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Sadao Kurokawa, Tetsuo Fukunaga, Akinori Nagano and Senshi Fukashiro
J Appl Physiol 95:2306-2314, 2003. First published Jul 18, 2003; doi:10.1152/japplphysiol.00219.2003
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Explanation of the bilateral deficit in human vertical squat jumping
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J Appl Physiol 95: 2306–2314, 2003.
First published July 18, 2003; 10.1152/japplphysiol.00219.2003.
Interaction between fascicles and tendinous structures
during counter movement jumping investigated in vivo
Sadao Kurokawa,1 Tetsuo Fukunaga,2 Akinori Nagano,3 and Senshi Fukashiro4
1
Laboratory of Sports Sciences, Joshibi University of Art and Design, Suginami, Tokyo 166-8538;
School of Human Sciences, Waseda University, Tokorozawa, Saitama 359-1164; 3Computer &
Information Division, RIKEN, Wako, Saitama 351-0198; and 4Department of Life Sciences,
The University of Tokyo, Meguro, Tokyo 153-8902, Japan
2
Submitted 3 March 2003; accepted in final form 2 July 2003
ultrasonography; elastic energy; vertical jump
movements, such as running, jumping, and throwing, are generated as a combination of joint actions. Joint moments are caused by
tensional forces developed by muscle fibers, which are
NATURAL AND COMPLEX HUMAN
Address for reprint requests and other correspondence: S.
Fukashiro, Dept. of Life Sci., Univ. of Tokyo, Komaba 3-8-1, Meguro,
Tokyo 153-8902, Japan (E-mail: [email protected]).
2306
transmitted to bones through tendinous structures
(i.e., external tendon and aponeuroses). Therefore, mechanical properties of the tendinous structures need to
be considered to obtain insights regarding the behavior
of muscle fibers during natural and complex human
movements. Tendinous structures have nonlinear elastic properties (12, 40, 43). Length change in muscle
fibers is not singularly determined by joint angle
changes, although it is assumed that the length of the
muscle-tendon complex (MTC) is singularly determined by joint angles (19, 26).
The stretch-shortening cycle (SSC) is observed quite
often in natural human movements. It has been observed in many studies that a counter movement
and/or a prestretch improve the performance, especially in relatively fast movements (4, 44). For instance, in maximal-effort vertical jumping, it has been
demonstrated that subjects achieve a greater jump
height with a counter movement starting from an
erect standing position [counter movement jumping
(CMJ)] than without a counter movement starting
from a squatting position [squat jumping (SQJ);
Refs. 4, 38]. This is true even when the body configuration at the start of the push-off is identical between SQJ and CMJ (3, 9). It has also been reported
that subjects are able to produce greater work
around the hip joint in CMJ than in SQJ (21).
According to preceding studies, the following factors
are assumed to be contributing to the work enhancement with a counter movement: the time available for
force development (9), storage and reutilization of elastic energy (4), potentiation of the contractile machinery
(6, 37), and the contribution of stretch reflexes (16, 24,
46). There have been several simulation studies that
investigated how these factors contribute to work enhancement with a counter movement (3, 8, 9, 46).
However, only a limited amount of direct experimental
measurements has been performed regarding the behavior of the MTC during natural human motions.
Therefore, to proceed to the next step in this field, it is
necessary to investigate how muscle fibers and tendi-
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Kurokawa, Sadao, Tetsuo Fukunaga, Akinori Nagano,
and Senshi Fukashiro. Interaction between fascicles and
tendinous structures during counter movement jumping investigated in vivo. J Appl Physiol 95: 2306–2314, 2003. First
published July 18, 2003; 10.1152/japplphysiol.00219.2003.—
Behavior of fascicles and tendinous structures of the m.
