Vol. 93, Issue 5, 1744-1752, November 2002
Characteristics of surface mechanomyogram are dependent on
development of fusion of motor units in humans
Yasuhide
Yoshitake1,
Minoru
Shinohara2,
Hidetoshi
Ue1, and
Toshio
Moritani1
1 Laboratory of Applied Physiology, Graduate School
of Human and Environmental Studies, Kyoto University, Sakyo-ku,
Kyoto 606-8501, Japan; and 2 Department of
Kinesiology, The Pennsylvania State University, University Park,
Pennsylvania 16802
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ABSTRACT |
The purpose of this study
was to test whether surface mechanomyogram (MMG) recorded on the skin
reflects the contractile properties of individual motor units in
humans. Eight motor units in the medial gastrocnemius muscle were
identified, and trains of stimulation at 5, 10, 15, and 20 Hz were
delivered to each isolated motor unit. There was a significant positive
correlation between the duration of MMG and twitch duration. MMG
amplitude decreased with increasing stimulation frequency. Reductions
in MMG amplitude were in parallel with the reductions in force
fluctuations, and the rate of change in both was positively correlated
across the motor units. Rate of change in MMG amplitude against force
was negatively correlated to half relaxation time and twitch duration. Similar negative correlations were found between force fluctuations and
contractile properties. These results provide evidence supporting a
direct relation between MMG and contractile properties of individual motor units within the gastrocnemius muscle, indicating that surface MMG is dependent on the contractile properties of the activated motor
units in humans.
intramuscular microstimulation; force fluctuation; contractile
property
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INTRODUCTION |
THE MECHANOMYOGRAM
(MMG) is a recording of the pressure wave produced by lateral expansion
of a number of muscle fibers (22). In vitro
studies using simple evoked contractions in frog muscles provide
evidence that the vibratory signal from the muscle is an expression of
the mechanical behavior of the muscle mass, although the main source of
the MMG signal is motor unit activity (2, 12). A
similar vibratory signal can be recorded easily from the surface of the
skin in humans as a muscle contracts (surface MMG) (22),
and it is expected that this technique will prove useful for
investigating mechanical characteristics of muscle in the fields of
physiology, clinical medicine, and rehabilitation. Surface MMG should
prove useful if it is possible to ascertain the contributions of
isolated motor units to the surface recording in human muscle. As has
been extensively studied in the surface electromyogram (EMG), however,
surface MMG is the sum of the signals emitted from a number of
activated motor units, mediated and modulated by the architecture of
the muscle-tendon complex, fat, and skin. To elucidate mechanical
characteristics of the muscle from the recorded surface MMG, it is
critical to determine how contractile properties and activation
characteristics of individual motor units contribute to the surface MMG.
Studies conducted on the gastrocnemius muscle of rats
(5-7) and cats (23, 24, 28) have
examined the contributions of isolated motor units to the surface MMG
signals under well-controlled conditions. Bichler and colleagues
(5-7), for example, investigated isolated motor units
within the same muscles in vivo, and the contractile properties of the
motor units were identified. The amplitude of MMG during repetitive
stimulation of isolated motor units was shown to be associated with the
amplitude of force oscillation (6, 7). Similar results
were also obtained by Orizio et al. (23) in studies
examining the medial gastrocnemius muscle of cats in situ. Therefore,
evidence exists in mammals that isolated motor units contribute
significantly to the surface MMG signal.
In contrast to the research in mammals, there is little evidence
supporting a close relation between surface MMG of the whole muscle and
contractile properties and activation characteristics of the involved
motor units in humans. In maximal twitch contractions evoked by direct
whole muscle stimulation, the rising time of MMG (from the onset to the
highest peak) was shown to be very similar to the contraction time of
the single-twitch force, and it was found to be longer in the soleus
muscle than in the vastus lateralis muscle (15). In
studies using voluntary contractions, MMG from the soleus muscle
contained an increased percentage of low frequencies compared with the
biceps brachii muscles (18). Additionally, distinct
responses to the increasing force level are observed in the amplitude
of surface MMG between the soleus and medial gastrocnemius muscle
(35). It has been further speculated that different
contractile properties of motor units, in particular the speed of
contraction and relaxation, may affect the development of fusion in
relation to the contractile properties and discharge rate of motor
units, thus affecting the amplitude of surface MMG (35).
In these studies, the response of surface MMG from different muscles
was interpreted with the presumption of the following fiber-type
compositions: soleus contains the greatest abundance of slow fibers,
followed by vastus lateralis (15), biceps brachii (18), and gastrocnemius (35). However, the
contractile properties of the involved motor units were not examined.
This kind of design is incomplete because it cannot discriminate the
possible substantial effects due to slight differences in the setup of
the sensor or the architecture of the muscle-tendon complex, fat, and
skin (22).
