influences balance and gait control [13] and lower extremity strength [14].

Given the growing number of aging populations in developed as well as developing countries [14], it is essential to establish safe, inexpensive interventions and exercise methods to enhance lower extremity functional ability, balance performance, and cognitive performance among the elderly [15].

Transcranial direct current stimulation (tDCS) has recently drawn attention as an inexpensive, painless, safe, and effective technique in improving cognitive and motor performance [15, 16]. tDCS is a neuromodulatory technique that results in cortical excitation without generating active potential. It can modulate the resting membrane potential, thereby modulating action potential of neurons [15]. The technique involves using a weak electrical current applied on the scalp through two electrodes with the intention to manipulate certain regions of the brain. It works on ion homeostasis inside and outside the membrane, stimulating shifts in the resting membrane threshold [17].

Anodal current enhances cortical excitability and depolarizes cell membranes while cathodal current decreases cortical excitability and hyperpolarize cell membranes [18]. Based in this, it is generally assumed that tDCS can enhance and preserve the effects of various physical and cognitive exercises on performance capacity in individuals [16]. These positive effects were first reported in the human motor cortex [19]; however, later studies demonstrated the same positive effects on other cortical regions including the visual cortex [20], the sensorimotor cortex [21], the prefrontal cortex [17], and the cerebral cortex [22].

For example, a session of anodal tDCS (a-tDCS) on M1 was reported to enhance upper extremity functional ability in the elderly [23]. Similar findings were reported by other studies [24, 25, 26]. However, to the best of our knowledge, few studies have examined how a-tDCS on M1 can influence lower extremity functional ability in the healthy elderly. For example, Craig & Doumas [27] examined how tDCS on the celebellum as well as M1 can influence postural control in adults and the elderly. Their findings indicated a minimal effect of tDCS on postural control in the eyes-open condition. In another study on the elderly, [5] reported similar positive results. Therefore, a-tDCS seems to be a promising technique to enhance lower extremity functional ability.

In addition, aging leads to changes in all systems of the body. Moreover, morphological and biochemical changes in different areas of the brain, such as frontal and parietal cortices, reduce cognitive capacity while causing changes to appear in the musculoskeletal system [28]. An investigation of neuroimaging indicates how working memory functions in the brain. The prefrontal region, particularly the dorsolateral prefrontal cortex, was cited as a major area involved in working memory processes and defects [29]. Furthermore, a study of neuroimaging results has shown that the right inferior frontal gyrus is activated during inhibitory control activities [29]. Thus, tDCS techniques that monitor and regulate activities of the dorsolateral prefrontal cortex (DLPFC) are capable of improving working memory as well as balance performance [17].

Furthermore, many studies with promising results have examined effectiveness of noninvasive direct current stimulation of the brain (30). These effects may vary depending on electrode placement, their polarity, and current intensity. Studies about effects of electrical cortical stimulation on cognitive functions produced mixed results. For example, Andrews et al., [31] examined the link between cognitive activity and anodal stimulation of the DLPFC to improve working memory in ten participants with the age of 20–51 years. Their findings indicated improved working memory function as a result of controlled stimulation combined with an n-back task.

However, while some studies reported favorable impact of this training technique on working memory as well as motor performance in children [32], adults [33, 34, 35], and the elderly [36, 37], the results in this area are still inconsistent and others [38, 39, 40] failed to demonstrate positive effects of tDCS on cognitive and motor performance. For example, Kiminski et al [39] showed that a single session of anodal tDCS in the M1 region could not improve balance performance in the elderly. It seems, one possibility is that the degree of difficulty in postural balance control tasks leads to different results. Previous studies investigated tDCS effects on postural balance control during static standing with open or closed eyes, open or closed legs, and stable or movable platform [35, 36, 41, 42]. Additionally, most studies have focused on the immediate effects of tDCS on postural balance control, but one paper reported that the 10 sessions of anodal tDCS (2 mA) over M1 and physical therapy training improve ankle control and balance in stroke patients [43]. Therefore, the repeated anodal tDCS over M1 and balance exercise program may improve balance performance [43, 44]. However, to the best of our knowledge, no study has examined whether repeated anodal tDCS over M1 and balance exercise program improves balance performance and working memory in elderly persons. Therefore, the present study aims to examine the effects of a 16-session balance exercise program combined with a-tDCS in M1 on motor and cognitive performance among the elderly. Accordingly, it is hypothesized that a 16-session balance exercise program combined with a-tDCS in M1, improves the balance performance of the elderly immediately after the exercise sessions and also one month after the end of the training. It is also hypothesized that this mentioned exercise program can also improve the working memory of the elderly.