gastrocnemius medialis (MG) was quantitatively examined
during human jumping in vivo. Eight male subjects performed maximal-effort counter movement jumping (CMJ)
motions. Kinematic and kinetic data were obtained using a
high-speed camera and a force platform. Behavior of fascicles
and tendinous structures was determined using ultrasonography and electromyography. Although the muscle-tendon
complex (MTC) shortened by only 1.6% during the downward
phase of the counter movement, fascicles shortened as much
as 10.4%. This shortening of fascicles caused elongation of
tendinous structures by 2.2%. Although the MTC remained
at almost constant length during the upward-I phase (⫺250
to ⫺100 ms before toe-off), fascicles shortened by 19.2% of the
initial length with an elongation of tendinous structures by
4.4%. The MTC shortened rapidly by 5.3% of the initial
length during the upward-II phase (⫺100 to 0 ms), whereas
fascicles shortened slightly during the first half of this phase
and contracted in a quasi-isometric manner during the latter
half of this phase. These findings implied that elastic energy
was stored in tendinous structures throughout the latter half
of the downward phase (1.0 J) and upward-I phase (5.6 J),
which was thereafter rapidly released during the upward-II
phase (3.8 J). It was found that muscle fibers of the MG were
not stretched during counter movement; therefore, stretch
reflex and potentiation of the contractile component of the
MG might not contribute to the work enhancement in CMJ.
It was suggested that the interaction between fascicles and
tendinous structures was essential in a generation of higher
joint power during the late push-off phase. This behavior of
the MTC of the MG in CMJ was quite similar to what was
observed in squat jumping performed without counter movement.
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
METHODS
Subjects and experimental protocol. Eight healthy male
subjects [age 23 ⫾ 5 yr old; height 1.72 ⫾ 0.10 m; body mass
68 ⫾ 11 kg; shank length (measured from the lateral malleolus to lateral epicondyle) 0.40 ⫾ 0.03 m (means ⫾ SD)]
participated in this study. All subjects gave an informed
consent to participate in the study. This study was approved
by the Ethics Committee of the University of Tokyo. After
warming-up, subjects were asked to jump vertically as high
as possible, with a counter movement starting from an erect
standing position. Their hands were kept on the hips
throughout the movement. Kinematic, kinetic, ultrasonography, and electromyography (EMG) data were obtained from
lower leg muscles during movements and at an erect standing position.
Kinematic and kinetic data collection. Retroreflective
markers were placed over the following anatomic landmarks
on the right side of the subjects: the fifth metatarsophalangeal joint, the lateral malleolus, the lateral epicondyle of the
knee, the tip of the trochanter major, and the glenohumeral
joint. Four body segments, i.e., feet, shanks, thighs, and HAT
(head, arms, and trunk), and angles of the joints connecting
those segments were identified with reference to these landmarks. During CMJ, subjects were filmed at 200 Hz from the
right side of the body (perpendicularly to the sagittal plane)
with a digital high-speed video camera (MEMRECAMc2s,
NAC). Vertical and fore-aft components of the ground reaction force, as well as the location of the center of pressure of
this force under the feet, were determined using a force
platform (Type 9281B, Kistler Instruments AG). These data
were stored into a personal computer system through an
J Appl Physiol • VOL
analog-to-digital converter (MacLab/8s, AD Instruments) at
a sampling frequency of 1 kHz.
Location of the five anatomic landmarks was automatically digitized using a motion analyzer software package
(Frame-DIAS, DKH). Digitized coordinates were low-pass
filtered at 8 Hz (bidirectional Butterworth digital filter) (47).
After synchronization of kinematic and kinetic data, instantaneous net joint moments around the ankle and knee joints
were calculated through inverse dynamics (49). Net joint
moments in the direction of plantar flexion and in the direction of knee extension were defined as positive and were
referred to as “plantar flexion moment” and “knee extension
moment,” respectively. Net joint power output was calculated
by multiplying net joint moment and joint angular velocity.