We hypothesized that the characteristics of surface MMG from the whole
muscle in humans are largely dependent on the contractile properties of
the activated motor units, especially on those features influencing the
development of fusion (how fusion is developed in relation to
contractile properties and stimulation frequency). This is based on the
findings that fusion is developed at lower stimulation frequencies in
slow-twitch fibers compared with fast-twitch fibers (10,
31). Thus far, there is no direct evidence to support this
hypothesis because previous studies do not identify motor unit activity
in vivo (2, 12), were conducted on isolated motor units in
other mammals than humans (5-7, 23, 24, 28), or were
limited to the comparison between different muscles in humans
(15, 18, 35). To test this hypothesis, we compared, in
humans, the responses in surface MMG with the controlled intramuscular microstimulation of isolated motor units that belong to the same muscle
with a wide range of contractile properties. With the intramuscular microstimulation technique, individual motor units can be isolated and
the contractile properties of the stimulated motor units can be
identified with regard to contraction time, half relaxation time, and
development of fusion (13), thus allowing an accurate assessment of the contribution of individual motor units to the surface
MMG in humans.
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METHODS |
Subjects.
Eight isolated motor units were studied from the medial gastrocnemius
muscle of four healthy male subjects. Their age, height, and body mass
were 25.8 ± 0.4 (SE) yr, 177.2 ± 2.5 cm, and
68.3 ± 1.9 kg, respectively. The subjects had no medical history
or physical signs of neuromuscular disorder. After subjects were fully
informed about the nature of the experiment and possible risks
involved, written informed consent was obtained from each subject. The
protocol was in accordance with the criterion of the ethics committee
review board of Kyoto University.
Experimental setup.
Each subject was seated on an insulated, straight-back chair with wide
belts crossing the chest and abdomen that tightly immobilized the body.
An additional strap was used to secure the thigh to the chair. Force
was measured with a strain-gauge transducer (model TB-654T, Nihon
Kohden, Tokyo, Japan) positioned between a metal baseplate and a foot
lever plate (Fig. 1). The bottom
end of the foot lever plate had a semicircular attachment that
surrounded and secured the heel. The heel was also secured with a strap
at the bottom end of the foot lever plate. The strain-gauge
transducer was aligned between the two plates near the distal part of
the foot. The exact position of the entire device was carefully
adjusted so that the knee was fully extended with the ankle joint angle at 100°.
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Fig. 1.
Schematic diagram of the experimental setup. A
strain-gauge transducer for the force measurement, a microphone for
surface mechanomyogram (MMG), electrodes for surface electromyogram
(EMG), and wire electrodes for the intramuscular microstimulation from
an electrostimulator through an isolator are shown. Force, MMG, and EMG
signals were amplified and stored on a personal computer via an
analog-to-digital (A/D) converter. AC, alternating current; DC, direct
current.
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Force, EMG, and MMG recordings.
The strain-gauge transducer measured the isometric plantar flexion
force elicited by the electrical stimulations. The force signal was
amplified through a direct-current (DC) amplifier (bandwidth: DC to 128 Hz; model SA-100, TEAC, Tokyo, Japan), and the system operated linearly
between 0 and 9.8 N. Surface EMG was recorded with bipolar
silver-silver chloride electrodes (9-mm diameter, 35-mm interelectrode
distance) filled with conducting jelly that were applied over the belly
of the medial gastrocnemius muscle. Electrode placement was preceded by
abrasion of the skin surface to reduce the source impedance to 3 k
.
The signals were band-pass filtered (5-1,000 Hz) and
differentially amplified (model MEG-6100, Nihon Kohden; gain: ×1,000,
input impedance: >100 M, common mode rejection ratio: >80 dB)
before recording. The method for measuring MMG signals was similar to
methods previously employed in our laboratory (35, 36).
The MMG was detected by an electret condenser microphone that was
designed for research purposes (Daia Medical, Tokyo, Japan).
The basic technique for detecting sound by this particular microphone
is not different from other popular electret condenser microphones that
are commercially available. Transverse mechanical activity of a muscle
is transmitted to a thin diaphragm as it oscillates through an air
column. The microphone is relatively small (10-mm diameter and 5-g
mass), and it has a flat-frequency bandwidth between 3 and 2,000 Hz.
The microphone was attached with adhesive tape over the belly of the
medial gastrocnemius muscle between the electrodes for EMG measurement.
The MMG signals were band-pass filtered (1-500 Hz) and amplified
(model MEG-6100, Nihon Koden). The MMG, EMG, and force signals were
displayed on a 20-MHz digital oscilloscope (model 5020A, Kikusui,
Yokohama, Japan) and stored on a personal computer at a sampling rate
of 2,048 Hz via an analog-to-digital converter (13-bit; TransEra 410, i2net, Tokyo, Japan).
Stimulation procedures.
Two sets of fine-wire bipolar electrodes (stainless steel, 100-µm
diameter, 5-µm uninsulated area, ~200-µm interelectrode distance)
were inserted into the medial gastrocnemius muscle ~1.5-2.0 cm
under the skin surface located directly beneath the MMG microphone sensor. Single rectangular electrical pulse waves of 0.5-ms duration were delivered from an electrostimulator (model SEN-7203, Nihon Koden)
through a stimulator isolation unit (model SS 102J, Nihon Koden). To
verify that only single motor units were stimulated, the position of
the intramuscular fine-wire electrodes and the intensity of the
stimulus (1-10 V) were carefully adjusted until reproducible
all-or-nothing responses were acquired in both signals of EMG and
force, simultaneously. The evoked EMG responses were monitored
continuously to ensure that the same motor unit was stimulated
throughout. Any trials with irregular EMG responses were rejected
on-line.
