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Corticospinal excitability following repetitive voluntary movement
Journal of Clinical Neuroscience xxx (2018) xxx–xxx
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Experimental study
Corticospinal excitability following repetitive voluntary movement Natsumi Ishikawa a, Ryunosuke Miyao a, Shota Tsuiki b,c, Ryoki Sasaki b,c, Shota Miyaguchi c,⇑, Hideaki Onishi c a
Department of Physical Therapy, Niigata University of Health and Welfare, Japan Graduate School, Niigata University of Health and Welfare, Japan c Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Japan b
a r t i c l e
i n f o
Article history: Received 9 April 2018 Accepted 12 August 2018 Available online xxxx
a b s t r a c t Post-exercise cortical depression (PED) is induced by non-fatiguing finger movement. Because the type of exercise that causes PED remains unclear, we conducted two experiments to clarify which exercise factors induce PED. Fifteen healthy participants performed repetitive abduction movements of the right index finger at 2.0 Hz (simple rhythmic task) and 0.2 Hz (adjustment task) for 6 min each in experiment 1. Twelve healthy participants performed repetitive and isometric abduction contractions of the right index finger at 1.0 Hz with visuomotor tracking (visuomotor task) and without visuomotor tracking (simple isometric task) for 5 min each in experiment 2. Muscle contraction levels were 10% of the maximum voluntary contraction in all tasks. Motor evoked potentials (MEPs) evoked by transcranial magnetic stimulation were recorded from the right first dorsal interosseous muscle before and after the movement tasks. The simple rhythmic task transiently reduced MEP amplitudes when compared with baseline in experiment 1. In contrast, the visuomotor task increased MEP amplitudes in experiment 2. No MEP changes were observed following the adjustment task in experiment 1 and the simple isometric task in experiment 2. This study suggests that PED is induced by simple rhythmic movement. Ó 2018 Published by Elsevier Ltd.
1. Introduction The excitability of the corticospinal tract decreases after repetitive non-fatiguing movements. This phenomenon has been defined as post-exercise cortical depression (PED) [3,4]. PED is likely caused by a reduction in primary motor cortex (M1) excitability because the F wave, which is used as the index of spinal excitability, does not change [4,23], and the short-interval intracortical inhibition (SICI), which is used as the index of inhibitory circuits in the cortex, is increased [20,22]. Moreover, PED is modulated by changes in movement factors, such as levels [14], types [14] and frequency [2,22] of muscle contractions. For instance, PED is induced after movement at 2.0 Hz but not 1.0 Hz [2], and the degree of PED after finger movement at a moderate sustainable rate is larger than that at a maximal voluntary rate [22]. Although PED is observed not only after voluntary movement task but also after passive movement tasks, PED caused by voluntary movement tasks is more robust than PED caused by passive movement tasks [15]. Moreover, when repetitive finger movement of 10%, 20% or
⇑ Corresponding author at: Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, 1398 Shimami-cho, Kita-ku, Niigata City, Niigata 950–3198, Japan. E-mail address: [email protected] (S. Miyaguchi).
30% of the maximum voluntary contraction (MVC) at 2.0 Hz was performed, PED increased in conjunction with the contraction level [14]. Furthermore, PED is absent in Parkinson’s disease patients except after taking levodopa [21], and PED duration is shortened by repeating movement tasks that induce PED [2]. In contrast, post-exercise facilitation (PEF) consists of an increase in the excitability of the corticospinal tract after medium voluntary muscle contraction [1,5,12,19]. PEF was induced after sustained isometric contraction below 50% MVC for 5–30 s and after motor skill learning tasks such as the visual motor tracking task [6,8], ballistic movement [7,16] and pegboard task [10]. Based on these reports, it can be inferred that PEF occurs after sustained muscle contraction of medium intensity, motor control tasks and motor skill learning tasks. However, it is unclear what kind of motor task causes PED or PEF because various motor tasks with different muscle contraction levels and duration times were used in previous studies. In the present study, we conducted two experiments using simple motor task and motor control task with unified muscle contraction levels and duration times to clarify the movement factors that cause PED after non-fatiguing repetitive movement tasks. We hypothesized that PED occurs after rhythmical and simple repetitive movement tasks and that PEF occurs after movement tasks requiring motor control.
https://doi.org/10.1016/j.jocn.2018.08.026 0967-5868/Ó 2018 Published by Elsevier Ltd.
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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N. Ishikawa et al. / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
2. Methods 2.1. Subjects Twenty-four healthy adults [21.2 ± 0.7 years (age ± standard deviation), 11 males, 19 right-handed] participated in this study. Fifteen healthy subjects (21.1 ± 0.6 years, 6 males, 13 righthanded) participated in experiment 1, and 12 subjects (21.4 ± 1.0 years, 7 males, 9 right-handed) participated in experiment 2. All subjects provided written informed consent. This study was carried out in accordance with the recommendations of the ethics committee of Niigata University of Health and Welfare and conducted in accordance with the Declaration of Helsinki with written informed consent from all subjects. All subjects gave written informed consent in accordance with the Declaration of Helsinki. The protocol was approved by the ethics committee of Niigata University of Health and Welfare. 2.2. Data measurement 2.2.1. Electromyogram (EMG) measurement The surface EMG was recorded from the right first dorsal interosseous (FDI) using Ag/AgCl electrodes. The active electrode was positioned over the muscle belly, and the reference electrode was positioned over the metacarpophalangeal joint. The ground electrode was wrapped around the right forearm. The EMG signal was amplified by an amplifier (A - DL - 720 140, 4 ASSIST, Tokyo, Japan), processed by an A/D converter (Power Lab, AD Instruments, Colorado, USA) with a sampling frequency of 4 kHz, and then stored on a computer. For EMG analysis, high pass filter processing at 20 Hz was performed using biological signal analysis software (Lab Chart 7, AD Instruments, Australia).
