How is muscle force modulated during hand exercise? Oxygenation in the contralateral primary motor cortex (M1) has been observed to vary considerably across trials of repetitive handgrip exercise. No linear relationship was observed between the average value of oxygenation determined by a block design study and the force of the handgrip. We found reduced oxygenation in the ipsilateral M1 and unchanged oxygenation in the contralateral M1 during repetitive static handgrip exercises (40% and 60% maximal voluntary contraction; 10 s exercise/75 s rest; 5 sets), which might be due to short-term motor learning. These results support the hypothesis that the ipsilateral M1 might functionally compensate for the contralateral M1 in force modulation during unilateral exercises

Kenichi Shibuya

Masako Iwadate

Tomoko Sadamoto

English

Nature Precedings

Title: Reduced contribution of the ipsilateral primary motor cortex to force 
modulation with short-term motor learning in humans: An NIRS study 
 
Authors: Kenichi Shibuya1, Masako Iwadate1, 2, Tomoko Sadamoto1 
K.S.: Research Institute of Physical Fitness, Japan Women’s College of Physical Education, 8-19-1 
Kita-Karasuyama, Setagaya-ku, Tokyo 157-8565, Japan, kshibuya@jwcpe.ac.jp, TEL: 
+81-3-3300-9175, FAX: +81-3-3307-5825 
M.I: College of Humanities and Sciences, Nihon University, 3-25-40 Sakurajyosui, Setagaya-ku, 
Tokyo 156-8550, Japan, masakoiwadate77@yahoo.co.jp 
T.S.: Research Institute of Physical Fitness, Japan Women’s College of Physical Education, 8-19-1 
Kita-Karasuyama, Setagaya-ku, Tokyo 157-8565, Japan, sadamoto@jwcpe.ac.jp 
 
Correspondence should be addressed to K.S. (kshibuya@jwcpe.ac.jp). 
 
 
Abstract 
How is muscle force modulated during hand exercise? Oxygenation in the contralateral primary 
motor cortex (M1) has been observed to vary considerably across trials of repetitive handgrip 
exercise. No linear relationship was observed between the average value of oxygenation determined 
by a block design study and the force of the handgrip. We found reduced oxygenation in the 
ipsilateral M1 and unchanged oxygenation in the contralateral M1 during repetitive static handgrip 
exercises (40% and 60% maximal voluntary contraction; 10 s exercise/75 s rest; 5 sets), which might 
be due to short-term motor learning. These results support the hypothesis that the ipsilateral M1 
might functionally compensate for the contralateral M1 in force modulation during unilateral 
exercises. 
 