2. Materials And Methods

3. Results

Table 2 presents the results for analysis the demographic data as well as the study variables in the initial stage (pretest). As seen in this table, the sham and the intervention (tDCS) groups had similar results on all demographic indices and test variables except for BBS. All participants successfully completed training for 8 weeks. There were no reports of adverse events due to the training or tDCS.

4. Discussion

Several studies have examined effects of tDCS as a noninvasive technique on balance and postural control in the elderly [55]. Since these effects vary depending on a number of factors including where stimulation is applied in the brain [56], number of training sessions [57], and intensity of the current applied [58], it is difficult to make a general conclusion about the extent to which tDCS can influence balance and postural control, and thus further studies are needed in this area.

To extend the previous studies and shed more light on their findings, the present study examined the effects of balance exercise combined with tDCS on balance performance and working memory in the elderly. We hypothesized that participation in balance exercise + tDCS sessions can positively influence working memory and balance performance in the elderly compared to a sham group. Our findings showed that 16 sessions of balance exercise combined with anodal tDCS on M1 in the left hemisphere of the brain of the physically unimpaired elderly can improve balance performance immediately following the intervention and even one month after the intervention is finished. However, the findings failed to demonstrate positive effects of tDCS + balance exercise on working memory in the elderly.

Since the intervention group outperformed the sham group in terms of balance performance, our findings are largely consistent with major previous studies in this area [5, 18, 33, 34, 36, 37, 59, 60]. For example, Costa et al. [18] showed that an exercise program combined with tDCS can positively influence performance capacity of the elderly participants 24 hours following the intervention or even 30 days after the intervention is complete. In another study, Fujiyama et al. [60] observed significant improvements in motor skills associated with the upper limbs in the elderly who carried out isometric strength training and received tDCS compared to the control group.

In the present study, we examined balance using two common methods: Berg Balance Scale (BBS) and timed up-and-go test (TUG). Similar results were reported in the literature using BBS. For example, Ehasni et al. [59] showed that a tDCS-based training session applied to the cerebral cortex can improve balance performance in the elderly. A major difference between our study and Ehsani et al. [59] consist in the stimulated region in addition to the number of sessions. Here, we examined how 16 tDCS sessions combined with balance exercise influenced balance while Ehsani et al. [59] only used one session. Therefore, our findings present a set of more reliable results.

Anodal tDCS-based training can cause shifts in neurotransmitters of this region by increasing local concentration of glutamate and glutamine where tDCS is applied, thereby enhancing brain activity which, in turn, can eventually improve motor performance [2]. In addition, experimental evidence has shown that anodal tDCS can improve motor performance and learning by increasing excitability of the motor cortex, leading to amplified stimulation and engaging a greater number of motor units [61].

In other words, when excitability of M1 region in the primary motor cortex is increased through tDCS interventions, it is possible that supraspinal fatigue is delayed due to increased M1 output and downward shifts, and this in turn could enhance motor performance [19]. Furthermore, tDCS can influence the activity of the insular cortex, thereby reducing rate of perceived exertion (RPE) in participants. This can also improve motor performance in individuals [62]. Moreover, anodal tDCS can also amplify active muscle outputs by increasing M1 excitability, facilitating supraspinal stimulation, and reducing inhibitory feedback in M1 [63, 64]. Although we did not measure the motor cortex excitability in the current research, it can be said presumably that following 16 sessions of balance exercise combined with 20 minutes of unilateral a-tDCS on M1, the participants in the present study experienced higher motor excitability and engaged in a greater number of motor units in balance tests to outperform the sham group. This improved balance performance may also be caused by reduced number of inhibitory feedbacks in M1. Based on the studies described above, improved balance performance in the tDCS group can be attributed to increased activity of the insular cortex and lower levels of perceived exertion during training sessions. However, one limitation of our study that future studies should address is that we did not record this perceived exertion using standard checklists during training sessions. Another limitation of the current research was the use of clinical tests such as the Berg balance test to measure balance performance. Some researchers have shown that Berg balance test is not a suitable test for predicting falls in the older adults [65, 66]. Therefore, it is suggested that future researches use more accurate and reliable tools such as the force plate to measure balance performance.