Fig. 1. Schematic of the custom-design device with pulley and nylon line for index finger movement tasks (Experiment 1).
was adjusted (20–70 g) so that the average EMG signals during the movement task was 10% of the MVC (10% EMG). The movement range was from the neutral position to the end range of abduction. The joint angle of the proximal interphalangeal joint during the movement tasks was confirmed using an electric goniometer.
2.2.2. MEP measurement A transcranial magnetic stimulation (TMS) device (Magstim 200, Magstim Co, Dyfed, UK) and a figure-eight TMS coil (diameter: 95 mm) were used to elicite MEP. The stimulus site was the left primary motor cortex. The figure-eight TMS coil was placed tangentially approximately 45° from the midline with the handle facing posterolaterally on each subject’s skull. The optimal position for eliciting MEPs from the right FDI muscle was carefully determined by Visor 2 TMS Neuro-navigation (EEMAGINE Medical Imaging Solutions GmbH, BER, DE), which can correctly identify the position of M1 by monitoring each subject’s fMRI image. The stimulus intensity was set to the minimum intensity needed to elicit MEPs of 1 mV in at least 5 of 10 successive trials in the relaxed target muscle. The TMS was delivered at 0.20 Hz.
2.3.2. Experiment 2 The subjects performed repetitive isometric abduction movements of the right index finger for 5 min. We established two movement tasks: 1) adjusting the force according to the target automatically moving up and down on the display (visuomotor task) and 2) rhythmical and simple repetitive movements (simple isometric task). The tensiometer (Force link 9311B, Kistler, Switzerland) (Fig. 2-a) and force control software (Niigata Prefecture Industrial Technology Research Institute, Niigata, Japan) were used for both movement tasks. The contraction level was 10% of the MVC. In the visuomotor task, we instructed the subjects to trace a moving black line (target) as accurately as possible by moving grey circles (control marker) up and down according to the abduction force of the index finger (Fig. 2-b). The target was set to automatically move up and down between 0 and 10%MVC value at 1.0 Hz on the monitor. In the simple isometric task, the target was fixed at 10% of the MVC and did not move on the monitor. Subjects performed repetitive abduction movements so that the control marker reached the target by auditory feedback at 1.0 Hz.
2.3. Movement tasks
2.4. Experimental procedure
2.3.1. Experiment 1 The subjects performed repetitive isotonic abduction movements of the right index finger for 6 min. We established two movement tasks: 1) rhythmical and simple repetitive movement (simple rhythmic task) and 2) a movement task that required control of muscle activity (adjustment task). In the simple rhythmic task, subjects performed repetitive abduction movements at 2 Hz using auditory feedback from headphones. In the adjustment task, subjects gradually performed abduction movements over the course of 5 s, so that the smoothing EMG waveform linearly reached the target value according to the indicator displayed on the PC screen. The waveform returned to the neutral position after 5 s. For both movement tasks, the subjects’ index fingers were attached to the custom-design device consisting of a pulley and nylon line to adjust the load with a weight (Fig. 1). The weight
2.4.1. Experiment 1 The MVC of the right FDI was completed for 5 s, and the weight was adjusted so that the average EMG signals would be 10% of the EMG value. Subjects practiced the movement task for 30 s. There was a 5-min break after the practice. The MEP was measured 12 waveforms before the movement task (T0). The MEP was also measured 12 waveforms 1 min (T1), 2 min (T2), 3 min (T3), 4 min (T4), 5 min (T5), 8 min (T8) and 11 min (T11) after the movement task. The two movement tasks were randomly performed in a repeatedmeasures design with a break of at least 15 min between each movement task. 2.4.2. Experiment 2 The MVC of the right FDI was completed for 5 s to set the strength of the movement task. Subjects practised the movement
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
N. Ishikawa et al. / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
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Fig. 2. Schematic of the visuomotor task and PC monitor (Experiment 2). a) Body position during the movement task. The right index finger was inserted into the force ring and fixed. The forearm was in a pronated position. b) Examples of target and control markers in the visuomotor task are shown. A black line indicates a target, and a grey circle indicates a control marker. The subjects traced a moving target as accurately as possible by moving the control marker up and down according to the abduction force of the index finger. The target was set to automatically move up and down between 0 and 10%MVC value at 1.0 Hz on the monitor.
task for 10 s. There was a 3-min break after the practice. Twelve MEPs were measured before the movement task (T0). The MEP was also measured 12 waveforms 1 min (T1), 2 min (T2), 3 min (T3), 4 min (T4), 5 min (T5), 6 min (T6), 7 min (T7), 8 min (T8), 9 min (T9), and 10 min (T10) after the movement task. The visuomotor task and the simple isometric task were completed with an interval of at least one day between tasks.
differences were found for the main effect of the task factor (F(1,14) = 1.242, P = 0.284) or the time factor (F(7,98) = 0.892, P = 0.516). Post hoc analyses demonstrated that the MEP amplitude at T1 and T2 were significantly lower (P < 0.05) than that at T0 in the simple rhythmic task, whereas no significant difference was observed in the change in MEP amplitudes from T3 to T11. No statistical difference was found among the MEP amplitudes during the adjustment task.