Ultrasonography. A real-time B-mode computerized ultrasonic apparatus (SSD-2000, Aloka) was used with an electronic linear array probe of 7.5-MHz wave frequency (UST
5710–7.5, Aloka) to obtain longitudinal ultrasonic images of
the MG during CMJ. The probe was fixed at a proximal part
of the lower leg (30%) between the popliteal crease and the
center of malleolus, at the midpoint of the mediolateral width
of the MG. The probe was carefully fixed on the skin surface
with a specially designed supporting device and elastic tape
to minimize noisy fluctuations. During CMJ (from 1,150 ms
before the toe-off to 100 ms after the toe-off), longitudinal
ultrasonic images of the MG were stored consecutively in the
cine-memory of the ultrasonic apparatus at 40 Hz. The ultrasonic images were synchronized with kinematic and kinetic data using a specially constructed trigger controller.
With these arrangements, it was possible to obtain echoes
reflected from interspaces among fascicles and from the superficial and deep aponeuroses of the MG on ultrasonic images. These images were stored frame by frame into a personal computer equipped with a video card.
Fascicle length was measured as the length of the echo
image that runs diagonally from the superficial to the deep
aponeurosis along the direction of fascicles (39). Fascicle
angle was determined as the average value of two angles; i.e.,
the angle between the deep aponeurosis and the line drawn
tangentially to the fascicle (␪deep) and the angle between the
superficial aponeurosis and the tangential line to the fascicle
(␪sup). These measurements were performed frame by frame
by means of an image processing and analysis application
software package [National Institutes of Health (NIH) image
1.60b, NIH]. The reproducibility of fascicle length and angle
determination has been evaluated in a preceding study (34,
35, 39). Measurements of fascicle lengths and angles were
repeated for three times on each ultrasonic image, and the
average value of the three measurements was used to represent the image. Coefficients of variation (CV) of three measurements were in the range of 0–4%.
EMG. Surface EMG was obtained from the MG, m. gastrocnemius lateralis (LG), m. soleus (Sol), and in some trials
m. tibialis anterior using bipolar Ag/AgCl electrodes (NEC
Medical System) with a constant interelectrode distance of 20
mm from the muscle belly. The electrodes were connected to
a preamplifier and a differential amplifier with a bandwidth
between 5 Hz to 1 kHz (1253A, NEC Medical System). EMG
signals were analog-to-digital converted at a sampling frequency of 1 kHz (MacLab/8s, AD Instruments) and stored
into a personal computer system for further analyses. Raw
EMG signal was high-pass filtered at 20 Hz, low-pass filtered
at 500 Hz, full-wave rectified, and smoothed using a bidirectional low-pass Butterworth digital filter with a cut-off frequency of 7 Hz to yield smoothed-rectified EMG (EMGSR).
EMGSR values were subsequently normalized relative to the
maximum value attained during CMJ.
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nous structures behave during human natural and
complex movements in vivo.
Muscle fibers are packed in fascicles that attach to
proximal and distal tendinous tissues on either end.
Intrafascicle muscle fibers are serially connected to
compose one functional unit, whose length is identical
to that of fascicles, although some muscle fibers taper
off to a point and terminate midfascicularly (35). Thus
a change of fascicle length corresponds to a change of
muscle fiber length. Recently, using ultrasonography,
we succeeded in determining the muscle architecture
(length and angle of fascicles) and elongation of tendinous structures of human muscles in vivo (20, 22, 35).
Kurokawa et al. (39) applied this methodology to investigate the behavior of the m. gastrocnemius medialis (MG) during human SQJ. They reported that fascicles shortened and tendinous structures were
stretched during the first phase of take-off and that
fascicles generated force quasi-isometrically, although
the MTC shortened rapidly during the last phase of
take-off. They concluded that the compliance of tendinous structures, together with no yielding of muscle
fibers, allowed the MTC to effectively generate relatively large power at the high joint angular velocity
region during the last part of push-off.