In line with some previous research [67] our findings failed to indicate tDCS effects on working memory, although there are reports of these effects in the existing literature. For example, Berryhill & Jones [68] showed that three a-tDCS training sessions on the left and right premotor cortices (F3 and F4) can improve working memory in the elderly with higher levels of academic educations although they found no improvement in the elderly with lower education levels. Ineffectiveness of tDCS in improving our participants’ working memory may be associated with the fact that they had low levels of academic education.

On the other hand, studies that demonstrated positive effects of tDCS on working memory [31, 69] assumed that tDCS enhances excitability in the outer anterior prefrontal cortex, probably due to increased levels of glutamate, an amino acid associated with working memory, recognition, and learning how to respond to a stimulus [70]. Another probable reason behind ineffectiveness of tDCS in improving working memory of our participants is the fact that the outer anterior prefrontal cortex was not stimulated here. Thus, future studies can re-examine these effects by including the factors noted above.

In our study, the active electrode was placed on M1 in the left hemisphere of the brain to examine effects of unilateral tDCS. The technique was similar to those reported in the literature [71, 72]. The left hemisphere appears to play a more important role in motor control and balance performance [73]. However, it is recommended that future studies should examine the other hemisphere as well or examine how bilateral tDCS influences balance performance and working memory. We applied 2mA anodal tDCS, but since the outcome may vary depending on current and type of stimulation (anodal vs. cathodal) [55], future studies may examine tDCS effects by manipulating these two variables. Of the different cognitive functions associated with motor performance, we only examined working memory using the n-back task. Therefore, we recommend future studies to assess working memory using other available standard tests while noting other cognitive functions such as selective attention and cognitive flexibility. As we only examined the elderly, our findings cannot be generalized to other age groups including adults, children, or the middle-aged. Thus, further studies can be conducted to examine the effects of unilateral a-tDCS in M1 on balance performance and other cognitive functions in adults, children, or the middle-aged. Nevertheless, our findings indicated that the effect of the within-group was significant, it can be concluded that sixteen sessions of balance exercises, regardless of the presence or absence of tDCS, had a positive effect on improving working memory. These results are in line with the findings in this field that have shown physical exercise, especially balance practice improve elderly’s working memory [74, 75]. For example, Azhdar et al [74] showed that a balance exercises intervention can increase cognitive performance and especially working memory in the elderly. In the present research, both the intervention and sham groups were able to increase the working memory of the elderly, since the balance exercise was applied to the same extent in both groups, so it can be concluded that the balance exercises has been able to improve the cognitive function and especially the working memory of the elderly. Of course, since in the current study, we did not have a control group (a group that does not have balance exercise), so this conclusion should be used with caution and it is suggested that future studies add a control group to the research for more clarification. In addition, the present study used balance exercises, where the authors suppressed a single sensory pathway, such as the visual. However, a specific balance program should mix multiple sensory pathways such as the visual, vestibular, and somatosensory systems. Further studies are warranted to investigate which type of balance training is most effective to improve balance when combined with anodal tDCS.

5. Conclusions

In summary, our findings indicated that physically unimpaired elderly can improve their balance performance compared to a sham group by attending 16 sessions of balance exercise based on unilateral a-tDCS applied to M1. Although the intervention group did not outperform the sham group in terms of working memory, it seems that tDCS can be used as a safe, useful, noninvasive technique to enhance balance and assist the elderly to walk better and reduce their falls. Therefore, it is recommended that trainers and coaches working with senior citizens should use this safe, inexpensive, and effective technique more frequently.

Declarations

Ethics approval and consent to participate

Before the start of this study, informed consent was obtained from all participants. This study was approved by the Shahid Chamran University Ethics Committee (EE/1400.2.24.32886/scu.ac.ir; 26/10/2021). All methods were carried out in accordance with relevant guidelines and regulations. 

Consent for publication

Not applicable. No individual or indemnifiable data is being published as part of this manuscript. 

Availability of data and materials

The datasets generated and analyzed during the current study are not publicly available due to ethical restrictions, however, they are available from the corresponding author on reasonable request.

Competing interests

The authors declare that the present study was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding

This research received no external funding.

Authors' contributions

Conceptualization, M. M and E.S; methodology, E.S software, ES; validation, M. M, E.S and M.D.; formal analysis, M.M; investigation, E.S.; resources, M.M; data curation, M. M, E.S and M.D; writing—original draft preparation, E.S and T. Y; writing—review and editing, M. M and E.S. visualization, E.S and T. Y; supervision, M.M and E. S; project administration. All authors have read and agreed to the published version of the manuscript. 

Acknowledgements

The authors would like to thank all participants for their participation in this study. 

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