2.5. Data analysis 3.2. Experiment 2 MEP amplitudes, except the maximum and minimum MEP amplitudes, were calculated from peak-to-peak amplitudes of 12 trials. In addition, the average amplitudes of the smoothing EMG signals and abduction force value during the movement tasks were normalized with the values obtained for the MVC of each subject (% EMG and %Force, respectively). Data are expressed as mean ± stan dard error. 2.6. Statistical processing IBM SPSS statistics Ver. 24 (IBM, Armonk, NY, USA) was used for statistical analysis. Two-way repeated-measures ANOVAs (TASK factor TIME factor) were used to compare MEP amplitudes before and after the movement tasks. Post hoc analyses were completed with the Dunnett method. A paired t-test was used to compare %EMG and %Force between two movement tasks. Differences were considered statistically significant at P < 0.05 for all analyses. 3. Results 3.1. Experiment 1 3.1.1. %Emg Fig. 3 shows the joint angles and %EMG values during the simple rhythmic task and adjustment task. The %EMG values were 9.93 ± 0.38 %EMG during the simple rhythmic task and 10.28 ± 0.34 %EMG during the adjustment task. A paired t-test showed no statistical difference in the %EMG values between the two movement tasks. 3.1.2. MEP amplitude Fig. 4 shows change in the MEP amplitudes during the simple rhythmic task and adjustment task. A two-way repeatedmeasures ANOVA revealed a significant task factor time factor interaction (F(4.104,57.457) = 2.790, P = 0.033). No significant
3.2.1. %EMG and %Force Fig. 5 shows the %EMG and %Force values during the visuomotor task and simple isometric task. The %EMG values were 8.21 ± 0.93 %EMG during the visuomotor task and 9.97 ± 1.13 % EMG during the simple isometric task. A paired t-test showed no statistical difference in the %EMG values between movement tasks. The %Force values were 10.56 ± 0.40 %MVC during the visuomotor task and 10.50 ± 0.29 %MVC during the simple isometric task. A paired t-test showed no statistical difference in the %Force values between movement tasks.Fig. 6. 3.2.2. MEP amplitude Fig. 5 shows the changes in MEP amplitudes during the visuomotor task and simple isometric task. A two-way repeatedmeasures ANOVA revealed a significant main effect of time (F(3.700,40.705) = 3.856, P = 0.011) and an interaction of task time (F(10,110) = 3.339, P = 0.001). No significant differences were found for the main effect of the task (F(1,11) = 2.573, P = 0.137). Post hoc analyses demonstrated that the MEP amplitude at T1 and T10 were larger than that at T0 during the visuomotor tasks (P < 0.05). No statistical difference was found between the MEP amplitudes during the simple isometric task. 4. Discussion We conducted two experiments to elucidate the movement factors that cause PED after non-fatiguing repetitive movement tasks. In experiment 1, we compared the temporal change in MEP after a simple rhythmic task and adjustment task. In experiment 2, we compared the temporal change in MEP after a visuomotor task and simple isometric task. Here, we report 3 major findings: 1) PED occurs after repetitive rhythmical simple movements for 6 min at 10%MVC but not after non-rhythmic movement; 2) PEF is observed after a visuomotor tracking task for 5 min at 10%MVC;
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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Fig. 3. Typical examples of joint angle, EMG waveform, and smoothing EMG waveform during movement tasks. a) Simple rhythmic task. Subjects performed repetitive abduction movements of the index finger for 6 min at 2 Hz by auditory feedback. b) Adjustment task. Subjects gradually performed abduction movements over the course of 5 s. The smoothing EMG waveform linearly reached the target value, according to the indicator displayed on the PC screen, in intervals of 5 s. The waveform returned to the neutral position after 5 s.
Fig. 4. Changes in MEP amplitude in experiment 1. a) MEP amplitudes before and after the simple rhythmic task. The MEP amplitudes at T1 and T2 were significantly smaller than that at T0 for the simple rhythmic task. b) MEP amplitudes before and after the adjustment task. No statistical difference was found among the MEP amplitudes for the adjustment task. Error bars indicate standard error. * P < 0.05.
and 3) PED does not occur after an isometric movement task that makes the contraction force visually approach the target value. In experiment 1, PED after repetitive 2-Hz rhythmical simple movements for 6 min at 10%MVC persisted for 2 min. In our previous study, PED after rhythmic repetitive movements at 2 Hz persisted for 3 min. Therefore, the present study supports our previous findings [14]. Several previous studies reported that PED is caused after non-fatiguing movement tasks. Bonato, Zanette, and colleagues reported that PED after thumb adductionabduction movements for 1 min persisted for 30 min [3,4,23],
and F waves, which reflect spinal excitability, did not change during PED [4]. Although PED after thumb adduction-abduction movements at 2 Hz persisted for 30 min, PED after the same movements at 1 Hz did not occur [2]. Moreover, Teo et al. (2012) showed that PED after index finger flexion or adduction-abduction movements for 10 s persisted for 6–8 min, and SICI, which reflects intra-cortical inhibitory circuit activity, was increased during PED [20,22]. Notably, the duration of PED is different among these reports. The movement task used by Bonato et al. (1994, 1996) and Zanette et al. (1995) was a thumb adduction-abduction movement at a
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
N. Ishikawa et al. / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
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Fig. 5. Typical examples of abduction force, EMG waveform, and smoothing EMG waveform during movement tasks. a) Visuomotor task. b) Simple isometric task. The upper figure shows the abduction force (solid line) and target force (dotted line). The middle figure shows the EMG waveform, and the lower figure shows the smoothing EMG waveform.
Fig. 6. Changes in MEP amplitude in experiment 2. a) MEP amplitudes before and after the visuomotor task. The MEP amplitudes at T1 and T10 were significantly larger than that at T0 for the visuomotor task. b) MEP amplitudes before and after the simple isometric task. No statistical difference was found among the MEP amplitudes for the simple isometric task. Error bars indicate standard error. * P < 0.05.