The purpose of this study was to quantitatively determine the mechanical output of fascicles and tendinous structures of the human MG during counter
movement vertical jump and to discuss the mechanism
of performance enhancement in CMJ compared with
SQJ (39).
2307
2308
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
MTC length, tendon length, and moment arm length. Instantaneous length of the MTC of the MG (LMTC), i.e., the
distance between the origin and insertion, was calculated by
substituting instantaneous ankle and knee joint angles into
the equations developed by Grieve et al. (26). Instantaneous
length of tendinous structures was determined based on a
geometrical MTC model proposed by Allinger and Herzog (2).
Properties of the fascicles and tendinous structures were
assumed to be uniform along the length of the MTC. It was
also assumed that all fascicles were parallel. Length of the
tendinous structures (LTS) was defined according to the following equation.
L TS ⫽ LMTC ⫺ Lfascicle 䡠 cos ␣
F tendon MG ⫽ c 䡠 共Mankle 䡠 d⫺1兲
F fascicles MG ⫽ Ftendon MG 䡠 cos ␣⫺1
where Mankle and d indicate the plantar flexion moment
generated by a single leg and the moment arm length of the
MG at the ankle joint, respectively.
Usually, the muscle stress component perpendicular to the
line of action of a muscle is not taken into account when
considering Hill’s muscle model. Additionally, the tensional
external mechanical work is not affected by this perpendicular component. Therefore, this muscle stress component
was not considered in this study.
Velocity, power, and work outputs of fascicles and tendon.
Velocity of the MTC, fascicles, and tendinous structures was
calculated by numerically differentiating the corresponding
length value with respect to time. Shortening direction of the
MTC, fascicles, and tendinous structures was defined as
positive. Mechanical power generated by the MTC and tendinous structures was calculated as a product of Ftendon MG
and shortening velocity of the MTC and tendinous structures, respectively. Ffascicles MG was multiplied with the velocity of fascicles to calculate mechanical power generated by
fascicles. Negative and positive mechanical work outputs
performed by the MTC, fascicles, and tendinous structures
were calculated by numerically time integrating the corresponding power values.
Statistical analysis. After synchronization of the variables
obtained as described previously, mean curve (⫾SE) of each
variable was calculated for the group of subjects.
For comparison of mechanical work outputs between CMJ
and SQJ, a Student’s paired t-test was used. The level of
significance was set at P ⬍ 0.05.
J Appl Physiol • VOL
Ankle and knee joint angles decreased gradually
until 175 and 225 ms before toe-off, respectively, and
then rapidly increased (Fig. 1). On the other hand, the
change in plantar flexion moment generated by both
legs was small during the downward movement phase.
Subsequently, plantar flexion moment increased gradually (peak value: 226 ⫾ 22 N 䡠 m at ⫺85 ms) and
thereafter rapidly decreased. Plantar flexion moment
changed in synchronization with the EMG activity of
plantar flexor muscles (peak of EMG of Sol was observed at around ⫺175 ms). Peak joint power of the
ankle generated by both legs (1,950 W) was observed at
⫺45 ms, whereas angular velocity of the ankle joint
was 81% of the peak value (14 rad/s) at that instant.
In the present study, three phases were distinguished during CMJ based on the movement of the
mass center of the body (MCB) and MTC (Fig. 2):
downward phase, from the start of downward movement of the MCB (⫺800 ms) to the start of the upward
movement of the MCB (⫺250 ms); upward-I phase,
from the start of the upward movement of the MCB to
the start of rapid shortening of the MTC (⫺100 ms);
and upward-II phase, from the start of rapid shortening of the MTC to toe-off (Fig. 2).
During the downward phase, the MTC shortened by
only 1.6% (7 mm) of the initial length, whereas fascicles shortened by 22.5% (15 mm) of the initial length,
and the tendinous structures were lengthened by 2.2%
(8 mm) of the initial length. Especially this elongation
of tendinous structures occurred predominantly in the
latter half of the downward phase, where fascicles
shortened actively by 12.1% of the initial length with
EMG activities of plantar flexor muscles. Shortening of
fascicles during the first half of the downward phase
was 10.4% of the initial fascicle length, which was
accompanied by small EMG activity of the plantar
flexors.
