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Journal of Electromyography and Kinesiology 22 (2012) 74–79

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Journal of Electromyography and Kinesiology


journal homepage: www.elsevier.com/locate/jelekin

Spatial EMG potential distribution pattern of vastus lateralis muscle during


isometric knee extension in young and elderly men
Kohei Watanabe a,b,⇑, Motoki Kouzaki c, Roberto Merletti d, Mami Fujibayashi a,e, Toshio Moritani a
a
Laboratory of Applied Physiology, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
b
Japan Society for the Promotion of Science (JSPS), Kyoto, Japan
c
Laboratory of Neurophysiology, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
d
Laboratorio di Ingegneria del Sistema Neuromuscolare, Dipartimento di Elettronica, Politecnico di Torino, Torino, Italy
e
Division of Physical and Health Education, Setsunan University, Osaka, Japan

a r t i c l e i n f o a b s t r a c t

Article history: The aim of the present study was to compare spatial electromyographic (EMG) potential distribution dur-
Received 1 February 2011 ing force production between elderly and young individuals using multi-channel surface EMG (SEMG).
Received in revised form 20 September Thirteen elderly (72–79 years) and 13 young (21–27 years) healthy male volunteers performed ramp
2011
submaximal contraction during isometric knee extension from 0% to 65% of maximal voluntary contrac-
Accepted 20 September 2011
tion. During contraction, multi-channel EMG was recorded from the vastus lateralis muscle. To evaluate
alteration in heterogeneity and pattern in spatial EMG potential distribution, coefficient of variation
Keywords:
(CoV), modified entropy and correlation coefficients with initial torque level were calculated from
Aging multi-channel SEMG at 5% force increment. Increase in CoV and decrease in modified entropy of RMS
Multi-channel surface electromyography with increase of exerted torque were significantly smaller in elderly group (p < 0.05) and correlation coef-
Knee extensor ficients with initial torque level were significantly higher in elderly group than in young group at mod-
erate torque levels (p < 0.05). These data suggest that the increase of heterogeneity and the change in the
activation pattern are smaller in elderly individuals than in young individuals. We speculated that multi-
channel SEMG pattern in elderly individual reflects neuromuscular activation strategy regulated predom-
inantly by clustering of similar type of muscle fibers in aged muscle.
Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Recently, multichannel surface EMG (multi-channel SEMG)


technique is developing as methodology to estimate MU behavior
Muscular weakness in elderly people has been explained by in the large area of a muscle during force production (Farina
age-related morphological change in skeletal muscle, e.g. decline et al., 2008; Holtermann et al., 2008; Holtermann and Roeleveld,
of muscle mass (Deschenes, 2004; Lang et al., 2010; Thompson, 2006; Merletti et al., 2008). The previous studies using multi-chan-
2009). On the other hand, the underlying physiological mecha- nel SEMG reported that spatial activation distribution in a muscle
nisms in aged-neuromuscular system have yet to be fully under- is non-uniform and spatial EMG potential distribution pattern is al-
stood. The muscular force production is determined by for tered by contraction levels or fatigue. These phenomenon would be
recruitment of motor unit (MU) and firing rate of recruited MUs. explained by a spatial inhomogeneity in the location of different
Previous studies investigated the behavior of MU in order to clarify types of muscle fibers (Buchthal et al., 1957; Chanaud and Macph-
the age related neuromuscular system during force production erson, 1991) and a clustering of muscle fiber innervated by one MU
(Kamen, 2005; Roos et al., 1997). However, these knowledge are in limited territory (Lexell et al., 1986; Lexell and Downham, 1991;
provided from a very small portion of the muscle using intramus- Sjostrom et al., 1986). The previous studies by Holtermann and
cular electromyography (EMG) technique (Nelson et al., 1983; Roos Roeleveld (2006), Holtermann et al. (2005), (2009) demonstrated
et al., 1999; Welsh et al., 2007). The invasiveness could be also one that alteration of spatial distribution of multi-channel SEMG can
of the issues of this technique in order to apply to elderly people be explained by physiological phenomena of MU recruitment and
and other wide population. suggested that spatial distribution of multi-channel SEMG could
be used to study changes in MU recruitment. While this technique
⇑ Corresponding author at: Laboratory of Applied Physiology, Graduate School of
is indirect way to assess MU behavior, multi-channel SEMG can
Human and Environmental Studies, Kyoto University, Yoshidanihonmatsucho,
Sakyo, Kyoto 606-8501, Japan. Tel./fax: +81 75 753 2878.
non-invasively investigate MU activation in a large area of a mus-
E-mail address: watanabe.kohei@aw7.ecs.kyoto-u.ac.jp (K. Watanabe). cle during force production at low to high force level.