maximum voluntary frequency for 1 min [3,4,23]. Because the maximum frequency movement significantly attenuates movement frequency and range of motion within 20 s [17,20], it can be inferred that muscle fatigue has occurred after maximum frequency movement for 1 min [3,4,23]. Many studies reported that MEP decreased after a muscle fatigue task [11,13,18]; thus, the presence or absence of muscle fatigue may be involved in the difference in PED duration observed in this study and the previous studies by Bonato et al. (1994, 1996) and Zanette et al. (1995). On the other hand, PED persisted for 30 min after thumb
adduction-abduction movement at 2 Hz for 1 min [2], and PED persisted for 8 min after index finger flexion movement at 1–3 Hz for 10 s [20,22]. Further research is needed to determine the cause of varying PED durations across studies. In experiment 1, non-rhythmic adjustment tasks were similar to the simple rhythmic task in total muscle activity and duration of movement, but PED was not observed. In experiment 2, the MEP amplitude increased after the visuomotor task, indicating PEF occurred. PED did not occur after the adjustment tasks in experiment 1, likely because the motor task was required to adjust
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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muscle activity based on visual feedback whereas watching the monitor is not rhythmic repetitive movement. Previous studies showed that MEP amplitude was increased after a visuomotor task, indicating PEF occurs [6,8,9]. For example, PEF occurred after the visuomotor task for 3 min or 6 min in 2–3 sets [6,8,9]. In experiment 1, it is inferred that both PED and PEF did not occur because the contraction levels were low (10%MVC) and, although the motor task was similar to the visuomotor task, it was a relatively simple visuomotor task that linearly increases muscle activity over 5 s. On the other hand, PEF was observed after the visuomotor task in experiment 2. Despite the same muscle contraction level, PEF likely occurred [6,8,9] because the motor task in experiment 2 was a difficult visuomotor tracking task requiring a match of the abduction force to the moving index when compared with the non-rhythmic control task in experiment 1. In experiment 2, PED was not observed after the simple isometric task with 10%MVC at 1 Hz for 5 min. Our previous study showed that PED changes according to the muscle contraction levels during movement task, and that PED after movement tasks at 10%MVC is small. And also, PED after the isometric contraction task is smaller than that after the isotonic contraction task [14]. As described above, PED occurs at a 2-Hz movement frequency but not at 1-Hz movement frequency 6). Based on previous reports, we speculate PED was not observed after the simple isometric task in experiment 2 because it was an isometric contraction with 10% MVC at 1 Hz. Additionally, it we speculate PED did not occur because the motor task was not only a simple repetitive rhythmic movement task combined with an auditory stimulus but also required muscle contraction adjustments so that the abduction force reached the target value displayed on the PC display. The present study has two limitations. First, we did not measure the excitability of spinal cord anterior horn cells or the activity of the intra-cortical inhibitory circuit. Previous studies have reported that the F wave does not change during PED and PEF and that SICI increases or decreases [4,23]. Therefore, further research is necessary to investigate whether these previous findings can be replicated. Second, the reason why the duration of PED was shorter than the previous study remains unknown. However, we believe that the present study verifies the hypothesis that rhythmical and simple non-fatiguing repetitive movement causes PED. In conclusion, we investigated the influence of a simple repetitive voluntary movement task and a movement task requiring muscle contraction control on the excitability of the corticospinal tract. We demonstrated that 1) the excitability of the corticospinal tract is decreased after rhythmic repetitive movement at 2 Hz, 2) the excitability of the corticospinal tract does not change after repetitive movements requiring muscle contraction control at 0.2 Hz and simple isometric repetitive movements at 1 Hz, and 3) the excitability of the corticospinal tract increases after a visuomotor task at 1 Hz. Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments This work was supported by a Grant-in-Aid for Scientific Research (B) 16H03207 from the Japan Society for Promotion of
Science and Grant-in-Aid for Scientific Research of Niigata University of Health and Welfare (H28C06). The authors would like to thank Enago (www.enago.jp) for the English language review. References [1] Balbi P, Perretti A, Sannino M, Marcantonio L, Santoro L. Postexercise facilitation of motor evoked potentials following transcranial magnetic stimulation: a study in normal subjects. Muscle Nerve 2002;25:448–52. [2] Bonato C, Zanette G, Fiaschi A, Rossini PM. Activity-dependent modulation of synaptic transmission in the intact human motor cortex revealed with transcranial magnetic stimulation. Cereb Cortex 2002;12:1057–62. [3] Bonato C, Zanette G, Manganotti P, Tinazzi M, Bongiovanni G, Polo A, et al. ’Direct’ and ’crossed’ modulation of human motor cortex excitability following exercise. Neurosci Lett 1996;216:97–100. [4] Bonato C, Zanette G, Polo A, Bongiovanni G, Manganotti P, Tinazzi M, et al. Cortical output modulation after rapid repetitive movements. Ital J Neurol Sci 1994;15:489–94. [5] Brasil-Neto JP, Araujo VP, Carneiro CR. Postexercise facilitation of motor evoked potentials elicited by ipsilateral voluntary contraction. Muscle Nerve 1999;22:1710–2. [6] Cirillo J, Hughes J, Ridding M, Thomas PQ, Semmler JG. Differential modulation of motor cortex excitability in BDNF Met allele carriers following experimentally induced and use-dependent plasticity. Eur J Neurosci 2012;36:2640–9. [7] Cirillo J, Rogasch NC, Semmler JG. Hemispheric differences in use-dependent corticomotor plasticity in young and old adults. Exp Brain Res 2010;205:57–68. [8] Cirillo J, Todd G, Semmler JG. Corticomotor excitability and plasticity following