J Appl Physiol 99: 603– 608, 2005.

First published April 21, 2005; doi:10.1152/japplphysiol.00189.2005.

Muscle-tendon interaction and elastic energy usage in human walking

Masaki Ishikawa,1 Paavo V. Komi,1 Michael J. Grey,1,2 Vesa Lepola,3 and Gert-Peter Bruggemann4
1
Department of Biology of Physical Activity, Neuromuscular Research Center, University of Jyväskylä,
Jyväskylä, Finland; 2Department of Health Science and Technology, Clinic of Surgery, Center for
Sensory-Motor Interaction, Aalborg University, Aalborg, Denmark; 3Central Hospital of Central Finland,
Jyväskylä, Finland; and 4Institute for Biomechanics, German Sport University of Cologne, Cologne, Germany
Submitted 16 February 2005; accepted in final form 19 April 2005

Ishikawa, Masaki, Paavo V. Komi, Michael J. Grey, Vesa
Lepola, and Gert-Peter Bruggemann. Muscle-tendon interaction and
elastic energy usage in human walking. J Appl Physiol 99: 603–608, 2005.
First published April 21, 2005; doi:10.1152/japplphysiol.00189.2005.—The
present study was designed to explore how the interaction between the
fascicles and tendinous tissues is involved in storage and utilization of
elastic energy during human walking. Eight male subjects walked with a
natural cadence (1.4 ⫾ 0.1 m/s) on a 10-m-long force plate system. In
vivo techniques were employed to record the Achilles tendon force and
to scan real-time fascicle lengths for two muscles (medial gastrocnemius
and soleus). The results showed that tendinous tissues of both medial
gastrocnemius and soleus muscles lengthened slowly throughout the
single-stance phase and then recoiled rapidly close to the end of the
ground contact. However, the fascicle length changes demonstrated
different patterns and amplitudes between two muscles. The medial
gastrocnemius fascicles were stretched during the early single-stance
phase and then remained isometrically during the late-stance phase. In
contrast, the soleus fascicles were lengthened until the end of the single-
stance phase. These findings suggest that the elastic recoil takes place not
as a spring-like bouncing but as a catapult action in natural human
walking. The interaction between the muscle fascicles and tendinous
tissues plays an important role in the process of release of elastic energy,
although the leg muscles, which are commonly accepted as synergists, do
not have similar mechanical behavior of fascicles in this catapult action.
tendinous tissue; soleus; medial gastrocnemius
IN HUMAN LOCOMOTION, there are two fundamental concepts for
different energy-conserving mechanisms. First, mechanical en-
ergy stored in the elastic elements of muscle can be recovered
as both kinetic and gravitational energy (spring-like bouncing
mechanism). Second, gravitational potential energy is con-
verted to kinetic energy as the leg swings in a pendulum-like
mechanism. Both of these mechanisms are important for the
mechanics and energetics of locomotion (5, 17, 19). In running
or jumping, it has been proposed that skeletal muscle stores
energy by the active stretching due to inertial, gravitational, or
any other external forces during the first half of the stance
phase of the step cycle and then immediately returns this
energy effectively over the later part of the stance phase as a
spring-like bouncing mechanism (for review, see Ref. 2). In
walking, the pendulum-like movement concept has been pro-
posed as a basis for energy saving. In brief, this would mean
that the muscles perform the external positive work for each
step effectively just to give an additional push forward during
the middle of the double-stance phase and to complete the
vertical lift during the middle of the single-stance phase to
sustain the forward speed changes. Thus the recovery of
mechanical energy through a pendulum-like motion, in which
the potential and kinetic energy exchanges are conveniently in
opposite phases, can be utilized for energy saving (16). How-
ever, the energy saving may not necessarily come from the
pendulum-type action alone during walking. For example,
when a person walks in simulated reduced gravity condition,
his/her net metabolic cost does not decrease according to body
weight (21, 26). The relatively small decrease in metabolic cost
in the reduced gravity condition cannot be explained by a
mismatch of kinetic and gravitational potential energy that
would compromise the pendulum energy exchange. Conse-
quently, other mechanisms have also been proposed for
the energy saving during human locomotion (25, 30, 40, 41,
43, 44).