Electrical stimulation and analyses of the data.
First, each motor unit was identified by measuring its mechanical
properties during single-twitch contractions. The EMG, MMG, and force
signals were averaged from 10 single-twitch contractions for each motor
unit. Figure 2 shows examples of the
averaged EMG, MMG, and force signals from two motor units that
exhibited distinctively different mechanical properties. Peak twitch
force, contraction time, and half relaxation time were calculated from
the averaged force signals by following the methods of our
laboratory's previous studies (19, 35).
Contraction time was the time interval between the onset of force and
the peak force. The onset of force was defined as the point at which
the value exceeded three standard deviations of the baseline noise for
three consecutive sampled points. Half relaxation time was defined as
the time taken for the force to decline to one-half of the peak force
value in the relaxation phase. Half relaxation time was employed for
twitch force because it is a standard method to characterize the
relaxation phase of motor units. As a measure of twitch contraction
duration, contraction time and half relaxation time were summed and
termed as "twitch duration" according to its usage in a previous
study (8).
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Fig. 2.
Examples of the surface EMG (A), MMG (B), and
force (C) signals averaged for 10 single twitches of a motor
unit. For comparison, data from a motor unit with the shortest twitch
duration (163.2 ms, MU 1; left) and with the longest twitch
duration (220.6 ms, MU 8; right) are shown. Onset of EMG
corresponds to 0 ms on x-axis.
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MMG duration was measured in the following way from the averaged MMG
signals. The MMG duration was defined as the interval between the onset
and end of MMG signals produced by single-twitch contractions. In
contrast to the analysis of twitch force, the end of MMG signals was
employed because the MMG signals do not necessarily decrease
monotonically after the peak. In this study, the end of MMG signals was
defined as the point at which the rectified MMG declined to three
standard deviations of the baseline noise for three consecutive sampled
points. Similar to the methods used for force signals, the onset of MMG
signals was also defined as the point at which the value exceeded three
standard deviations of the baseline noise for three consecutive sampled points.
Second, each individual motor unit was stimulated at 5, 10, 15, and 20 Hz. To exclude the trials that involved stimulation of surrounding
motor units, evoked mass action potentials (M wave) were examined to
determine whether they remained constant. Each stimulus lasted ~6 s
with a 10-min rest period between frequencies to avoid fatigue. Mean
force was calculated from the middle 2-s segment of the signal. For
further analysis of the force signals, both the DC component and linear
trend of the force signals were eliminated by digital filtering to
exclude transient responses (filtered force). From these signals,
peak-to-peak amplitude of the MMG signals (MMG amplitude) and force
signals (force fluctuations) were measured. For further analysis, the
obtained MMG amplitude and force fluctuations were then normalized to
the respective maximal values in each individual motor unit. Also,
frequency analysis (4,096 points, Hamming window, fast Fourier
transform) of the filtered force and corresponding MMG signals was
performed over the same 2-s window to obtain the mean power frequency
as in our laboratory's previous studies (20, 35). The
mean power frequency was defined as the ratio between spectral moments
of orders one and zero (20). The mean power frequency of
MMG and force was analyzed to confirm whether their responses matched the stimulation frequency.
Statistics.
Descriptive statistics include mean and SE. Statistical analyses were
made by using linear correlation coefficients (Bravais-Pearson's r). All values are expressed as means ± SE
throughout the text, figures, and table. A probability level
of P < 0.05 was considered to be statistically significant.
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RESULTS |
Single-twitch contractions.
The investigated motor units possessed a wide range of contractile
properties with regard to twitch force, contraction time, half
relaxation time, and twitch duration (Table
1). The MMG duration also varied over a
wide range. The differences in the contractile properties of the motor
units and the corresponding surface MMG signals were obvious when the
signals of the two motor units with the shortest and longest twitch
duration were compared (Fig. 2). As can readily be seen, the MMG signal
lasted for the full duration of the force twitch. The waveforms were
not similar to those measured by accelerometers in which the MMG signal
was rarely observed during relaxation phase (3, 4, 25).
But the waveforms of the present study were similar to those usually obtained by electret condenser microphones (29) or
piezoelectric microphones (5). The relations between MMG
duration and contraction time, half relaxation time, and twitch
duration of all the motor units are reported in Fig.
3. MMG duration was strongly correlated with half relaxation time and twitch duration, but it was not related
to contraction time.
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Fig. 3.
Relationships between MMG duration and contraction time
(A), half relaxation time (B), and twitch
duration (C) of all the motor units (n = 8).
NS, not significant.
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Repetitive contractions.