complex visuomotor training in young and old adults. Eur J Neurosci 2011;34:1847–56. [9] Gallasch E, Christova M, Krenn M, Kossev A, Rafolt D. Changes in motor cortex excitability following training of a novel goal-directed motor task. Eur J Appl Physiol 2009;105:47–54. [10] Garry MI, Kamen G, Nordstrom MA. Hemispheric differences in the relationship between corticomotor excitability changes following a finemotor task and motor learning. J Neurophysiol 2004;91:1570–8. [11] Kotan S, Kojima S, Miyaguchi S, Sugawara K, Onishi H. Depression of corticomotor excitability after muscle fatigue induced by electrical stimulation and voluntary contraction. Front Hum Neurosci 2015;9:363. [12] Lentz M, Nielsen JF. Post-exercise facilitation and depression of M wave and motor evoked potentials in healthy subjects. Clin Neurophysiol 2002;113:1092–8. [13] McKay WB, Tuel SM, Sherwood AM, Stokic DS, Dimitrijevic MR. Focal depression of cortical excitability induced by fatiguing muscle contraction: a transcranial magnetic stimulation study. Exp Brain Res 1995;105:276–82. [14] Miyaguchi S, Kojima S, Kirimoto H, Tamaki H, Onishi H. Do differences in levels, types, and duration of muscle contraction have an effect on the degree of post-exercise depression? Front Hum Neurosci 2016;10:159. [15] Miyaguchi S, Onishi H, Kojima S, Sugawara K, Tsubaki A, Kirimoto H, et al. Corticomotor excitability induced by anodal transcranial direct current stimulation with and without non-exhaustive movement. Brain Res 2013;1529:83–91. [16] Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M. Role of the human motor cortex in rapid motor learning. Exp Brain Res 2001;136:431–8. [17] Rodrigues JP, Mastaglia FL, Thickbroom GW. Rapid slowing of maximal finger movement rate: fatigue of central motor control? Exp Brain Res 2009;196:557–63. [18] Sacco P, Thickbroom GW, Byrnes ML, Mastaglia FL. Changes in corticomotor excitability after fatiguing muscle contractions. Muscle Nerve 2000;23:1840–6. [19] Samii A, Wassermann EM, Ikoma K, Mercuri B, Hallett M. Characterization of postexercise facilitation and depression of motor evoked potentials to transcranial magnetic stimulation. Neurology 1996;46:1376–82. [20] Teo WP, Rodrigues JP, Mastaglia FL, Thickbroom GW. Changes in corticomotor excitability and inhibition after exercise are influenced by hand dominance and motor demand. Neuroscience 2012;210:110–7. [21] Teo WP, Rodrigues JP, Mastaglia FL, Thickbroom GW. Modulation of corticomotor excitability after maximal or sustainable-rate repetitive finger movement is impaired in Parkinson’s disease and is reversed by levodopa. Clin Neurophysiol 2014;125:562–8. [22] Teo WP, Rodrigues JP, Mastaglia FL, Thickbroom GW. Post-exercise depression in corticomotor excitability after dynamic movement: a general property of fatiguing and non-fatiguing exercise. Exp Brain Res 2012;216:41–9. [23] Zanette G, Bonato C, Polo A, Tinazzi M, Manganotti P, Fiaschi A. Long-lasting depression of motor-evoked potentials to transcranial magnetic stimulation following exercise. Exp Brain Res 1995;107:80–6.
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Experimental study
Corticospinal excitability following repetitive voluntary movement Natsumi Ishikawa a, Ryunosuke Miyao a, Shota Tsuiki b,c, Ryoki Sasaki b,c, Shota Miyaguchi c,⇑, Hideaki Onishi c a
Department of Physical Therapy, Niigata University of Health and Welfare, Japan Graduate School, Niigata University of Health and Welfare, Japan c Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Japan b
a r t i c l e
i n f o
Article history: Received 9 April 2018 Accepted 12 August 2018 Available online xxxx
a b s t r a c t Post-exercise cortical depression (PED) is induced by non-fatiguing finger movement. Because the type of exercise that causes PED remains unclear, we conducted two experiments to clarify which exercise factors induce PED. Fifteen healthy participants performed repetitive abduction movements of the right index finger at 2.0 Hz (simple rhythmic task) and 0.2 Hz (adjustment task) for 6 min each in experiment 1. Twelve healthy participants performed repetitive and isometric abduction contractions of the right index finger at 1.0 Hz with visuomotor tracking (visuomotor task) and without visuomotor tracking (simple isometric task) for 5 min each in experiment 2. Muscle contraction levels were 10% of the maximum voluntary contraction in all tasks. Motor evoked potentials (MEPs) evoked by transcranial magnetic stimulation were recorded from the right first dorsal interosseous muscle before and after the movement tasks. The simple rhythmic task transiently reduced MEP amplitudes when compared with baseline in experiment 1. In contrast, the visuomotor task increased MEP amplitudes in experiment 2. No MEP changes were observed following the adjustment task in experiment 1 and the simple isometric task in experiment 2. This study suggests that PED is induced by simple rhythmic movement. Ó 2018 Published by Elsevier Ltd.
1. Introduction The excitability of the corticospinal tract decreases after repetitive non-fatiguing movements. This phenomenon has been defined as post-exercise cortical depression (PED) [3,4]. PED is likely caused by a reduction in primary motor cortex (M1) excitability because the F wave, which is used as the index of spinal excitability, does not change [4,23], and the short-interval intracortical inhibition (SICI), which is used as the index of inhibitory circuits in the cortex, is increased [20,22]. Moreover, PED is modulated by changes in movement factors, such as levels [14], types [14] and frequency [2,22] of muscle contractions. For instance, PED is induced after movement at 2.0 Hz but not 1.0 Hz [2], and the degree of PED after finger movement at a moderate sustainable rate is larger than that at a maximal voluntary rate [22]. Although PED is observed not only after voluntary movement task but also after passive movement tasks, PED caused by voluntary movement tasks is more robust than PED caused by passive movement tasks [15]. Moreover, when repetitive finger movement of 10%, 20% or
⇑ Corresponding author at: Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, 1398 Shimami-cho, Kita-ku, Niigata City, Niigata 950–3198, Japan. E-mail address: [email protected] (S. Miyaguchi).