Recent direct fascicle length measurements using ultrasonic
techniques can provide the information of the mechanical events
inside muscle-tendon unit (MTU). With regard to mechanics and
energetics of locomotion, it is of interest to study the possible
effects of tendon elasticity during locomotion. In running or
jumping, it has been confirmed that tendinous tissues (TT; apo-
neuroses and outer tendon) can store energy by the active stretch-
ing due to inertial, gravitational, or any other external forces
during the first half of the stance phase of the step cycle and then
immediately return this energy effectively over the later part of the
stance phase (34, 42) as a spring-like bouncing mechanism (2,
17). On the fascicle level, the gastrocnemius muscle fascicles have
been shown to contract isometrically or shorten throughout the
ground contact in running (42) and jumping (34). This muscle
fiber-TT interaction for the effective utilization of TT in running
and jumping has been named as “concerted action” (31). In
walking, MTU of the triceps surae muscle are lengthened before
shortening during the contact phase. This may imply that tendon
compliance would play an important role during the contact phase
of walking. In direct fascicle length measurement during slow
treadmill walking, several studies have reported that muscle fibers
behaved isometrically during the contact phase (25, 27, 32). These
results also suggest the importance of TT elasticity during the
contact phase of walking. However, it has been argued that no
strain energy can be gained in the initial impact to power the
push-off during human walking (5). Compared with running,
walking is characterized by smaller braking force and longer
coupling time between the braking and push-off phases. Conse-
quently, it is of interest to know how elastic energy can be stored
and released efficiently during the stance phase of natural human
walking on level ground. To the best of our knowledge, literature

Address for reprint requests and other correspondence: M. Ishikawa, Neu-

romuscular Research Center, Dept. of Biology of Physical Activity, Univ. of The costs of publication of this article were defrayed in part by the payment
Jyväskylä, PO Box 35 (LL2), 40014 Jyväskylä, Finland (E-mail: of page charges. The article must therefore be hereby marked “advertisement”
masaki@sport.jyu.fi). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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604 CATAPULT ACTION DURING HUMAN WALKING
lacks reports that have examined interaction between fascicle-TT
during the natural walking on level ground.
In the present study, we used novel in vivo techniques to
measure Achilles tendon force (ATF) and fascicle lengths for two
muscles [medial gastrocnemius (MG) and soleus (Sol)] during
natural human walking on level ground. The present study was
designed to explore how the interaction between the fascicles and
TT is involved in storage and utilization of elastic energy during
human walking with a natural cadence. We hypothesized that the
elastic bouncing may not be the most important way to utilize
elastic energy. Instead, it is believed that the specific interaction
between fascicle and TT allows elastic energy to be utilized for
energy saving. This possible mechanism may not, however, ap-
pear similarly in MG and Sol muscles. One of the possible
candidates for this mechanism is a catapult action introduced by
Alexander and Bennet-Clark (6).
METHODS
Subjects and experimental procedure. Eight male subjects, age
28.4 yr (SD 5.0), height 171.8 cm (SD 4.3), body mass 71.7 kg (SD
7.2), participated in the study after giving informed consent of the
procedures and risks associated with the study according to the
Declaration of Helsinki. The study was approved by the Ethics
Committee of the University of the Jyväskylä.
The subjects walked with a natural cadence, speed 1.4 m/s (SD 0.1)
and ground contact time 640 ms (SD 50), on a unique 10-m-long force
platform system with two separate rows of force plates (Raute; Fig. 1)
starting from 5 m before. The horizontal and vertical ground reaction
forces were recorded separately (right and left sides). In the present study,
the ultrasonographic apparatus (SSD-2000, 5500; Aloka) were used to
measure fascicle length in the MG and Sol muscles during walking (50
and 96 images/s, a linear array probe with scanning frequency of 5–10
MHz, Aloka) (25, 34 –36, 39). In the present study, the width and depth
resolution of our high-speed scanning ultrasonography were 0.45 and
0.36 mm, respectively. The ultrasound apparatus was pushed on the side
of the force platform at the subjects’ walking speed. Simultaneously, an
optic fiber transducer passed transversely through the Achilles tendon
was used to measure the tensile stress within the Achilles tendon. The use
of optic fiber as a transducer for tendon stress is based on light-intensity
Fig. 1. A: setup for the walking experiment.