1050-6411/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jelekin.2011.09.010
K. Watanabe et al. / Journal of Electromyography and Kinesiology 22 (2012) 74–79 75

In this study, we aimed to compare spatial EMG potential distri- 2.3. EMG recording
bution during force production between elderly and young individ-
uals using multi-channel SEMG. In aged-skeletal muscle, number Multi-channel SEMG signals were detected from the VL muscle
of MU decreases, innervation ratio increases caused by motor unit with a semi-disposable adhesive grid of 64 electrodes (ELS-
remodeling and this MU remodeling is generally altered such that CH064R3S, OT Bioelectronica, Torino, Italy). The grid is made of 13
fast type fibers are selectively denervated and reinnervated by ax- rows and 5 columns of electrodes (1 mm diameter, 8 mm inter-elec-
ons from slow type MU (Deschenes, 2004; Lang et al., 2010). These trode distance in both directions) with one missing electrode at the
morphological changes would induce that the large area is occu- upper left corner. Prior to attaching the electrode grid, the skin was
pied by similar type of MUs (muscle fibers) such as clustering (Lex- shaved, abraded and cleaned with alcohol. Conductive gels were in-
ell et al., 1986; Lexell and Downham, 1991; Sjostrom et al., 1986). serted into the cavities of the grid electrode to assure proper elec-
We expected that clustering of similar type of MUs (muscle fibers) trode skin contact. The center of electrode grid was placed at mid-
are reflected as low heterogeneity and small change in spatial EMG point of the line between the head of great trochanter and inferior
potential distribution with increase of force level in elderly individ- lateral edge of patella. The rows of electrodes were placed along
uals as compared with young individuals. In this study, the vastus the longitudinal axis of VL muscle such as the line between the head
lateralis (VL) muscle in the quadriceps femoris (QF) muscle group of great trochanter and inferior lateral edge of patella. The position of
was used since the QF muscle group has been focused on most missing electrode was located at proximal side of longitudinal axis
aging study (Knight and Kamen, 2008; Roos et al., 1999; Young of VL muscle. The grid electrode was connected to the amplifier
et al., 1984, 1985) and the effect of task dependent artifact on through four connectors which were fixed at the subject skin by
EMG potential distribution could be minimized as the VL is a elastic tape. A reference electrode was placed at the iliac crest. At
mono-articular muscle. the center of electrode location, longitudinal ultrasonographic im-
age (SSD-900, ALOKA, Tokyo, Japan) were taken to determine the
thickness of the subcutaneous tissue and VL muscle.
2. Materials and methods
Monopolar EMG signals were amplified by a factor of 1000,
sampled at 2048 Hz and converted to digital form by a 12-bit ana-
2.1. Subjects
log-to-digital converter (EMG-USB, OT Bioelectronica, Torino, Italy)
with the signal of force transducer. Recorded monopolar surface
Thirteen elderly men (age: 72–79 years, height: 164.0 ± 3.2 cm,
EMG signals were off-line band-pass filtered (10–500 Hz) and
body mass: 58.7 ± 5.4 kg) and 13 young men (age: 21–27 years,
transferred into analysis software (MATLAB 7, MathWorks GK, To-
height: 172.0 ± 7.3 cm, body mass: 65.2 ± 6.6 kg) volunteered for
kyo, Japan). Fifty-nine bipolar surface EMG signals along the rows
this experiment. They gave written informed consent for the study
were made from 64 electrodes. To calculate root mean square
after receiving a detailed explanation of the purposes, potential
(RMS), EMG signals were sampled over 1 s at 5% increment from
benefits, and risks associated with participation in the study. All
20% to 80% of MVC ramp contraction. Since performed ramp rate
subjects were healthy with no history of any neurological disor-
was 10% of the MVC force/1 s of sampled signals were overlapped
ders, and their vision corrected to normal levels with corrective
by 0.5 s between neighboring contraction levels.
lenses. All procedures used in this study were in accordance with
To characterize heterogeneity in spatial EMG potential distribu-
the Declaration of Helsinki and were approved by the Committee
tion at individual torque levels, coefficient of variation (CoV) and
for Human Experimentation at the Graduate School of Human
modified entropy were used in the present study. CoV was defined
and Environmental Studies, Kyoto University.
as quotient of standard deviation among 59 RMS and averaged va-
lue of 59 RMS at a torque level. Modified entropy of the spatial dis-
2.2. Experimental design tribution of EMG amplitude was calculated for 59 RMS values (in
space) of single differential signals computed over a 1 s epoch ta-
The subjects performed maximal voluntary contractions (MVC) ken at 20%, 25%, . . ., 75%, 80% of MVC during the ramp contraction.
and ramp submaximal contraction during isometric knee exten- As done by Farina et al. (2008) in a previous work, modified entro-
sion. During submaximal contraction, multi-channel SEMG was re- py was defined as entropy of the signal power, that is
corded from VL muscle. X59
E¼ pðiÞ2 log2 pðiÞ2
Isometric knee extensions were performed on a custom dyna- i¼1