30% of the maximum voluntary contraction (MVC) at 2.0 Hz was performed, PED increased in conjunction with the contraction level [14]. Furthermore, PED is absent in Parkinson’s disease patients except after taking levodopa [21], and PED duration is shortened by repeating movement tasks that induce PED [2]. In contrast, post-exercise facilitation (PEF) consists of an increase in the excitability of the corticospinal tract after medium voluntary muscle contraction [1,5,12,19]. PEF was induced after sustained isometric contraction below 50% MVC for 5–30 s and after motor skill learning tasks such as the visual motor tracking task [6,8], ballistic movement [7,16] and pegboard task [10]. Based on these reports, it can be inferred that PEF occurs after sustained muscle contraction of medium intensity, motor control tasks and motor skill learning tasks. However, it is unclear what kind of motor task causes PED or PEF because various motor tasks with different muscle contraction levels and duration times were used in previous studies. In the present study, we conducted two experiments using simple motor task and motor control task with unified muscle contraction levels and duration times to clarify the movement factors that cause PED after non-fatiguing repetitive movement tasks. We hypothesized that PED occurs after rhythmical and simple repetitive movement tasks and that PEF occurs after movement tasks requiring motor control.
https://doi.org/10.1016/j.jocn.2018.08.026 0967-5868/Ó 2018 Published by Elsevier Ltd.
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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2. Methods 2.1. Subjects Twenty-four healthy adults [21.2 ± 0.7 years (age ± standard deviation), 11 males, 19 right-handed] participated in this study. Fifteen healthy subjects (21.1 ± 0.6 years, 6 males, 13 righthanded) participated in experiment 1, and 12 subjects (21.4 ± 1.0 years, 7 males, 9 right-handed) participated in experiment 2. All subjects provided written informed consent. This study was carried out in accordance with the recommendations of the ethics committee of Niigata University of Health and Welfare and conducted in accordance with the Declaration of Helsinki with written informed consent from all subjects. All subjects gave written informed consent in accordance with the Declaration of Helsinki. The protocol was approved by the ethics committee of Niigata University of Health and Welfare. 2.2. Data measurement 2.2.1. Electromyogram (EMG) measurement The surface EMG was recorded from the right first dorsal interosseous (FDI) using Ag/AgCl electrodes. The active electrode was positioned over the muscle belly, and the reference electrode was positioned over the metacarpophalangeal joint. The ground electrode was wrapped around the right forearm. The EMG signal was amplified by an amplifier (A - DL - 720 140, 4 ASSIST, Tokyo, Japan), processed by an A/D converter (Power Lab, AD Instruments, Colorado, USA) with a sampling frequency of 4 kHz, and then stored on a computer. For EMG analysis, high pass filter processing at 20 Hz was performed using biological signal analysis software (Lab Chart 7, AD Instruments, Australia).
Fig. 1. Schematic of the custom-design device with pulley and nylon line for index finger movement tasks (Experiment 1).
was adjusted (20–70 g) so that the average EMG signals during the movement task was 10% of the MVC (10% EMG). The movement range was from the neutral position to the end range of abduction. The joint angle of the proximal interphalangeal joint during the movement tasks was confirmed using an electric goniometer.
2.2.2. MEP measurement A transcranial magnetic stimulation (TMS) device (Magstim 200, Magstim Co, Dyfed, UK) and a figure-eight TMS coil (diameter: 95 mm) were used to elicite MEP. The stimulus site was the left primary motor cortex. The figure-eight TMS coil was placed tangentially approximately 45° from the midline with the handle facing posterolaterally on each subject’s skull. The optimal position for eliciting MEPs from the right FDI muscle was carefully determined by Visor 2 TMS Neuro-navigation (EEMAGINE Medical Imaging Solutions GmbH, BER, DE), which can correctly identify the position of M1 by monitoring each subject’s fMRI image. The stimulus intensity was set to the minimum intensity needed to elicit MEPs of 1 mV in at least 5 of 10 successive trials in the relaxed target muscle. The TMS was delivered at 0.20 Hz.
2.3.2. Experiment 2 The subjects performed repetitive isometric abduction movements of the right index finger for 5 min. We established two movement tasks: 1) adjusting the force according to the target automatically moving up and down on the display (visuomotor task) and 2) rhythmical and simple repetitive movements (simple isometric task). The tensiometer (Force link 9311B, Kistler, Switzerland) (Fig. 2-a) and force control software (Niigata Prefecture Industrial Technology Research Institute, Niigata, Japan) were used for both movement tasks. The contraction level was 10% of the MVC. In the visuomotor task, we instructed the subjects to trace a moving black line (target) as accurately as possible by moving grey circles (control marker) up and down according to the abduction force of the index finger (Fig. 2-b). The target was set to automatically move up and down between 0 and 10%MVC value at 1.0 Hz on the monitor. In the simple isometric task, the target was fixed at 10% of the MVC and did not move on the monitor. Subjects performed repetitive abduction movements so that the control marker reached the target by auditory feedback at 1.0 Hz.
2.3. Movement tasks
2.4. Experimental procedure
2.3.1. Experiment 1 The subjects performed repetitive isotonic abduction movements of the right index finger for 6 min. We established two movement tasks: 1) rhythmical and simple repetitive movement (simple rhythmic task) and 2) a movement task that required control of muscle activity (adjustment task). In the simple rhythmic task, subjects performed repetitive abduction movements at 2 Hz using auditory feedback from headphones. In the adjustment task, subjects gradually performed abduction movements over the course of 5 s, so that the smoothing EMG waveform linearly reached the target value according to the indicator displayed on the PC screen. The waveform returned to the neutral position after 5 s. For both movement tasks, the subjects’ index fingers were attached to the custom-design device consisting of a pulley and nylon line to adjust the load with a weight (Fig. 1). The weight
2.4.1. Experiment 1 The MVC of the right FDI was completed for 5 s, and the weight was adjusted so that the average EMG signals would be 10% of the EMG value. Subjects practiced the movement task for 30 s. There was a 5-min break after the practice. The MEP was measured 12 waveforms before the movement task (T0). The MEP was also measured 12 waveforms 1 min (T1), 2 min (T2), 3 min (T3), 4 min (T4), 5 min (T5), 8 min (T8) and 11 min (T11) after the movement task. The two movement tasks were randomly performed in a repeatedmeasures design with a break of at least 15 min between each movement task. 2.4.2. Experiment 2 The MVC of the right FDI was completed for 5 s to set the strength of the movement task. Subjects practised the movement
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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Fig. 2. Schematic of the visuomotor task and PC monitor (Experiment 2). a) Body position during the movement task. The right index finger was inserted into the force ring and fixed. The forearm was in a pronated position. b) Examples of target and control markers in the visuomotor task are shown. A black line indicates a target, and a grey circle indicates a control marker. The subjects traced a moving target as accurately as possible by moving the control marker up and down according to the abduction force of the index finger. The target was set to automatically move up and down between 0 and 10%MVC value at 1.0 Hz on the monitor.