In repetitive contractions, the characteristics of MMG and force
signals varied, whereas the mean power frequency of MMG and force
oscillations approximately matched the stimulation frequency, in all
the motor units. The r values were 0.953 (P < 0.001) between mean power frequency of MMG and stimulation frequency
and 0.980 (P < 0.001) between mean power frequency of
force and stimulation frequency.
Figure 4 shows two examples of surface
MMG and force signals during repetitive stimulations of a motor unit
with different stimulation frequencies. DC components of the force
signals are removed as described in METHODS, and the motor
units with the shortest and longest twitch duration correspond to the
two motor units in Fig. 2. In both of the motor units,
systematic reductions in the MMG amplitude and force fluctuations were
observed concomitantly as the stimulation frequency increased. When the
MMG amplitude and force fluctuations were normalized with respect to
the maximal values for each individual motor unit, the MMG amplitude
appeared to decline linearly in relation to the decrease in force
fluctuations as the stimulation frequency increased (Fig.
5A). The change in the MMG
amplitude was most pronounced when the stimulation frequency increased
from 5 to 10 Hz, where a highly significant correlation was exhibited
between the changes in the MMG amplitude and force fluctuations (Fig.
5B). These results indicate that the changes in the
amplitude of surface MMG signals are significantly related to how
fusion is developed in relation to the contractile properties of the
activated motor units and stimulation frequency.
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Fig. 4.
Examples of the surface MMG signals and filtered force (DC
component and linear trend were eliminated) during repetitive
stimulation of a motor unit at 5, 10, 15, and 20 Hz. MU 1 (top) and MU 8 (bottom) correspond to those in
Fig. 2.
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Fig. 5.
A: relationship between the amplitude of MMG and force
fluctuations with different stimulation frequencies. Data are
normalized to the maximal values of each measurement. Values are
means ± SE. B: correlation for relative changes
between the amplitude of MMG and force fluctuations in individual motor
units (n = 8) by the increase in the stimulation
frequency from 5 to 10 Hz.
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In addition, in the two motor units shown in Fig. 4, reductions in the
MMG amplitude seem to be more pronounced in the motor unit with the
slower contractile properties. In general (10, 34) and
also in the present study (data not shown), contractions of slower
motor units produce smaller force compared with faster motor units.
Practically, mean force is most often related to the MMG signals in the
studies utilizing voluntary contractions (26, 30, 35).
Therefore, we further tried to identify and present the effects of
contractile properties of the activated motor units on the relation
between the characteristics of surface MMG and the magnitude of the
mean force. Although the available number of motor units was small,
four motor units with longer twitch duration (207.2 ± 6.9 ms)
formed the "slower motor units" group and the four remaining motor
units with shorter twitch duration (166.9 ± 2.0 ms) formed the
"faster motor units" group. These groups were formed to
ascertain whether any effect of the contractile properties of motor
units appear. The MMG amplitude and force fluctuations of each group
were investigated in relation to the mean force during repetitive
stimulations. It should be noted that the mean force was calculated
from the force signals that were not filtered. In Fig. 6, A
and B, greater declines in the group of slower motor units
were apparent for the MMG amplitude and force fluctuations as mean
force increased. Furthermore, we calculated the individual rate of
decline in both MMG amplitude and force fluctuation against the
increase in the mean force for each individual motor unit. In this
calculation, regression analyses were applied to those values obtained
at four different stimulation frequencies. Figure 7 shows that the
rates of change in MMG amplitude and force fluctuations are
significantly related to half relaxation time and twitch duration, with
higher r values in those relations to half relaxation time.
These results suggest that declines in the amplitude of surface MMG
signals with force are more pronounced when the contractile properties
of the activated motor unit are slower.
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Fig. 6.
Relationships between the amplitude of MMG and mean force
(A) and between force fluctuations and mean force
(B) during repetitive stimulation with different
stimulation frequencies. Values are means ± SE.  ,
Data from the 4 motor units with shorter twitch durations (Faster MUs);
 , data from the 4 motor units with longer twitch
durations (Slower MUs).
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Fig. 7.
Rate of changes with force in MMG amplitude (A and
B) and in force fluctuations (C and D)
compared with half relaxation time and twitch duration. Rate of change
with force was calculated by the regression analysis of the relations
between MMG amplitude (%) and mean force (N) for individual motor
units or the relationships between force fluctuations (%) and mean
force (N) for individual motor units. Data are from all the individual
motor units (n = 8).
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DISCUSSION |
Among numerous attempts to clarify the significance of surface
MMG, this is the first study that provides evidence in humans of a
direct relation between the characteristics of surface MMG signals from
a single whole muscle and the contractile properties of motor
units. Major findings of this study were 1) that
the duration of surface MMG was strongly correlated with the twitch duration of a motor unit, 2) that the decline in the
amplitude of surface MMG was closely related to the decline in force
fluctuations generated by increased frequency of contraction,
3) and that fluctuations in surface MMG and force signals
were related to the twitch duration and half relaxation time of the
activated motor units. These results support the hypothesis that the
characteristics of surface MMG are largely dependent on the contractile
properties of the activated motor units, especially on those features
influencing the development of fusion.