mometer mounted force transducer (LU-100KSE; Kyowa Electronic where p(i) is the square of the RMS value of channel i divided by the
Instruments, Tokyo, Japan). During contraction, both hip and knee sum of the squares of all the 59 RMS values, at the given force level.
joint angles were flexed at 90° (180° is fully extended), respectively. Therefore p(i)2 represents the normalized power of each channel. It
The MVC involved a gradual increase in knee extension force exerted is E = 0 when all the p(i) are zero except one and is maximal and
by the knee extensor muscles from baseline to maximum in 2–3 s equal to log2 59 = 5.884 when the p(i) values are identical and equal
and then sustained at maximum for 2 s (Watanabe and Akima, to 1/59 (all channels have the same energy). Increase in CoV and de-
2009). The timing of the task was based on a verbal count given at crease in modified entropy, respectively, mean that increase of het-
a 1-s interval, with vigorous encouragement from the investigators erogeneity in spatial EMG potential distribution within an electrode
when the force began to plateau. The subjects performed at least two grid.
MVC trials with P2 min rest between trials. The highest MVC force Correlation coefficients were calculated from the 59 pairs of RMS
was used to calculate the MVC torque and target torque for ramp values at the same regions between 20% of MVC and those of all
submaximal contraction. Knee extension torque was calculated as other torque levels to compare the spatial EMG potential distribu-
the product of the knee extension force and length between the esti- tion pattern. Decrease of correlation coefficient indicates change in
mated knee joint center and the distal portion of the shank linked to spatial EMG potential distribution pattern. In the present study,
force transducer. After MVC, the ramp submaximal contraction from MU recruitment strategy was estimated from these three variables.
0% to 80% of the MVC force with approximately 10% of the MVC
force/1 s of ramp rate was performed. The produced and target tor- 2.4. Statistics
ques were shown to the subjects on a personal computer monitor.
Subjects practiced MVC and ramp submaximal contraction All data are provided as mean and SD. Before the analysis, the
P10 min before test session. normal distribution of the data was confirmed using Shapiro–Wilk
76 K. Watanabe et al. / Journal of Electromyography and Kinesiology 22 (2012) 74–79