task for 10 s. There was a 3-min break after the practice. Twelve MEPs were measured before the movement task (T0). The MEP was also measured 12 waveforms 1 min (T1), 2 min (T2), 3 min (T3), 4 min (T4), 5 min (T5), 6 min (T6), 7 min (T7), 8 min (T8), 9 min (T9), and 10 min (T10) after the movement task. The visuomotor task and the simple isometric task were completed with an interval of at least one day between tasks.
differences were found for the main effect of the task factor (F(1,14) = 1.242, P = 0.284) or the time factor (F(7,98) = 0.892, P = 0.516). Post hoc analyses demonstrated that the MEP amplitude at T1 and T2 were significantly lower (P < 0.05) than that at T0 in the simple rhythmic task, whereas no significant difference was observed in the change in MEP amplitudes from T3 to T11. No statistical difference was found among the MEP amplitudes during the adjustment task.
2.5. Data analysis 3.2. Experiment 2 MEP amplitudes, except the maximum and minimum MEP amplitudes, were calculated from peak-to-peak amplitudes of 12 trials. In addition, the average amplitudes of the smoothing EMG signals and abduction force value during the movement tasks were normalized with the values obtained for the MVC of each subject (% EMG and %Force, respectively). Data are expressed as mean ± stan dard error. 2.6. Statistical processing IBM SPSS statistics Ver. 24 (IBM, Armonk, NY, USA) was used for statistical analysis. Two-way repeated-measures ANOVAs (TASK factor TIME factor) were used to compare MEP amplitudes before and after the movement tasks. Post hoc analyses were completed with the Dunnett method. A paired t-test was used to compare %EMG and %Force between two movement tasks. Differences were considered statistically significant at P < 0.05 for all analyses. 3. Results 3.1. Experiment 1 3.1.1. %Emg Fig. 3 shows the joint angles and %EMG values during the simple rhythmic task and adjustment task. The %EMG values were 9.93 ± 0.38 %EMG during the simple rhythmic task and 10.28 ± 0.34 %EMG during the adjustment task. A paired t-test showed no statistical difference in the %EMG values between the two movement tasks. 3.1.2. MEP amplitude Fig. 4 shows change in the MEP amplitudes during the simple rhythmic task and adjustment task. A two-way repeatedmeasures ANOVA revealed a significant task factor time factor interaction (F(4.104,57.457) = 2.790, P = 0.033). No significant
3.2.1. %EMG and %Force Fig. 5 shows the %EMG and %Force values during the visuomotor task and simple isometric task. The %EMG values were 8.21 ± 0.93 %EMG during the visuomotor task and 9.97 ± 1.13 % EMG during the simple isometric task. A paired t-test showed no statistical difference in the %EMG values between movement tasks. The %Force values were 10.56 ± 0.40 %MVC during the visuomotor task and 10.50 ± 0.29 %MVC during the simple isometric task. A paired t-test showed no statistical difference in the %Force values between movement tasks.Fig. 6. 3.2.2. MEP amplitude Fig. 5 shows the changes in MEP amplitudes during the visuomotor task and simple isometric task. A two-way repeatedmeasures ANOVA revealed a significant main effect of time (F(3.700,40.705) = 3.856, P = 0.011) and an interaction of task time (F(10,110) = 3.339, P = 0.001). No significant differences were found for the main effect of the task (F(1,11) = 2.573, P = 0.137). Post hoc analyses demonstrated that the MEP amplitude at T1 and T10 were larger than that at T0 during the visuomotor tasks (P < 0.05). No statistical difference was found between the MEP amplitudes during the simple isometric task. 4. Discussion We conducted two experiments to elucidate the movement factors that cause PED after non-fatiguing repetitive movement tasks. In experiment 1, we compared the temporal change in MEP after a simple rhythmic task and adjustment task. In experiment 2, we compared the temporal change in MEP after a visuomotor task and simple isometric task. Here, we report 3 major findings: 1) PED occurs after repetitive rhythmical simple movements for 6 min at 10%MVC but not after non-rhythmic movement; 2) PEF is observed after a visuomotor tracking task for 5 min at 10%MVC;
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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Fig. 3. Typical examples of joint angle, EMG waveform, and smoothing EMG waveform during movement tasks. a) Simple rhythmic task. Subjects performed repetitive abduction movements of the index finger for 6 min at 2 Hz by auditory feedback. b) Adjustment task. Subjects gradually performed abduction movements over the course of 5 s. The smoothing EMG waveform linearly reached the target value, according to the indicator displayed on the PC screen, in intervals of 5 s. The waveform returned to the neutral position after 5 s.