Surface MMG and contractile properties of motor units in twitch
contraction.
In vitro studies (2, 12) confirm that the main sources of
the MMG signals are the pressure waves generated by the gross lateral
movement of the muscle fibers that occur during contraction and
relaxation of the fibers. It is not clear, however, how these pressure
waves can be reflected on MMG signals that are recorded at the skin
surface in humans, although studies have tried to relate the
characteristics of surface MMG signals to the contractile properties of
muscle fibers by comparing different muscles (15, 18). In
single-twitch contractions, pressure waves are generated from a simple
movement of muscle fibers by a set of contraction and relaxation.
Contraction time and relaxation time during single-twitch contractions
are mostly related to myosin ATPase activity and reuptake of calcium,
respectively, both of which characterize fiber types, and the latter
can be acutely impaired by fatigue (11). If surface MMG
signals reflect the pressure waves from motor unit activity, then a
close correlation should exist between the duration of surface MMG and
the required time for the muscle fibers to complete a set of
contraction and relaxation. In the present study, the duration for a
set of contraction and relaxation of a motor unit was evaluated by the
sum of contraction time and half relaxation time (twitch duration). In
the motor unit pool of the gastrocnemius muscle in humans, a strong
correlation between duration of surface MMG and twitch duration was
found (Fig. 3). Within the twitch duration, the duration of MMG was
also correlated with half relaxation time but not with contraction
time. This may simply be due to the wider range of half relaxation
times compared with contraction times. The present results clearly
indicate that the duration of surface MMG during twitch contractions
depends on the contractile properties of activated motor units and
suggest that the time characteristics of the pressure waves in twitch contractions is well reflected on surface MMG signals. The
contributions of individual motor units to the surface MMG were
examined in the medial gastrocnemius muscle of rats by stimulating
isolated motor units (5-7). The close connection
between contractile characteristics of motor units and surface MMG
signals in rats has been demonstrated by the strong correlation between
the MMG amplitude and the twitch tension of a motor unit
(5). Together with the present findings on the strong
correlation between the time characteristics of MMG and twitch tension
in humans, it is likely that surface MMG during twitch contractions is
largely dependent on the contractile characteristics of motor units.
Surface MMG in relation to the development of fusion.
In tetanic contractions, lateral movement of muscle fibers may depend
on the combination of the contractile properties of the muscle fibers
and the frequency of the stimulation. Fluctuations of force during
tetanic contractions are generated by the oscillation in tension during
a series of contraction and relaxation. As a rule, the relative
contribution of the relaxation phase to the fluctuations will be
smaller as the stimulation frequency increases and fusion is developed.
It is also known that the slower the twitch of the muscle, the lower
the frequency at which fusion of the evoked mechanical events takes
place (10, 31). As a corollary, force fluctuations at a
given stimulation frequency would be smaller in motor units that have
slower contractile properties. In the present study, this is
demonstrated in the gastrocnemius muscle in humans as a greater rate of
decline in force fluctuations in the slower motor units (Fig.
6B). It is further supported
by a significant correlation between the changes in force fluctuations and twitch duration as well as in the half relaxation time of the motor
units (Fig. 7, C and
D).
Provided that both the lateral movement of muscle fibers and force
fluctuations originate from a common source (2, 12, 22-24), features influencing the development of fusion in
the motor units can affect lateral movement of the muscle fibers and
the characteristics of surface MMG as a consequence. In this study, the
amplitude of MMG decreased in close relation to the force fluctuations
produced by the different frequencies of stimuli (Fig. 5A),
and the magnitude of these reductions was significantly correlated
across the sampled motor units (Fig. 5B). Moreover, the rate
of decline in the amplitude of MMG was significantly correlated with
twitch duration as well as the half relaxation time of motor units
(Fig. 7, A and B). Collectively, these results indicate that the changes in the amplitude of surface MMG during tetanic contractions of the gastrocnemius muscle in humans are largely
dependent on the contractile characteristics and the development of
fusion in the active motor unit. During unfused tetani with a variable
degree of fusion in rats, progressively decreasing fluctuations in
tension have been observed with increasing stimulation frequency, and
the MMG amplitude and fluctuations in tension have been linearly
related (7). This is consistent with the apparently linear
decrease in MMG amplitude and force fluctuations with increasing stimulation frequency in humans (Fig. 5). Although the findings of the
present study are limited because of the small number of motor units
that were studied, previous literature on a rat muscle favors the
present results in a human muscle and lends support to the hypothesis
that the characteristics of surface MMG are largely dependent on the
contractile properties of motor units.
Surface MMG in relation to mean force and EMG during voluntary
contractions.
On the basis of the present findings and previous literature on MMG
during electrically evoked contractions, various characteristics of
surface MMG during voluntary contractions may reasonably be explained.