test. The parametric analysis was used for normally distributed smaller in elderly than in young men and (3) correlation coeffi-
data and the non-parametric analysis was used for non-normally cients with initial torque level were higher in elderly than in young
distributed data. MVC torques and thickness of subcutaneous tis- men at moderate torque levels. These results demonstrate that the
sue and VL muscle between groups was compared using t-test. heterogeneity and change of pattern in spatial EMG potential dis-
CoV and modified entropy of RMS were analyzed using two-way tribution of VL are smaller in elderly individuals than in young
(group  torque) analysis of variance (ANOVA) with repeated mea- individuals during ramp submaximal isometric contraction.
sures. In the case of two-factor interaction, the analysis was broken In the present study, high absolute value in SEMG amplitude
into t-test at each torque level to compare the value between el- was found in young men comparing with elderly men (Fig. 1). In
derly and young groups. One-way ANOVA with repeated measures addition to physiological factors, it is well known that non-physi-
was also applied to CoV and modified entropy of RMS for each ological factors, i.e. anatomy, detection system, geometry and so
group. Normal distribution and homogeneity of variance for ana- on, also affect SEMG variables (Farina et al., 2004). The anatomical
lyzed data were confirmed for two-way ANOVA and t-test, respec- properties were considered as the main non-physiological factors
tively. Correlation coefficient was analyzed using Friedman test for inducing the difference in SEMG amplitude between the groups.
each group and using Mann–Whitney U-test at each torque level to While the thickness of subcutaneous tissue was not significantly
compare the value between elderly and young groups. The level of different between the groups, greater thickness of VL muscle was
statistical significance was set at p < 0.05. Statistical analyses were obtained in young men. This difference in muscle thickness would
performed using SPSS software (version 15.0; SPSS, Tokyo, Japan). reflect age-related morphological changes in the skeletal muscle,
i.e. muscle fiber atrophy and decrease in number of fibers and mo-
3. Results tor units (Deschenes, 2004; Lang et al., 2010; Lexell et al., 1986;
Lexell and Downham, 1991; Sjostrom et al., 1986). These morpho-
MVC torque was significantly different between elderly logical changes could be one of the causes of lower value of EMG
(104.4 ± 9.7 N m) and young men (188.6 ± 25.4 N m) (p < 0.05). amplitude in elderly men.
There was no significant difference in thickness of subcutaneous tis- In the present study, some subjects couldn’t control or raise
sue between the groups (0.58 ± 0.18 cm for elderly men and their force to target force at high force level (>65% MVC). It could
0.54 ± 0.20 cm for young men). Thickness of VL muscle was signifi- be speculated that muscle fatigue might have occurred during
cantly greater in young men (2.72 ± 0.32 cm) comparing with el- the given task and induced task failure. However, previous studies
derly men (1.67 ± 0.28 cm) (p < 0.05). reported that young men could keep the sustained isometric force
All subjects could perform until 65% of MVC during the ramp con- for 30–70 s at moderate to high force level (50–80% of MVC) during
traction. The RMSs of multi-channel SEMG from 20% to 65% of MVC knee extension (Ebenbichler et al., 1998; Smolander et al., 1998;
were analyzed. Fig. 1 illustrates representative multi-channel SEMG Watanabe and Akima, 2010). Since duration was 10 s in our ramp
amplitude shown as color maps and the calculated parameters of contraction, we supposed that the main cause of task failure was
multi-channel SEMG amplitude at selected torque level for elderly not induced by muscle fatigue, but induced by difficulty to control
and young men. As compared to young men, similar amplitude force at high force level. Also, Sbriccoli et al. (2003) showed that
intensity area is larger in elderly men at high torque levels (50– the speed of isometric contractions (ramp rate) strongly influenced
65% MVC), reflecting lower CoV of amplitude and higher modified SEMG responses during a ramp contraction using elbow flexor
entropy in elderly men at high torque levels. With increase of ex- muscle (Sbriccoli et al., 2003). Although time or peak force level
erted torque, alteration of distribution was mainly seen in color, was different among the subjects in the present study, ramp rate
but not in pattern in elderly men, while alteration of distribution was controlled during our ramp contraction. We, thus, could as-
was seen in both color and pattern in young men. These alterations sume that the effect of isometric contraction speed could be min-
of spatial EMG potential distribution were reflected as decrease of imized in our results.
correlation coefficient value with increase of contraction level in el- The increase of CoV and decrease of modified entropy of multi-
derly men and small change of that in young men. channel SEMG were demonstrated in both elderly and young men
Significant group-by-torque interactions were seen for CoV and with torque development (Figs. 2 and 3). To our knowledge, this is
modified entropy of RMS (p < 0.05) (Figs. 2 and 3). There was no the first attempt to quantify the heterogeneity in spatial EMG poten-
significant difference between elderly and young groups for CoV tial distribution at various torque levels in knee extensor muscle.
of RMS at each torque level (Fig. 2). Modified entropy at 65% of Such heterogeneity in spatial activation distribution of multi-chan-
MVC was significantly larger in elderly group than in young group nel SEMG means variation of surface EMG amplitudes among chan-
(p < 0.05) (Fig. 3). CoV and modified entropy of RMS in both groups nels. Different types of MUs (muscle fibers) are inhomogeneously
were significantly increased and decreased, respectively, with in- located within a muscle (Buchthal et al., 1957; Chanaud and Macph-
crease of exerted torque (p < 0.05) (Figs. 2 and 3). erson, 1991) and MUs are newly recruited as force increases in
Correlation coefficients between RMSs at 20% of MVC and those accordance with the size principle (Henneman et al., 1965). On the
at other torque level for both elderly and young groups were signif- other hand, change of firing rate of recruited MUs is also considered
icantly decreased with increase of exerted torque (p < 0.05) (Fig. 4). as one of the causes for change in spatial activation distribution.
At 40%, 45% and 50% of MVC, correlation coefficients in elderly However, since an almost equal change in firing rate with force level
group were significantly higher than in young group (p < 0.05). among different MUs was reported during intermediate force level
(De Luca and Hostage, 2010; Erim et al., 1996), it was expected that
4. Discussion recruitment of MUs could become a major cause for the change in
spatial distribution of multi-channel SEMG that has been observed
The present study compared the spatial EMG potential distribu- in the present study.
tion during knee extension between elderly and young individuals Correlation analysis is also used to assess changes in spatial
using multi-channel SEMG. The primary results of the present EMG potential distribution. Holtermann et al. (2005) reported that
study were that: (1) changes in CoV of RMS, the modified entropy correlation coefficient of multi-channel SEMG decreased with in-
of RMS and in the correlation coefficient between RMSs at initial crease of performed force during ramp isometric contraction in bi-
torque level and other torque levels were found in both groups ceps brachii muscle (Holtermann et al., 2005). This finding suggests
in relation to exerted torque, (2) increase in CoV and decrease in that spatial EMG potential distribution changes with alteration of
modified entropy of RMS with increase of exerted torque were exerted force. Moreover, they showed that alteration pattern of
K. Watanabe et al. / Journal of Electromyography and Kinesiology 22 (2012) 74–79 77