Muscle-tendon compartments [medial gas-
trocnemius (MG) and soleus (Sol) muscles;
ultrasonography], Achilles tendon forces
(ATF), and electromyograms (EMGs) were
measured simultaneously on a unique 10-m-
long force plate system composed of 2 rows
of individual force plates. The data logger for
EMG (3 muscles) and tendon transducer (op-
tic fiber) unit was attached to the subject’s
waist. The ultrasound apparatus was pushed
forward at the speed of the subject outside the
force plate area. Ankle, knee, and hip joint
angles were also measured simultaneously by
using goniometers (Gonio). B: calculation of
the fascicle length and angle from MG and
Sol muscles.
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modulation occurring in a micro-deformable optic fiber. The light signal
detected by the receiver unit is converted to analog signal and further to
force using calibration curves and equation of balance of the moments
(see Refs. 9, 22, 38 for details). Surface bipolar electromyographic
(EMG) electrodes were used to record the tibialis anterior, MG, and Sol
muscle activities (Ag/AgCl miniature surface bipolar electrodes, diameter
of 5 mm, interelectrode distance of 20 mm; Beckman skin electrode
650437). The midbellies of the muscles were confirmed from B-mode
ultrasonographic images, and care was taken not to place the electrodes
over the peripheries of muscles to minimize EMG cross talk between
muscles. EMGs were amplified (input impedance of ⬎25 M⍀, common
mode rejection ratio ⬎90 dB) and sent telemetrically to the recording
computer (12-bit analog-to-digital converter) with a sampling frequency
of 1 kHz. Care was taken that the interelectrode resistance was below 5
k⍀. The goniometers were used to record the angular position of the hip,
knee, and ankle joints. The output signal triggered from the vertical
ground reaction force of the right leg side was used to synchronize the
signal and ultrasound data. Ground reaction forces, ATF, EMGs, and
angular data were sampled at 1,000 Hz simultaneously.
Analyses. The contact phase of the step cycle was subdivided
into four different phases based on the ground reaction force
curves (brake I and II, push I and II; see Fig. 2A for detail). During
the contact of walking, the model of Hawkins and Hull (28) was
used to estimate length changes in MTU from the ankle (Sol and
MG) and knee joint angular (MG) position. The muscle fascicle
length of both MG and Sol muscles were measured from each
ultrasonographic image during walking (Fig. 1B). The MG and Sol
fascicles were identified in each image along their length from the
superficial and deep aponeuroses (Fig. 1B). These fascicles were
then tracked continuously frame by frame using Motus software
(Peak Performance Technologies). The fascicle angles in the MG
and Sol muscles were determined as the angle between the apo-
neurosis and the line drawn tangentially to the fascicle (see Fig.
1B). The analyzed ultrasound data were interpolated at 100 Hz.
The length of TT (LTT) in both muscles were calculated from the
following equation (25, 34, 39)
L TT ⫽ LMTU ⫺ Lfascicle 䡠 cos ␣
where Lfascicle, ␣, and LMTU are fascicle length, fascicle angle, and
MTU length, respectively.
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 CATAPULT ACTION DURING HUMAN WALKING
The velocities of MTU, fascicle, and TT were calculated by the
weighted quadratic polynomial differentiation (5 discrete points) of
the corresponding length value. Shortening direction was defined as
positive. The reliability and reproducibility of the fascicle length
measurement with the ultrasound method has been confirmed else-
where (23, 25, 36, 39).
From the direct ATF during walking, ATF was further reduced to
the relative physiological cross-sectional area of the MG and Sol in
the Achilles tendon (24). The mechanical power was calculated by
velocities of the length changes (MTU and TT) and tendon forces in
the MG and Sol muscles, respectively (34, 39).
In each subject, the signal data of 8 –10 steps were averaged (after the
EMG signals were full-wave rectified), and then eight subjects’ data were
averaged. For the ultrasound data, the three steps were averaged for each
subject, and then eight subjects’ data were averaged.
Statistics. Values are presented as means and standard deviations
unless stated otherwise. Statistical analysis was performed using the
two-tailed paired Student’s t-test for the comparison between MG and
Sol muscles. The Wilcoxon signed rank test was used for the com-
parison of the fascicle lengthening between MG and Sol because the
normality test was failed. A two-way ANOVA was used to analyze
the difference in the averaged EMG amplitude and fascicle length
changes during the brake II and push I phases. The probability level
for statistical analysis was set at P ⬍ 0.05.