The main text 
 The brain-machine interface (BMI) enables support devices such as artificial hands to restore lost 
human capabilities. The development of these devices would be a breakthrough for neuroscientists in 
the field of movement control. Enabling individuals who have lost their hands to drink a cup of 
coffee through the use of an artificial hand would offer immense gratification to them. BMI 
technology can achieve this goal. However, if the artificial hand is unable to decipher the 
information transmitted by the brain for force modulation, it would breach or release the held object. 
Force modulation of an artificial hand by the brain is a key factor in the development of artificial 
hands through the application of BMI technology. 
  Studies to confirm the relationship between oxygenation in the contralateral primary motor cortex 
(M1) and power output in humans have yielded contradictory results1–3. Recently, it was confirmed 
that the oxygenation in the ipsilateral M1 is considerably higher than that in the contralateral M1. 
This finding was attributed to precise force control during contractions1. Further, the function of the 
ipsilateral M1 complements or inhibits that of the contralateral M14–7. In case of force modulation, 
the ipsilateral M1 may function complementarily to the contralateral M1. 
 Plasticity of the cerebral cortex often poses problems in studies on the oxygenation in the 
bilateral M18. Some researchers have described the relationship between force modulation and the 
ipsilateral M1 oxygenation1,8. This relationship is not constant and is altered by the plasticity of the 
brain. The validation of M1 oxygenation measured at each trial especially fails to explain the force 
modulation. If the ipsilateral M1 modulates the muscle force in a complementary manner, the 
oxygenation in the ipsilateral M1 should decrease with the habituation of an exercise task. On the 
other hand, if the ipsilateral M1 does not control muscle force in a complementary manner or if the 
ipsilateral M1 modulates muscle force predominantly, then the oxygenation in the ipsilateral M1 
should not decrease with the habituation of an exercise task. 
 Subsequently, we aimed to investigate the effect of motor learning on the contribution of the 
changes in the ipsilateral M1 to force modulation. We monitored the oxygenation in the bilateral M1 
during a repetitive handgrip task using near-infrared spectroscopy (NIRS) (details in Supplementary 
Methods and Figure S1). Changes in bilateral M1 oxygenation were measured by NIRS during 5 
repetitions of the handgrip task [exercise: 10 s, rest: 75 s; the tasks were performed at 40% and 60% 
of maximal voluntary contraction (MVC)]. Unlike functional magnetic resonance imaging (fMRI), 
NIRS can monitor the changes in oxygenation in the bilateral M1 at real time without the need for 
the superposition of the slices (details in Supplementary Methods). 
The results of repeated two-way analysis of variance (ANOVA) for the peak changes in the 
oxygenation in the bilateral M1from resting values at 40% MVC (Experiment 1) and 60% MVC 
(Experiment 2) are shown in Table 1 and Table 2. The peak changes in the oxyhemoglobin (HbO2) 
values in the contralateral M1 did not significantly differ across the MVC trials at both intensities 
(40% MVC: F = 0.798, p = 0.5358; 60% MVC: F = 0.403, p = 0.8050) (Figure 1 and 2). 
Correspondingly, the peak changes in deoxyhemoglobin (Hb) in the contralateral M1 did not differ 
significantly across the MVC trials at both intensities (40% MVC: F = 3.154, p = 0.0281; 60% 
MVC: F = 2.929, p = 0.0371) (Figure 1 and 2). The peak changes in HbO2 in the ipsilateral M1 
significantly differed across the MVC trials at both intensities (40% MVC: F = 3.154, p = 0.0281; 
60% MVC: F = 2.929, p = 0.0371) (Figures 1 and 2). On the other hand, the peak changes in Hb in 
the contralateral M1 did not significantly differ across the trials, whereas those in the ipsilateral M1 
significantly differed across the trials (40% MVC: F = 6.711, p = 0.0005; 60% MVC: F = 3.057, p 
= .0317) (Figures 1 and 2). A post-hoc test (paired t-test) revealed significant differences in the 
oxygenation (HbO2 and Hb) changes in the ipsilateral M1 between the first and fifth trials (Tables 1 
and 2). 
The results of this study contradict the fact that the ipsilateral M1 partially contributes in force 
modulation. Muscle power output during exercise is fundamentally controlled by the contralateral 
M1. During the motor learning phase, the ipsilateral M1 may act in a complementary manner with 
regard to force modulation. In the present study, we used the handgrip ergometer (details in 
Supplementary Fig 1). The use of this instrument rather than a visual feedback system, as in previous 
studies8,9, enabled easy evaluation of force modulation. In addition, the subjects practiced using the 
device over several days. Thus, the effects of motor learning on force modulation could be 
determined in relatively fewer repetitions of the exercise task. A previous study showed a decrease in 
ipsilateral M1 oxygenation during a sustained handgrip exercise performed at 30% MVC9. These 
results indicate that the contribution of the ipsilateral M1 to force modulation might be 
complementary to that of the contralateral M1. As shown by Newton et al.10, the increased neural 
activation in the M1 of one hemisphere induces reduced neuronal activity in the M1 of the opposite 
hemisphere. Based on these results, oxygenation in the ipsilateral M1 should reduce neural 
activation in the contralateral M1. 
However, NIRS cannot be used to determine the involvement of both hemispheres of the brain in 
force modulation because of technical drawbacks. The contribution of the ipsilateral and 
contralateral M1 to force modulation can be clearly studied using transcranial magnetic stimulation 
(TMS). Thereafter, the uniformity of the contribution of the ipsilateral and contralateral M1 to force 
modulation remains unclear. The present results suggest collateral contribution of the ipsilateral M1 
to force modulation, and that this contribution declines with motor learning. Further studies should 
focus on elucidating the contribution of the ipsilateral M1 to force modulation. This information will 
help achieve advances in BMI technology. 
 