Contrary to the tetanic contractions of individual motor units in the
present study, voluntary contractions involve a greater number of
activated motor units, and the discharge rate of these motor units
varies and is generally not synchronized. It is of additional note that
the amplitude of surface MMG is proportional to the amplitude of the
motor unit action potential (35). The amplitude of MMG is
known to increase with force in most muscles during voluntary
contractions from low-to-moderate force levels, and the same holds true
for the amplitude of EMG (1, 26, 30, 35). In this range of
force, newly recruited motor units augment the gross lateral movement
of the muscle fibers while the discharge rate of motor units is not yet
high enough to attenuate the amplitude of MMG. At higher force levels,
declines in the amplitude of MMG with increasing force have been
observed, whereas the amplitude of EMG increases continuously because
of the additional recruitment of motor units and the increase in their
discharge rate (1, 26, 35). The decline in the amplitude of MMG may be attributed to the development of fusion where the high
discharge rate of motor units may have greatly reduced the dimensional
changes possible in muscle fibers. It is also expected that a muscle
with a greater percentage of slow motor units is more likely to have a
reduced amplitude of MMG (35).
During voluntary contractions at a submaximal force level, the deficit
in force of motor units during a fatiguing protocol is compensated for
by increases in the discharge rate of already recruited motor units
and/or by the additional recruitment of motor units (20).
These changes in the activation patterns of motor units are reflected
in the increased amplitude of EMG with time, whereas the amplitude of
MMG declines in time with fatigue (27, 30). It is known
that the relaxation time of muscle is prolonged by fatigue
(8). The increased discharge rate of motor units with
prolonged relaxation time under fatigue would facilitate the
development of fusion and thus would decrease the amplitude of MMG.
Collectively, the EMG-MMG relation during voluntary contractions can
exhibit a linear relation under the condition where the positive
effects on the amplitude of MMG and EMG by the recruitment of motor
units are not substantially counteracted by the negative effects on the
amplitude of MMG caused by the development of fusion. The present
findings indicate that the influence of the development of fusion on
MMG would explain this relation between EMG and MMG. It seems,
therefore, that the relation between surface MMG and the force exerted
during voluntary contractions of various muscles is dependent on the
discharge rate and contractile properties of the activated motor units
and on relative proportion of slow motor units in the muscle under
investigation. This interpretation may also be applied to
characterizing physiological tremor by MMG (17), where
unfused tetani may play a role (16).
Technical consideration.
Lastly, it is relevant to point out some technical considerations about
the employed methods and limitations of the obtained results. In
previous studies seeking a relation between surface MMG signals and the
mechanical characteristics of a single motor unit, the spike-triggered
averaging technique has been applied during voluntary contractions
(29, 35). This technique is advantageous in that it does
not require sophisticated stimulation techniques and voluntary
contractions are possible, but it cannot necessarily measure true
mechanical activity of a single motor unit because the averaged signals
can easily be distorted by partial fusion even when it is discharging
at a very low rate (14, 21). The present intramuscular
microstimulation technique circumvents this problem (14)
because it allows the control of discharge rate of a single motor unit
(13, 33).
Analysis or comparison of the recorded signals is further complicated
by the types of transducers and by the layers of tissue between the
muscle and the transducer (9, 22). With the utilization of
an electret condenser microphone in the present study, MMG signals during twitch contraction lasted for the entire duration of the
force twitch as in the previous studies that utilized electret condenser microphones (present study; Ref. 29) or
piezoelectric microphones (5). In contrast, MMG signals
detected by accelerometers have not exceeded the contraction phase of
the single twitch with its main oscillations (3, 4, 25).
Also, the mean frequency of MMG signals matches the stimulation
frequency in the studies with electret condenser microphones (32,
35), whereas the studies with accelerometers tend to have higher
mean frequencies of MMG signals than the stimulation frequency
(37, 38). From the basic mechanical properties of motor
units and the consequent force signals in a single twitch, it is
obvious that acceleration measured during the displacement of the
muscle is much smaller during the relaxation phase compared with the
contraction phase. As a consequence, the second-order derivative of the
displacement during the contraction phase will be particularly
emphasized in the signals recorded with accelerometers. For these
reasons, the waveforms obtained by accelerometers (3, 4,
25) could be different from the ones obtained by electret
condenser microphones (present study; Ref. 35) or
piezoelectric microphones (5).
The skin and fat tissues beneath the transducer can act as low-pass
filters (3, 22), and the occurrence of this is greatly different among subjects and individual muscles. It is true
that the number of motor units is limited in the present study because of the major drawback of the electrical stimulation in humans, but many
of the possible problems in the nature of the signals may be resolved
by employing the intramuscular microstimulation technique on a single
motor unit belonging to the same muscle and by utilizing the electret
condenser microphones. Despite a limited number of motor units sampled,
the mean frequency of MMG matched the stimulation frequency, and the
observed range of contractile measures was substantially wide and
closely consistent with the literature for the human gastrocnemius
muscles (13, 33). This indicates that the effects of the
medium are small or consistent and that the sampled motor units are
well mixed in contractile properties. Still, the findings should be
limited to the present setup for the human gastrocnemius muscles.
Further studies on a larger number of motor units within a single
muscle from a variety of muscles may extend the present findings.
