Ⅰ. Introduction
Transcranial direct current stimulation (tDCS), a promising therapeutic modality that stimulates cortical excitability by applying low intensity stimulation to scalp surface, has been demonstrated its safety and effectiveness (Gandiga. P.C., 2006;Iyer. M.B., 2005). Specifically, recently in tDCS studies, they found that non-invasive brain stimulation using magnetic field or direct electrical current changed both cognitive and motor functions (Dockery C.A. et al., 2009;Nitsche. M.A., 2003;Fregni. F., 2005;Flöel, A., 2014;Matsumoto. J., 2010). On the basis of the above- mentioned previous evidences, tDCS has been used clinically for patients with neurological symptoms such as stroke or poliomyelitis that showed positive effects on the daily motor performances (Acler M. et al., 2013;McCambridge A. B., Stinear J. W. & Byblow W. D., 2017)
Across a variety of motor performances in daily activities, reaching performance is a frequently and unconsciously performed function (van Meulen, F.B., 2011), although this requires complex interactions between the nervous and musculoskeletal systems. (Maynard E.M. et al, 1999). Especially, for the goal-directed reaching is performed accurately in time, proper motor coordination with the normal onset timing of individual muscle activations is prerequisite (Bernsetin N.A., 1996) and, in decades, the work of muscle coordination during a specific performance has been investigated by using electromyography (EMG).
In both brain and tDCS research areas, primary motor cortex, which called M1 has been considered importantly to investigate (Lemon R.N., 1993) because even a single neuron of M1 could make joint reaction (Donoghue J.P,, 1992;McKiernan B.J., 1998;Park M.C., 2001). For producing the well-coordinated reaching performance, firstly, M1 involved in encoding the motor output signal and then spinal circuit involved in proprioceptive feedback, modulating the movement error during the hands was moving within space. (Cheng, E.J. & Scott, S.H. 2000). Together with this basic control mechanisms in the central nervous system, motor neurons in peripheral nervous system is worked that, for examples, agonist activities propel hands toward goals and antagonist activities slow down to stop the performance at a target site. (Flanders M. et al. 1994;Marsden C.D. et al. 1983;Wierzbicka M.M. et al. 1986).
On basis of the physiological mechanisms mentioned above, several tDCS studies have already demonstrated that it could facilitate or inhibit cortical excitability of M1 (Nicolas M.A. et al., 2005), which result in the change in motor performance and learning (Vines B.W., 2008;Arias, P., 2016). According to Arias, P. et al. (2016), tDCS over M1 could change the time between the response-signal and the onset of muscle activation defined as the premotor time. However, to the best of our knowledge, there is still lack of physiological evidences to establish the effects of tDCS on the simultaneous activities of multiple muscles, involved in motor performance. Also, these physiological evidences would contribute to sports rehabilitation area by supporting the feasibility of tDCS for training to improve in athlete’s performances.
Therefore, the aim of this study is to discover the effects of tDCS on the onset of the functional muscles’ activities during forward reaching tasks. We hypothesized that bilateral tDCS (anode current over right M1 and cathode current over left M1) would affect the onset during the beyond arm-length and the within arm-length reaching tasks. Especially, considering the above-mentioned physiological evidences, the onset time would be faster after the 2mA stimulation session.
Ⅱ. Methods
1. Participants
15 healthy males (24.2 ± 1.55 yrs) was recruited at the Korea University. They were all right-handed as dominant hand. They had no history of neurological and orthopedic diseases. Before all experiments start, participants filled out consent form that explain the experiment procedures and Information about tDCS. if participants used any medication that could affect the central nervous system, they were excluded from the study. The study protocol was approved by the Institutional Review Board of Korea University (KU-IRB-16-146-A-2).
2. Transcrainal direct current stimulation (tDCS)
The battery-driven, constant current stimulator (Y-Brain Inc, Korea) was used to apply the direct current of 2mA intensity during all experiments. The placement of two-saline sponge electrodes (5cm2) were placed on right primary motor cortex (M1) with anodal current and left M1 with cathodal current which called C3, C4 in accordance with 10-20 EEG system (Klem GH, LuÈders HO, Jasper HH & Elger C., 1999). A total of two experimental sessions were performed. In first session, one of sham or 2mA were induced during 20 minutes randomly, then after more than four days for wash-out period, second session were performed with the current type not used in the first session. During all experimenters, subjects were blind to intensity and the current type.