ACKNOWLEDGEMENTS 
We thank N. Kuboyama and C. Ueda for their helpful comments. This work was supported by the “Academic 
Frontier” Project for Private Universities: matching fund subsidy from the Ministry of Education, Culture, Sports, 
Science and Technology of Japan to the Research Institute of Physical Fitness, Japan Women’s College of Physical 
Education. It was also supported by a Grant-in-Aid for Young Scientists (B, #19700532) from the Ministry of 
Education, Science and Culture of Japan to K.S. 
 
AUTHOR CONTRIBUTIONS 
This study was designed by all 3 authors. Data collection was performed by all 3 authors. K.S. was responsible for 
data analysis and writing the paper. 
 
COMPETING INTERESTS STATEMENT 
The authors declare competing financial interests. 
 
REFERENCES 
1. Dai, T.H. et al. Exp Brain Res. 140, 290-300 (2001) 
2. Dettmers, C. et al. J. Neurophysiol. 74, 802-815 (1995) 
3. Thickbroom, G.W. et al. Exp Brain Res. 121, 59-64 (1998) 
4. Benwell N. Mastaglia, F.L., Thickbroom, G.W. Exp Brain Res. 175, 626-632 (2006) 
5. Gandevia, S.C. Physiol Rev. 81, 1725-1789 (2001) 
6. Shibuya, K. & Kuboyama, N. Brain Res. 1156, 120-124 (2007) 
7. Shibuya, K. et al. Brain Res. doi:10.1016/j.braires.2008.03009 (2008) 
8. Ward, N.S. and Frackowiak, R.S.J. Brain. 136, 873-888 (2003) 
9. Liu, J.Z. et al. J Neurophysiol. 90, 300-312 (2003) 
10. Newton J.M., Sunderland A., Gowland P.A. NeuroImage. 24, 1080-1087 (2005) 
 
Figure legends 
Figure 1. The peak value in oxygenation changes from resting levels at 40%MVC trials. The 
astarisks are shown the significant difference between the first trials. Upper panels represent the 
results of oxyhemoglobin (HbO2) changes. Lower panels represent the results of deoxyhemoglobin 
(Hb) changes. Right panels represent the results of contralateral primary motor cortex oxygenation 
changes, and left panels represent the results of ipsilateral primary motor cortex oxygenation 
changes. Asterisks show significant differences from the first trial (p < 0.05). Error bars indicate 
s.e.m. 
 
Figure 2. The peak value in oxygenation changes from resting levels at 60%MVC trials. The 
astarisks are shown the significant difference between the first trials. Upper panels represent the 
results of oxyhemoglobin (HbO2) changes. Lower panels represent the results of deoxyhemoglobin 
(Hb) changes. Right panels represent the results of contralateral primary motor cortex oxygenation 
changes, and left panels represent the results of ipsilateral primary motor cortex oxygenation 
changes. Asterisks show significant differences from the first trial (p < 0.05). Error bars indicate 
s.e.m. 
 