During the upward-I phase, the MCB was raised by
0.12 m. MTC length remained at an almost constant
value of 0.423 m, whereas fascicles were further shortened by 19.2% (13 mm) of the initial length, and the
tendinous structures were further stretched by 4.4%
(16 mm) of the initial length. During the upward-II
phase, the MCB continued moving upward and the
MTC shortened rapidly by 5.3% (22 mm) of the initial
length, whereas fascicles shortened by 5.2% (4 mm) of
the initial length. As a consequence, tendinous structures rapidly shortened by 5.2% (19 mm) of the initial
length. Especially during the latter half of this phase,
only a small amount of shortening of fascicles was
observed. Shortening of fascicles was accompanied by
an increase of fascicle angle.
Shortening velocity of MTC was almost zero (i.e.,
constant length) during the downward phase and upward-I phase because of the interaction between shortening of fascicles and lengthening of tendinous structures (Fig. 3). During the upward-II phase, shortening
velocity of fascicles decreased gradually to zero, and
the behavior of tendinous structures changed from
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where Lfascicle, ␣, and LMTC are fascicle length, fascicle angle,
and MTC length, respectively. Instantaneous moment arm
length of the MG at the ankle joint was calculated by referring to Bobbert et al. (11).
Fascicle and tendon force. Force applied to the Achilles
tendon was calculated as the quotient of plantar flexion
moment generated by a single leg and the moment arm
length of the MG at the ankle joint. It was assumed that
relative contribution of the force developed by the MG on the
Achilles tendon force was equal to the relative physiological
cross-sectional area (PCSA) of the MG among all plantar
flexors, represented as “c.” Also, it was assumed that the
ratio of tendon cross-sectional area of the MG in the Achilles
tendon can be represented by “c.” According to Fukunaga et
al. (23), averaged relative PCSA of the MG was 15.4% of the
total plantar flexors (c ⫽ 0.154). Instantaneous tendon force
developed by the MG (Ftendon MG) and tensional force of
fascicles of the MG (Ffascicles MG) were calculated as follows
RESULTS
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
2309
DISCUSSION
Fig. 1. Mean time history of joint angles (A), joint angular velocities
(B), joint moments (C), joint powers (D), moment arm length of the
gastrocnemius medialis (MG) at the ankle joint (E), as well as
normalized electromyography (EMG) activity from lower leg muscles
(F). Positive joint moment around the ankle joint and the knee joint
indicates ankle plantar flexion moment and knee extension moment,
respectively. Time is expressed relative to the instant of toe-off
(time ⫽ 0). Thin vertical bars indicate SE for 8 subjects. Sol, soleus;
LG, gastrocnemius lateralis; TA, tibialis anterior.
J Appl Physiol • VOL
The purpose of this study was to determine quantitatively the mechanical behavior (force and length
changes) of the MTC of the MG during CMJ compared
with SQJ (39). CMJ is a typical SSC exercise (38). It
has been generally considered in CMJ that agonist
MTCs are stretched through counter movement. The
MTC length of the biarticular MG is determined as a
result of interaction between ankle dorsi flexion and
knee flexion during downward phase (Fig. 1). In this
study, the biarticular MG shortened by 1.6 and 22.5%
of the initial length of MTC and fascicles in the downward phase, respectively (Fig. 2). Fascicle shortening of
the MG during the downward phase might be caused
through the following mechanism. At the erect standing position, fascicles might have already been in a
stretched position without elongation of tendinous
structures because of the relatively lower stiffness of
fascicles than that of tendinous structures (45). Active
shortening of fascicles associated with the increase of
joint moment during the downward phase, where
length of the MTC remained almost constant, occurred
due to the compliant nature of tendinous structures
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lengthening to shortening. Tendinous structures,
which were prestretched throughout the downward
phase and upward-I phase, began shortening rapidly
with a maximum value of 0.35 m/s at ⫺25 ms. Tendon
force corresponding to the tension of MG fibers attained the minimum value of 30 N at ⫺550 ms and
then increased to the peak value of 500 N at ⫺100 ms
and thereafter rapidly decreased during upward-II
phase. Time history of the force generated by fascicles
was similar to that of tendon force. The difference
between fascicle and tendon forces was remarkable
around ⫺100 ms because of the relatively large fascicle
angle.