Fig. 1. Representative multi-channel surface electromyography amplitude shown as color maps and the calculated parameters of multi-channel SEMG amplitude at selected
torque level for elderly and young individuals. (A) The scales are different between two examples because of difference in absolute values of EMG amplitude. (B)
Representative multi-channel surface electromyography amplitude shown as color maps normalized by the values at 20% of MVC for visual purpose. These color maps were
obtained by differential surface electromyography signals by using 13 rows and 5 columns of electrodes with 8 mm inter-electrode distance.

of MUs was reported (Holtermann et al., 2005), the correlation


coefficient of multi-channel SEMG could be reasonably used to
estimate recruitment of global MUs during force production. De-
crease of correlation coefficient of multi-channel SEMG calculated
with respect to a reference force level (20% of MVC) with increase
in torque level was seen in the present study (Fig. 4). Our result of
correlation coefficient of multi-channel SEMG in VL is in agreement
with that in the biceps brachii muscle obtained by Holtermann and
Roeleveld (2006). In addition to CoV and modified entropy of mul-
ti-channel SEMG, correlation coefficient of multi-channel SEMG
with respect to a reference force level could also reflect different
MU recruitment strategies with increase of exerted torque (Holter-
Fig. 2. Coefficient of variation in amplitude of multi-channel surface electromyog-
raphy during ramp contraction in elderly and young individuals. mann et al., 2005).
The present study demonstrated the different pattern of CoV
correlation coefficients during ascending and descending phases and modified entropy with increase of exerted torque intensity
during ramp contraction was not the same (Holtermann et al., during knee extension in relation to exerted torque between el-
2005). Since a deviation between recruitment and derecruitment derly and young men. The CoV was lower in elderly than in young
78 K. Watanabe et al. / Journal of Electromyography and Kinesiology 22 (2012) 74–79