Conclusion.
In conclusion, evidence from the present study supports a close
relation between the surface MMG and the contractile properties of
individual motor units within a single muscle in humans. It is
suggested that the major characteristics of surface MMG are largely
dependent on the contractile properties, especially on features in the
development of fusion, of the activated motor units.
| |
ACKNOWLEDGEMENTS |
The authors are grateful to Drs. Motoki Kouzaki, Tetsuo Fukunaga,
and Hiroaki Kanehisa (University of Tokyo, Tokyo, Japan) for helpful
suggestions and to Fumi Toyooka (University of Tokyo, Tokyo, Japan) for
assistance with the figures. We thank Kevin G. Keenan (University of
Colorado, Boulder, CO) for help proofreading and improving the manuscript.
| |
FOOTNOTES |
This study was partly supported by Grant-in-Aid for Scientific
Research 13-05038 from the Japan Society for the Promotion of Science.
Present address of Y. Yoshitake: Dept. of Health Sciences, Oita Univ.
of Nursing and Health Sciences, 2944-9 Notsuharu, Oita 870-1201, Japan.
Address for reprint requests and other correspondence: Y. Yoshitake, Dept. of Health Sciences, Oita Univ. of Nursing and Health Sciences, 2944-9 Notsuharu, Oita 870-1201, Japan (E-mail:
yoshitake{at}oita-nhs.ac.jp).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
July 19, 2002;10.1152/japplphysiol.00008.2002
Received 8 January 2002; accepted in final form 16 July 2002.
| |
REFERENCES |
1.
Akataki, K,
Mita K,
Watakabe M,
and
Itoh K.
Mechanomyogram and force relationship during voluntary isometric ramp contractions of the biceps brachii muscle.
Eur J Appl Physiol
84:
19-25,
2001[Medline].
2.
Barry, DT.
Acoustic signals from frog skeletal muscle.
Biophys J
51:
769-773,
1987[Abstract/Free Full Text].
3.
Barry, DT.
Vibrations and sounds from evoked muscle twitches.
Electromyogr Clin Neurophysiol
32:
35-40,
1992[Medline].
4.
Barry, DT,
Hill T,
and
Im D.
Muscle fatigue measured with evoked muscle vibrations.
Muscle Nerve
15:
303-309,
1992[Medline].
5.
Bichler, E.
Mechanomyograms recorded during evoked contractions of single motor units in the rat medial gastrocnemius muscle.
Eur J Appl Physiol
83:
310-319,
2000[Medline].
6.
Bichler, E,
and
Celichowski J.
Changes in the properties of mechanomyographic signals and in the tension during the fatigue test of rat medial gastrocnemius muscle motor units.
J Electromyogr Kinesiol
11:
387-394,
2001[Medline].
7.
Bichler, E,
and
Celichowski J.
Mechanomyographic signals generated during unfused tetani of single motor units in the rat medial gastrocnemius muscle.
Eur J Appl Physiol
85:
513-520,
2001[Medline].
8.
Bigland-Ritchie, B,
Johansson R,
Lippold OC,
and
Woods JJ.
Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions.
J Neurophysiol
50:
313-324,
1983[Abstract/Free Full Text].
9.
Bolton, C,
Parkes T,
Thompson R,
Clark M,
and
Sterne J.
Recording sounds from human skeletal muscle: technical and physiological aspects.
Muscle Nerve
12:
126-134,
1989[Medline].
10.
Burke, RE,
Levine DN,
Tsairis P,
and
Zajac FE, III.
Physiological types and histochemical profiles in motor units of the cat gastrocnemius.
J Physiol
234:
723-748,
1973[Abstract/Free Full Text].
11.
Close, RI.
Dynamic properties of mammalian skeletal muscles.
Physiol Rev
52:
129-197,
1972[Free Full Text].
12.
Frangioni, JV,
Kwan-Gett TS,
Dubrunz LE,
and
McMahon TA.
The mechanism of low frequency sound production in muscle.
Biophys J
51:
775-783,
1987[Abstract/Free Full Text].
13.
Garnett, RAF,
O'Donovan MJ,
Stephens JA,
and
Taylor A.
Motor unit organization of human medial gastrocnemius.
J Physiol
287:
33-43,
1979[Abstract/Free Full Text].
14.
Kossev, A,
Elek JM,
Wohlfarth K,
Schubert M,
Dengler R,
and
Wolf W.
Assessment of human motor unit twitches
a comparison of spike-triggered averaging and intramuscular microstimulation.
Electroencephalogr Clin Neurophysiol
93:
100-105,
1994[ISI][Medline].
15.
Marchetti, M,
Felici F,
Bernardi M,
Minasi P,
and
Di Filippo L.
Can evoked phonomyography be used to recognize fast and slow muscle in man?
Int J Sports Med
13:
65-68,
1992[Medline].
16.
McAuley, JH,
and
Marsden CD.
Physiological and pathological tremors and rhythmic central motor control.
Brain
123:
1545-1567,
2000[Abstract/Free Full Text].