RESULTS
Figure 2 presents the time course-averaged data during the
contact of walking, where changes in ground reaction forces,
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605
Fig. 2. Records (n ⫽ 8) of the vertical ground
reaction force of right and left legs (Fv_R and
Fv_L, respectively) and horizontal ground re-
action force of right leg (Fh_R) (A), Achilles
tendon force (ATF) and joint angles (B),
lengths of muscle-tendon unit (MTU), fasci-
cle, and tendinous tissue (TT) [in MG (C) and
Sol (D)], and the EMG patterns from MG (E)
and Sol (F) during the contact phase of walk-
ing. C and D: relative length changes from the
heel strike are shown. EMGs were normalized
to the individual peak values during the step
cycle. Due to timing differences of these peak
values, the averaged EMGs (shown in the
figure) are below 100%. The contact phase
was divided into 4 phases (A). Dotted lines
and bars show the positive values of 1 SE.
joint angular data, ATF, length changes, and EMGs are shown.
As expected from previous experiments (22, 37), ATF dem-
onstrated a sudden decrease on heel strike during walking on
ground in all subjects (Fig. 2B). Similar reductions in the
MTU, fascicle, and TT lengths in both muscles were observed
due to the rapid ankle plantar flexion during the brake I phase
(Fig. 2). In the subsequent brake II phase, the vertical ground
reaction force in the right leg decreased but ATF started to
increase after the first peak vertical ground reaction force in the
right leg (Fig. 2, A and B). The ATF and EMGs (MG and Sol)
increased with a simultaneous lengthening of MTU, fascicles,
and TT in both muscles in varying degrees (Figs. 2 and 3).
Increase of ATF took place until the beginning of the push II
phase (Fig. 2B). Thereafter, it decreased but much later than
the corresponding EMG activities of the MG and Sol muscles
(Fig. 2).
The MTU and TT in both muscles lengthened slowly during
the brake II and push I phases, and then they recoiled rapidly
during the push II phase in all subjects (Fig. 2, C and D).
However, the pattern and amplitude of the fascicle length
changes were different between muscles. MG fascicles were
stretched during the brake II phase and then remained isomet-
rically during the push I phase. In contrast, Sol fascicles
continued lengthening during the push I phase. In both cases,
the fascicles shortened with the low EMG activities during the
push II phase (Fig. 2).
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606 CATAPULT ACTION DURING HUMAN WALKING
Figure 3A shows the peak-to-peak amplitudes of lengthening
and shortening in MTU, fascicle, and TT during the right-leg
contact of walking. Compared with MG, Sol MTU lengthened
relatively more. The difference was not, however, statistically
significant. Similarly, there was no significant difference between
both muscles in the MTU shortening amplitude. On the fascicular
level, however, not only the patterns of the fascicle length but also
the lengthening amplitudes were different between muscles (Fig.
3B). The fascicle lengthening amplitude was greater in Sol than in
MG (P ⬍ 0.05). In contrast, the shortening was greater in MG
than in Sol (P ⬍ 0.05). On the TT level, the lengthening and
shortening amplitudes did not show any significant difference
between the two muscles (Fig. 3C).
DISCUSSION
The results of the present study demonstrated that, during
walking on level ground and with a natural cadence, TT
elasticity can be utilized. TT of both MG and Sol muscles were
stretched slowly during the single support phase and then
dramatically recoiled during the end of the contact phase. In
contrast to TT, the fascicles behaved differently during the
contact phase of walking. In addition, the fascicle and TT
length patterns did not follow the ATF patterns. These results
clearly indicate the existence of specific interactions between
fascicles, TT, and ATF during walking. Furthermore, we have
provided evidence that the two muscles (MG and Sol) that are
commonly accepted as synergists do not have similar mechan-
ical behavior of fascicles during walking.