Fig. 4. Changes in MEP amplitude in experiment 1. a) MEP amplitudes before and after the simple rhythmic task. The MEP amplitudes at T1 and T2 were significantly smaller than that at T0 for the simple rhythmic task. b) MEP amplitudes before and after the adjustment task. No statistical difference was found among the MEP amplitudes for the adjustment task. Error bars indicate standard error. * P < 0.05.
and 3) PED does not occur after an isometric movement task that makes the contraction force visually approach the target value. In experiment 1, PED after repetitive 2-Hz rhythmical simple movements for 6 min at 10%MVC persisted for 2 min. In our previous study, PED after rhythmic repetitive movements at 2 Hz persisted for 3 min. Therefore, the present study supports our previous findings [14]. Several previous studies reported that PED is caused after non-fatiguing movement tasks. Bonato, Zanette, and colleagues reported that PED after thumb adductionabduction movements for 1 min persisted for 30 min [3,4,23],
and F waves, which reflect spinal excitability, did not change during PED [4]. Although PED after thumb adduction-abduction movements at 2 Hz persisted for 30 min, PED after the same movements at 1 Hz did not occur [2]. Moreover, Teo et al. (2012) showed that PED after index finger flexion or adduction-abduction movements for 10 s persisted for 6–8 min, and SICI, which reflects intra-cortical inhibitory circuit activity, was increased during PED [20,22]. Notably, the duration of PED is different among these reports. The movement task used by Bonato et al. (1994, 1996) and Zanette et al. (1995) was a thumb adduction-abduction movement at a
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
N. Ishikawa et al. / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
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Fig. 5. Typical examples of abduction force, EMG waveform, and smoothing EMG waveform during movement tasks. a) Visuomotor task. b) Simple isometric task. The upper figure shows the abduction force (solid line) and target force (dotted line). The middle figure shows the EMG waveform, and the lower figure shows the smoothing EMG waveform.
Fig. 6. Changes in MEP amplitude in experiment 2. a) MEP amplitudes before and after the visuomotor task. The MEP amplitudes at T1 and T10 were significantly larger than that at T0 for the visuomotor task. b) MEP amplitudes before and after the simple isometric task. No statistical difference was found among the MEP amplitudes for the simple isometric task. Error bars indicate standard error. * P < 0.05.
maximum voluntary frequency for 1 min [3,4,23]. Because the maximum frequency movement significantly attenuates movement frequency and range of motion within 20 s [17,20], it can be inferred that muscle fatigue has occurred after maximum frequency movement for 1 min [3,4,23]. Many studies reported that MEP decreased after a muscle fatigue task [11,13,18]; thus, the presence or absence of muscle fatigue may be involved in the difference in PED duration observed in this study and the previous studies by Bonato et al. (1994, 1996) and Zanette et al. (1995). On the other hand, PED persisted for 30 min after thumb
adduction-abduction movement at 2 Hz for 1 min [2], and PED persisted for 8 min after index finger flexion movement at 1–3 Hz for 10 s [20,22]. Further research is needed to determine the cause of varying PED durations across studies. In experiment 1, non-rhythmic adjustment tasks were similar to the simple rhythmic task in total muscle activity and duration of movement, but PED was not observed. In experiment 2, the MEP amplitude increased after the visuomotor task, indicating PEF occurred. PED did not occur after the adjustment tasks in experiment 1, likely because the motor task was required to adjust
Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026
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muscle activity based on visual feedback whereas watching the monitor is not rhythmic repetitive movement. Previous studies showed that MEP amplitude was increased after a visuomotor task, indicating PEF occurs [6,8,9]. For example, PEF occurred after the visuomotor task for 3 min or 6 min in 2–3 sets [6,8,9]. In experiment 1, it is inferred that both PED and PEF did not occur because the contraction levels were low (10%MVC) and, although the motor task was similar to the visuomotor task, it was a relatively simple visuomotor task that linearly increases muscle activity over 5 s. On the other hand, PEF was observed after the visuomotor task in experiment 2. Despite the same muscle contraction level, PEF likely occurred [6,8,9] because the motor task in experiment 2 was a difficult visuomotor tracking task requiring a match of the abduction force to the moving index when compared with the non-rhythmic control task in experiment 1. In experiment 2, PED was not observed after the simple isometric task with 10%MVC at 1 Hz for 5 min. Our previous study showed that PED changes according to the muscle contraction levels during movement task, and that PED after movement tasks at 10%MVC is small. And also, PED after the isometric contraction task is smaller than that after the isotonic contraction task [14]. As described above, PED occurs at a 2-Hz movement frequency but not at 1-Hz movement frequency 6). Based on previous reports, we speculate PED was not observed after the simple isometric task in experiment 2 because it was an isometric contraction with 10% MVC at 1 Hz. Additionally, it we speculate PED did not occur because the motor task was not only a simple repetitive rhythmic movement task combined with an auditory stimulus but also required muscle contraction adjustments so that the abduction force reached the target value displayed on the PC display. The present study has two limitations. First, we did not measure the excitability of spinal cord anterior horn cells or the activity of the intra-cortical inhibitory circuit. Previous studies have reported that the F wave does not change during PED and PEF and that SICI increases or decreases [4,23]. Therefore, further research is necessary to investigate whether these previous findings can be replicated. Second, the reason why the duration of PED was shorter than the previous study remains unknown. However, we believe that the present study verifies the hypothesis that rhythmical and simple non-fatiguing repetitive movement causes PED. In conclusion, we investigated the influence of a simple repetitive voluntary movement task and a movement task requiring muscle contraction control on the excitability of the corticospinal tract. We demonstrated that 1) the excitability of the corticospinal tract is decreased after rhythmic repetitive movement at 2 Hz, 2) the excitability of the corticospinal tract does not change after repetitive movements requiring muscle contraction control at 0.2 Hz and simple isometric repetitive movements at 1 Hz, and 3) the excitability of the corticospinal tract increases after a visuomotor task at 1 Hz. Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments This work was supported by a Grant-in-Aid for Scientific Research (B) 16H03207 from the Japan Society for Promotion of
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Please cite this article in press as: Ishikawa N et al. Corticospinal excitability following repetitive voluntary movement. J Clin Neurosci (2018), https://doi. org/10.1016/j.jocn.2018.08.026