17.
McAuley, JH,
Rothwell JC,
and
Marsden CD.
Frequency peaks of tremor, muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing.
Exp Brain Res
114:
525-541,
1997[ISI][Medline].
18.
Mealing, D,
Long G,
and
McCarthy PW.
Vibromyographic recording from human muscles with known fibre composition differences.
Br J Sports Med
30:
27-31,
1996[Abstract].
19.
Moritani, T,
Berry MJ,
Bacharach DW,
and
Nakamura E.
Gas exchange parameters, muscle blood flow and electromechanical properties of the plantar flexors.
Eur J Appl Physiol
56:
30-37,
1987[ISI].
20.
Moritani, T,
Muro M,
and
Nagata A.
Intramuscular and surface electromyogram changes during muscle fatigue.
J Appl Physiol
60:
1179-1185,
1986[Abstract/Free Full Text].
21.
Nordstrom, MA,
Miles T,
and
Veale J.
Effect of motor unit firing pattern on twitches obtained by spike-triggered averaging.
Muscle Nerve
12:
556-567,
1989[ISI][Medline].
22.
Orizio, C.
Muscle sound bases for the introduction of mechanomyographic signal in muscle studies.
Crit Rev Biomed Eng
21:
201-243,
1993[ISI][Medline].
23.
Orizio, C,
Baratta RV,
Zhou BH,
Solomonow M,
and
Veicsteinas A.
Force and surface mechanomyogram relationship in cat gastrocnemius.
J Electromyogr Kinesiol
9:
131-140,
1999[Medline].
24.
Orizio, C,
Baratta RV,
Zhou BH,
Solomonow M,
and
Veicsteinas A.
Force and surface mechanomyogram frequency responses in cat gastrocnemius.
J Biomech
33:
427-433,
2000[Medline].
25.
Orizio, C,
Diemont B,
Esposito F,
Alfonsi E,
Parrinello G,
Moglia A,
and
Veicsteinas A.
Surface mechanomyogram reflects the changes in the mechanical properties of muscle at fatigue.
Eur J Appl Physiol
80:
276-284,
1999.
26.
Orizio, C,
Perini R,
and
Veicsteinas A.
Muscular sound and force relationship during isometric contraction in man.
Eur J Appl Physiol
58:
528-533,
1989.
27.
Orizio, C,
Perini R,
and
Veicsteinas A.
Changes of muscular sound during sustained isometric contraction up to exhaustion.
J Appl Physiol
66:
1593-1598,
1989[Abstract/Free Full Text].
28.
Orizio, C,
Solomonow M,
Baratta R,
and
Veicsteinas A.
Influence of motor units recruitment and firing rate on the soundmyogram and EMG characteristics in cat gastrocnemius.
J Electromyogr Kinesiol
2:
232-241,
1993.
29.
Petitjean, M,
and
Maton B.
Phonomyogram from single motor units during voluntary isometric contraction.
Eur J Appl Physiol
71:
215-222,
1995.
30.
Shinohara, M,
Kouzaki M,
Yoshihisa T,
and
Fukunaga T.
Mechanomyogram from the different heads of the quadriceps muscle during incremental knee extension.
Eur J Appl Physiol
78:
289-295,
1998.
31.
Steg, G.
Efferent muscle innervation and rigidity.
Acta Physiol Scand
61:
1-53,
1964[Medline].
32.
Stokes, MJ,
and
Cooper RG.
Muscle sounds during voluntary and stimulated contractions of the human adductor pollicis muscle.
J Appl Physiol
72:
1908-1913,
1992[Abstract/Free Full Text].
33.
Taylor, A,
and
Stephens JA.
Study of human motor unit contractions by controlled intramuscular microstimulation.
Brain Res
117:
331-335,
1976[ISI][Medline].
34.
Thomas, CK,
Johansson RS,
and
Bigland-Ritchie B.
Attempts to physiologically classify human thenar motor units.
J Neurophysiol
65:
1501-1508,
1991[Abstract/Free Full Text].
35.
Yoshitake, Y,
and
Moritani T.
The muscle sound properties of different muscle fiber types during voluntary and electrically induced contractions.
J Electromyogr Kinesiol
9:
209-217,
1999[Medline].
36.
Yoshitake, Y,
Ue H,
Miyazaki M,
and
Moritani T.
Assessment of lower-back muscle fatigue using electromyography, mechanomyography, and near-infrared spectroscopy.
Eur J Appl Physiol
84:
174-179,
2001[ISI][Medline].
37.
Vaz, MA,
Herzog W,
Zhang YT,
Leonard TR,
and
Ngyuyen H.
Mechanism of electrically elicited muscle vibrations in the in-situ cat soleus muscle.
Muscle Nerve
19:
774-776,
1996[Medline].
38.
Vaz, MA,
Herzog W,
Zhang YT,
Leonard TR,
and
Ngyuyen H.
The effect of muscle length on electrically elicited muscle vibrations in the in-situ cat soleus muscle.
J Electromyogr Kinesiol
7:
113-121,
1997.
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