Utilization of elasticity in walking. The fascicle length and
ATF measurements used in this study indicated that TT was
stretched slowly throughout the brake II and push I phases and
subsequently recoiled rapidly (Fig. 2). The stretched TT am-
plitudes from the heel strike in both MG (4.2 ⫾ 1.5%) and Sol
(4.3 ⫾ 1.4%) muscles are consistent with similar values re-
ported previously in animal walking (2– 6%) (8, 20). In the
present study, however, these TT behaviors during the contact
of walking do not follow the spring-like bouncing concept, in
which the tendons store energy in the first half of the step and
then return this energy in the second-half phase (2). According
to our interpretation of several studies that have examined
stretch-shortening cycle in both animals (42) and humans (34,
36, 39), the concerted fascicle action seems to refer to favoring
of the effective spring-like bouncing of TT during the ground
Fig. 3. Relative changes of lengthening and shortening in MTU
(A), fascicle (B), and TT (C) of MG and Sol muscles during the
contact of walking (means ⫹ SD; n ⫽ 8). Lengthening ampli-
tude was calculated from the lowest point after the rapid plantar
flexion (top right).
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contact. In running and jumping, for example, the elastic
energy comes mainly from the initial negative work. But in
walking with a natural cadence, ATF is low during the brake I
and II phases (Fig. 2B). Therefore, TT cannot be stretched
under the spring-like bouncing concept during the brake I and
II phases. To support this suggestion, the TT stretching curves
in both MG and Sol did not follow the ATF development slope
during contact of walking (Fig. 2). These results clearly indi-
cate existence of an alternative way for the spring-like bounc-
ing concept to utilize elasticity.
The question may be asked which mechanism would cause
utilization of elastic energy during the slow stretching and
rapid recoiling of TT during the ground contact of walking.
The natural candidate for this behavior is the concept of a
catapult action (6, 11, 12), in which the spring stretches slowly
and recoils rapidly. In this action, the power output can be
amplified by the rapid positive work against the negative work
done during the slow stretch, as demonstrated in insect jump-
ing (11, 12). The mechanical power curves of the present study
also showed a similar catapult behavior to amplify MTU power
production during the end of the ground contact (Fig. 4). To the
best of our knowledge, this has not been demonstrated earlier
in human locomotion. These catapult and spring-like bouncing
actions have a common feature of the dramatic TT shortening.
But the catapult action is fundamentally different from the
spring-like bouncing behavior of TT that is observed during
running (42) and in short contact jumps (34). In the catapult
action, which we now suggest to take place during human
walking, elastic energy is not provided directly from initial
negative work. Instead, it can be mainly provided by muscle
action. This does not exclude the possibility to utilize simul-
taneously the pendulum and energy transfer mechanisms.
Benefits of catapult action in walking. The spring-like
bouncing behavior of TT observed during running (42) and in
short-contact jumps (34) can be advantageous for effective
utilization of elasticity. However, the concerted contraction for
the spring-like bouncing is not necessarily economical to
achieve the highest possible positive work. In the natural
cadence walking performed in the present study, however, it
can be assumed that the energy expenditure can be lower
compared with other speeds of walking (15). Our data indicate
that the MG and Sol TT can act as a catapult action to amplify
muscle power production. The observed interaction between
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 CATAPULT ACTION DURING HUMAN WALKING
Fig. 4. Changes of the mechanical power (MTU, TT, and MTU ⫺ TT) in Sol
during the contact of walking (n ⫽ 8). It was assumed that relative contribution
of the force developed by Sol muscle on ATF was equal to the relative
physiological cross-sectional area of Sol among all plantar flexors. Mechanical
power was calculated by multiplying the velocity by force in MTU and TT,
respectively. The plus and minus signs refer to shortening and lengthening
powers, respectively.
fascicles and TT seems to be advantageous for utilization of
elastic energy during human walking. The energy expenditure
during the fascicle lengthening action can be less than that
during an isometric or shortening action (1, 2, 29). Thus the
fascicle lengthening can take advantage of energy-saving dur-
ing the single-stance phase. The fascicle behavior from the
treadmill walking (25), however, may stand in opposition to
our findings, especially for the Sol muscle. Fukunaga et al. (25)
suggested that if fascicles are lengthened instead of maintain-
ing the same length, the stored elastic energy in TT will
decrease during the single-stance phase. Consequently, addi-
tional metabolic energy will be required to make up for this
loss. However, TT was not stretched during the brake II phase
of natural human walking by the concerted fascicle action in
the manner it may occur in the spring-like bouncing mecha-
nism. This is because ATF cannot be high enough during the
braking phase. In addition, the contact time during human
walking does not match the cycle time of the resonant fre-
quency of the elastic component in ankle extensors (10). This
resonant oscillating frequency has a range of 2.6 – 4.3 Hz (10,
14, 18). This corresponds to the ground contact time between
233 and 385 ms. However, the contact time measured in the
present study (640 ⫾ 50 ms) was much longer than that of the
resonant elastic frequency. It is also possible that the bouncing
frequency of elastic component in ankle extensors can be
modified for the spring-like bouncing action by the regulation
of the ankle joint stiffness. To regulate the stiffness, one must
activate more triceps surae muscle during the braking phase.