3. Task
To minimize the ceiling effects by handedness, which was trained for each participant’s lifetime, the tasks were performed with non-dominant hand (Vines B.W., 2008). Forward reaching (FR) were performed in a total of 3 blocks. Each blocks consisted of 10 trials, which containing 3 FR beyond arm length, 3 FR within arm length, 3 meaningless FR, 1 catch trial. The sequence of trials was randomized. Participants were seated on a chair facing a television screen. Three custom-made switch buttons were positioned on the table that are approximately 20cm away from the chair. First button was positioned for FR beyond arm length (120% of arm length). Second button was positioned for FR within arm legnth (80% of arm length). Third button was positioned in straight line with home position for meaningless FR, which meant not for analysis in this study but only for the level of task difficulty. On the television screen, Three circles, indicating each buttons were shown to participants. Participants was instructed that if a trial starts, 0.5ms-1.5ms after warning sound, one of three buttons were lighted as response signal, then they should reach and press the corresponding button as fast as possible with non-dominant hand from the home position. Of 10 trials, 1 catch trial were inserted in which the response signal did not appear after the warning cue for identifying the participant’s real respond. There are 10 seconds of rest time between each blocks. Before the trial were executed, we provided enough time (about 5 min) to practice for reducing the learning effect. All FR task was evaluated in four periods; 1) before the tDCS application (baseline), 2) during the tDCS application (10min after the start of tDCS application) 3) immediate after ending the tDCS application and 4) 20 min after removing the tDCS electrodes.
4. Surface electromyography(sEMG)
sEMG signals were collected a rate of 1500 Hz from the muscle bellies of anterior deltoid (AD) as shoulder flexor, posterior deltoid (PD) as shoulder extensor, biceps brachii (BB) as elbow flexor, lateral triceps (Tri) as elbow extensor, pectoralis major (Pec) as shoulder internal rotator and infraspinatus (IS) as shoulder external rotator in accordance with SENIAM recommendation by using sEMG sensors (Noraxon Inc, USA). To prevent the impedance between skin and electrodes, we always cleaned the skin surface with alcohol. Raw EMG data was high-pass filtered at 20Hz (six-order Butterworth filter), then, demeaned, rectified, and low-pass filtered at 50 Hz (six-order Butterworth filter).
The EMG onset of each muscles was determined at the mean of the consecutive 75 samples amplitude above the EMG-background activity plus three standard deviation. The EMG-background was calculated in the time-window 100ms prior to the responde signal. Customized MatLab programmes (The Mathworks, Ltd) were used for calcuation.
5. Adverse effect
After each experiments ended, participants were asked if there are any adverse effects such as dizziness or nausea. Stimulation intensity they felt when applying tDCS was checked by visual analog scale range from 0 to 10.
6. Statistical analysis
After testing normality of data by Shapiro Wilk test, one-way repeated measures ANOVA was used for identifying the significant changes of muscle onset time after the application of two different current types (2mA or Sham) in six muscles (AD, PD, BB, Tri, PEC and IS) according to each four evaluation stages (before the tDCS application, during the tDCS application, immediate after removing the tDCS application and 20 min after removing the tDCS). p value of 0.05 was set to be significant. statistical analysis was performed by SPSS version 20 (SPSS Inc., USA).
Ⅲ. Results
1. Demographic data
Anthropometrics was measured prior to the reaching task evaluation. Furthermore, they were asked to avoid caffeine (＞3hr) and alcohol consumption (＞24hrs). They should have enough sleep time and avoid excessive exercise that cause the muscle fatigue to affect the muscle activation (Table 1)
2. Effects of active/sham tDCS on the EMG onset during reaching task
Table 2 shows the mean of the EMG onset in reaching to target within arm length which measured at each time conditions. Table 3 showed the same variable in reaching to target beyond arm length which measured at each time conditions.