-0.02
-0.01
0
0.01
0.02
0.03
1 2 3 4 5
(
m
M
*
c
m
)
Ipsilateral Hb
Trial No.
-0.02
-0.01
0
0.01
0.02
0.03
1 2 3 4 5
(
m
M
*
c
m
)
Ipsilateral HbO2
-0.02
-0.01
0
0.01
0.02
0.03
1 2 3 4 5
(
m
M
*
c
m
)
Trial No.
Contralateral Hb
1 2 3 4 5
-0.02
-0.01
0
0.01
0.02
0.03
(
m
M
*
c
m
)
Contralateral HbO2
n.s.
n.s.
*
**
-0.02
-0.01
0
0.01
0.02
0.03
1 2 3 4 5
(
m
M
*
c
m
)
Trial No.
Contralateral Hb
-0.02
-0.01
0
0.01
0.02
0.03
(
m
M
*
c
m
)
Contralateral HbO2
1 2 3 4 5
-0.02
-0.01
0
0.01
0.02
0.03
1 2 3 4 5
(
m
M
*
c
m
)
Ipsilateral HbO2
-0.02
-0.01
0
0.01
0.02
0.03
1 2 3 4 5
(
m
M
*
c
m
)
Trial No.
Ipsilateral Hb
n.s.
n.s.
*
*
HbO2 Hb
Trial No. Trial No.
1 0.0116 ± 0.0008 0.0140 ± 0.0010 1 -0.0079 ± 0.0005 -0.0124 ± 0.0010
2 0.0143 ± 0.0013 0.0101 ± 0.0010 2 -0.0111 ± 0.0012 -0.0127 ± 0.0009
3 0.0144 ± 0.0008 0.0107 ± 0.0006 3 -0.0101 ± 0.0006 -0.0103 ± 0.0006
4 0.0107 ± 0.0010 0.0070 ± 0.0008 4 -0.0051 ± 0.0005 -0.0039 ± 0.0006 *
5 0.0093 ± 0.0009 0.0029 ± 0.0010 * 5 -0.0054 ± 0.0003 -0.0011 ± 0.0007 *
F =0.798, p = 0.5358 F = 3.154, p = 0.0281 F =2.215, p = 0.0911 F = 6.771, p = 0.0005
There were significant differences between
Trial 1 and 4: t = 3.854, p = 0.0084; and
between Trail 1 and 5: t = 6.429, p =
0.0007
Table 1. The peak value in oxygenation changes from resting levels at 40%MVC trials. The astarisks are shown the significant difference between the first trials. Left panel represents the results of
oxyhemoglobin (HbO2) changes. Right panel represents the results of deoxyhemoglobin (Hb) changes.
Contralateral Ipsilateral Contralateral Ipsilateral
There was a significant difference
between Trial 1 and 5: t = 3.017, p =
0.0235
HbO2 Hb
Trial No. Trial No.
1 0.0173 ± 0.0016 0.0166 ± 0.0010 1 -0.0093 ± 0.0004 -0.0116 ± 0.0005
2 0.0160 ± 0.0012 0.0133 ± 0.0008 2 -0.0107 ± 0.0003 -0.0123 ± 0.0004
3 0.0186 ± 0.0012 0.0160 ± 0.0011 3 -0.0096 ± 0.0006 -0.0121 ± 0.0010
4 0.0171 ± 0.0015 0.0119 ± 0.0006 4 -0.0101 ± 0.0005 -0.0086 ± 0.0004
5 0.0123 ± 0.0015 0.0063 ± 0.0009 * 5 -0.0086 ± 0.0006 -0.0057 ± 0.0005 *
F = 0.403, p = 0.8050 F = 2.929, p = 0.0371 F = 0.405, p = 0.8036 F = 3.057, p = 0.0317
There was a significant difference
between Trial 1 and  5: t = 4.744, p =
0.0032
There was a significant difference between
Trial 1 and 5: t = 2.627, p = 0.0392
Table 2. The peak value in oxygenation changes from resting levels at 60%MVC trials. The astarisks are shown the significant difference between the first trials. Left panel represents the results of
oxyhemoglibin (HbO2) changes. Right panel represents the results of deoxyhemoglibin (Hb) changes.
Contralateral Ipsilateral Contralateral Ipsilateral


Reduced contribution of the ipsilateral primary motor cortex to force modulation with short-term motor learning in humans: An NIRS study

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Reduced contribution of the ipsilateral primary motor cortex to force modulation with short-term motor learning in humans: An NIRS study

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