This may cause an increase in vertical position of center of
mass during the middle of the single-stance phase, but it may
not contribute to any additional forward push during the middle
of the double-stance phase. Thus it can be suggested that the
consumption of minimal metabolic energy during human walk-
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607
ing cannot be provided by the spring-like bouncing but more
likely by the catapult action. Consequently, it can be speculated
that, if the contact time is shorter with increasing the walking
speed, the TT utilization process may shift from the catapult to
the spring bouncing action during the contact of walking. This
assumption needs to be verified in future studies.
Muscle-specific behavior. Another major finding of the
present study was that MG and Sol fascicles behaved differ-
ently during the push I phase during human walking (Fig. 2, C
and D). The MG fascicles remained at the same length during
the push I phase after the lengthening during the brake II phase.
However, the Sol fascicles were lengthened continuously dur-
ing the brake II and push I phases. Generally, the biarticular
MG muscle offsets the lengthening and shortening effects
during human movements. During the single-stance phase of
human walking, however, the knee joint is extended only
slightly (Fig. 2B). This indicates that the fascicles in the
biarticular MG muscle may not behave in the same way as in
the monoarticular Sol muscle (34). This muscle specificity
during human walking could be observed by the difference of
the fascicle behavior related to the muscle activation from the
end of the brake II phase to the push I phase (Fig. 5). The Sol
fascicles lengthened (P ⬍ 0.05) with increasing muscle acti-
vation, but the MG fascicles remained at the same length or
tended to shorten in the opposite direction. Alexander (3) was
the first to report the different muscle behavior between hip,
knee, and ankle joint muscles during the dog jumping. In
addition, the present study shows that leg muscles, which are
commonly accepted as synergists, do not have similar mechan-
ical behavior of fascicles during human walking. These results
highlight the fact that observations made from the fascicles of
one muscle cannot necessarily be extended to other muscles
during dynamic movements (33, 34) as well as in the static
human movements (13). On the TT level, however, both
muscles showed a similar length change pattern during the
contact of walking. These results suggest that, although TT
elasticity depends on the length and cross-sectional area (7),
the manner of the TT behavior may be the same between
different muscles. This certainly is still speculation and awaits
further verification.
Fig. 5. Relative changes in the fascicle length (■) and corresponding changes
in the averaged EMG (aEMG) during the brake II and push I phases. E,
corresponding changes in aEMG values of the MG (left) and Sol (middle)
muscles. Right: to calculate the aEMG changes, the brake I phase was used as
a reference value to obtain the relative aEMG values for the brake II and push
I phases.
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608 CATAPULT ACTION DURING HUMAN WALKING
Methodological consideration. There are certain points in
the methods that need to be addressed. The present study is
perhaps the first in which fascicle length and ATF measure-
ments were utilized simultaneously during human walking.
During the ATF measurements, it is possible that the skin
movement during walking may cause minor artifacts to signal.
However, the ATF patterns measured with this technique (22)
have been shown to be similar to those obtained with the
buckle transducer method (37) during human walking. With
regard to calculation of MG and Sol forces, we did not consider
the activation level and energy transfer from the knee joints.
This can naturally influence our power calculation data. How-
ever, we assume that these methodological problems in our
force calculation are minor and did not have a serious effect on
our results and interpretation.
Finally, the results of the present study cannot be general-
ized to apply to all speeds of walking. As Alexander (4)
argued, elastic energy-saving mechanisms cannot be equal
when walking speeds are changed. These points need to be
examined in future studies.
In summary, the present results demonstrate the concept of
elastic recoil by a catapult action in natural human walking.
The interactions between the muscle fascicles and TT play an
important role in the process of the economical storage and
release of elastic energy, although the manner in which this
action occurs may depend on the muscle that is studied.
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