5. Conclusion

We compared spatial EMG potential distribution during force


production between elderly and young individuals using multi-
channel SEMG. The present study indicated that increase of hetero-
geneity and change of pattern in spatial EMG potential distribution
with increase of exerted torque level are smaller in elderly individ-
uals than in young individuals during submaximal isometric con-
traction in VL muscle. We concluded that multi-channel SEMG
pattern of elderly individual reflects neuromuscular activation reg-
ulated predominantly by rate coding of MU and clustering of similar
type of muscle fiber in aged muscle.

Acknowledgements
Fig. 3. Modified entropy in amplitude of multi-channel surface electromyography
during ramp contraction in elderly and young individuals. ⁄p < 0.05 vs. young group.
This research was supported in part by a Grant-Aid for Japan Soci-
ety for the Promotion of Science (No. 22-1944). The authors are sin-
cerely grateful to Mr. Andrea Bottin (OT-Bioengineering, Italy) and
to the Researchers of LISiN (Politecnico di Torino, Italy) for the sup-
port in the use of multi-channel surface electromyography system
(electrode and amplifier). The authors thank Mr. Masanori Ozaki,
Mr. Atsushi Kawakami and Mr. Go Sakamoto of our laboratory for
help with measuring and analyzing surface electromyography. We
acknowledge Prof. Misaka Kimura of Kyoto Prefectual University
of Medicine for helpful suggestions.

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Kohei Watanabe received M.S. degree from Nippon Toshio Moritani was born in Japan in 1950. He
Sports Science University in 2007 and the Ph.D. received his Ph.D. degree in sports medicine from
degree from Nagoya University in 2010. Since 2010, the University of Southern California in 1980 under
he is working at Laboratory of Applied Physiology, the direction of Dr. Herbert A. deVries. In 1985,
Graduate School of Human and Environmental following faculty appointments at the University of
Studies, Kyoto University. as a Postdoctoral Texas at Arlington and Texas A&M University, he
researcher of Japan Society for the Promotion of Sci- returned to Japan and joined the Department of
ence. In 2011, he was also working at Laboratory for Integrated Human Studies at Kyoto University. In
Engineering of the Neuromuscular System (LISiN) of 1992, he was appointed as associate professor of
Ploitecnico di Torino, Italy, as a visiting researcher. Applied Physiology at the Graduate School of
His research interests are neuromuscular function Human and Environmental Studies at Kyoto Uni-
during movement and exercise in human and versity and became professor since 2000. He is
assessment of neuromuscular function for lifestyle currently director of the Laboratory of Applied
disease patients and elderly people during exercise. Physiology. Dr. Moritani has been elected as fellow
of the American College of Sports Medicine. Dr. Moritani is the editor of the
Journal of Electromyography and Kinesiology and European Journal of Applied
Motoki Kouzaki received his Ph.D. degree in 1999 Physiology. He has also served as one of the council members and the president of
from the Department of Life Science, The University of the International Society of Electrophysiology and Kinesiology.
Tokyo, Tokyo, Japan. From 1999 to 2007, he was an
assistant professor of the Department of Life Science,
The University of Tokyo, Tokyo, Japan. In 2007, he was
appointed as an associate professor of the Graduate
School of Human and Environmental Studies, Kyoto
University, Kyoto, Japan, where he is currently director
of the Laboratory of Neurophysiology. His major
research interests focus on neural mechanisms
underlying human motor control as related to muscle
fatigue, especially ‘‘alternate muscle activity of syn-
ergistic muscles’’.

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