1) Changes in the onset of muscle activities during within arm-length reaching task
For within arm-length reaching task, as figure 1, sham application showed significant decrease in three muscles; BB (p=0.036), Tri (p=0.003), Pec (p=0.22) in during-tDCS period. In 2mA application, AD (respectively, p=0.006; p＜0.001; p=0.002), PD (respectively, p=0.001; p＜0.001; p＜0.001), BB (respectively, p=0.009; p＜0.001; p=0.017) and IS (respectively, p=0.001; p＜0.001; p=0.005) were decreased significantly in during-tDCS, immediate- after-tDCS and 20minafter- tDCS periods compared to baseline. Pec showed significant decreases only in 20min-after-tDCS periods (p=0.001) compared to baseline.
2) Changes in the onset of muscle activities during beyond arm-length reaching task
For beyond arm-length reaching task, as figure 2, sham application showed no change of onset time of all muscles in all periods after tDCS compared to baseline. 2mA application showed AD (respectively, p=0.006; p＜0.001; p=0.002) PD (respectively, p=0.001; p＜0.001; p＜0.001), BB (respectively, p=0.009; p＜0.001; p=0.017) and IS (respectively, p=0.011; p＜0.001; p=0.005) showed significant decreases of onset in all periods after tDCS compared to baseline. The onset of Tri showed a significant decrease in immediate-after-tDCS and 20min-after-tDCS periods. For Pec, a significant change of onset were shown only in 20min-after-tDCS period compared to baseline.
3. Adverse effect
There are no adverse effects during or after tDCS application.
Ⅳ. Discussion
The aim of our study is to investigate the effects of tDCS over M1 on the onset of functional muscles’ activities during the reaching task. Although many tDCS studies have already reported the effects of tDCS on cortical excitability and motor performance during functional tasks, there are still lack of physiological evidences that would explain the underlying changes in terms of motor units. Also, we used two different task conditions (i.e. within and beyond arm-length reaching) to determine whether tDCS would provide the consistent effects of tDCS over M1 on muscle activities regardless task types.
As our results were shown, the significant decreases of onset in functional muscles during performing both within-arm-length and beyond-arm-length reaching were observed in all periods after tDCS compared to baseline (Figure 1,2). These findings were line with ones of previous studies which reported that anodal tDCS over M1 could enhance motor learning and skills in healthy adults during visuomotor adaptation task and serial reaction (Kantak S.S. et al., 2012). Also, the present study agreed with other previous reports to demonstrate that anodal tDCS facilitates cortical excitability which result in faster activations in functional upper limb muscles (Moura, R. C. F et al., 2017).
In addition, as bilateral tDCS montage used in our study, a previous tDCS study which used the bilateral tDCS application montage reported that bilateral tDCS reduced significantly premotor time during reaching task while there was no changes in reaction time and motor time (Arias, P. et al., 2016). Especially, they reported a significant increase in premotor time of triceps brachii muscle activity, explaining that the increase in premotor time would indicated a response by muscle fatigue. Our result also showed a similar trend in sham stimulation session, especially, in beyond arm-length task condition. Whereas, in 2mA stimulation session, most of muscles’ activity showed significant decreases in its onset time with no increasing trend.
For significant decreases in the onset of few muscles such as biceps brachii, triceps brachii and pectoralis major muscles during reaching performance in sham stimulation session, we speculated the placebo effect by which participants attempted to perform rapidly with anticipation to the next response signal. Therefore, future studies need to consider this sham effect of tDCS on EMG signals.
Although we did not observe the kinematic data such as reaching speed, our findings proposed that bilateral tDCS would change the excitability of motor units that lead to the change in motor strategy such as muscle synergy patterns for functional movements. Furthermore, the changes in muscle’s onset timing were reported to indicate the prerequisite for the changes in motor performance (Saito H., Yamanaka M., Kasahara S. & Fukushima J, 2014). Therefore, based on our findings, future studies to investigate the effects of tDCS on the motor strategy and motor performance is necessary.
In conclusion, our current study demonstrated that tDCS facilitate the onset of muscle activity during reaching performance regardless to target distances. We expected that our findings would contribute to the decision making for training strategy of sports rehabilitation area to improve in athlete’s motor performance.
Study Limitation
The primary limitation of our study is the small sample size and subjects’ age. Another limitation is the sex of participants for minimizing sex-specific differences in motor control ability. For these limitations, we can not generalize these results to all human. Therefore, future studies with large sample size with wide age group is needed for providing strong evidence.