During the downward phase, mechanical power generated by the MTC was almost zero. During upward-I
phase except for the last 25 ms, mechanical power of
the MTC remained near zero, because mechanical
power output of fascicles was approximately opposite
to that of tendinous structures (similar magnitude,
opposite sign). During upward-II phase, mechanical
power of fascicles decreased gradually and reached
zero in the latter half of this phase. Mechanical power
of tendinous structures and the MTC rapidly increased
and attained the peak value of 72 and 83 W, respectively, at ⫺50 ms.
Table 1 shows average mechanical work outputs
performed by the MTC, fascicles, and tendinous structures of the MG during three phases in CMJ. Absolute
value of work performed by tendinous structures during downward phase was small (1.0 J) compared with
work performed during upward-I phase (5.6 J) and
upward-II phase (3.8 J). Work performed by the MTC
during the downward phase was even smaller (0.3 J),
which was equivalent to the sum of positive work
performed by fascicles and negative work performed by
tendinous structures.
2310
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
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Fig. 3. Mean time history of force (B), velocity (A), and mechanical
power of the MTC, fascicles, and tendinous structures during counter
movement jumping (CMJ; C). Shortening of the MTC, fascicles, and
tendinous structures was defined as positive. Left vertical dotted
lines represent the start of the downward movement of the MCB.
Middle vertical dotted lines represent the start of upward movement
of the MCB. Right vertical dotted lines indicate the start of the rapid
shortening of MTC. Time is expressed relative to the instant of
toe-off (time ⫽ 0). Thin vertical bars indicate SE for 8 subjects.
Fig. 2. Mean time history of vertical displacement of mass center of
the body (MCB; A), muscle-tendon complex (MTC) length (B), fascicle
length (C), length of tendinous structures (D), and fascicle angle (E).
Left vertical dotted lines represent the start of the downward movement of the MCB. Middle vertical dotted lines represent the start of
the upward movement of the MCB. Right vertical dotted lines indicate the start of the rapid shortening of the MTC. Three phases were
defined as downward phase, upward-I phase, and upward-II phase.
Time is expressed relative to the instant of toe-off (time ⫽ 0). Thin
vertical bars indicate SE for 8 subjects.
J Appl Physiol • VOL
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2311
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
Table 1. Mechanical work output performed by the MTC, fascicles, and tendinous
structures of the MG during 3 phases in CMJ
CMJ
SQJ
CMJ
Downward
MTC
Fascicles
Tendinous
Mean
SE
0.3
1.4
⫺1.0
0.08
0.08
0.10
SQJ
CMJ
Upward-I
Mean
SE
SQJ
Upward-II
Mean
SE
Mean
SE
Mean
SE
Mean
SE
0.3
5.5
⫺5.6
0.17
0.18
0.86
0.2
4.8
⫺4.9
0.04
0.21
0.23
4.8
1.1
3.8
0.38
0.22
0.42
5.1
0.7
4.3
0.12
0.07
0.40
Values are mean and SE; n ⫽ 8. MTC, muscle-tendon complex; MG, gastrocnemius medialis; CMJ, counter movement jumping; SQJ, squat
jumping. Work measured in joules (J). Styles: CMJ and SQJ. Phases: downward, upward-I, and upward-II.
J Appl Physiol • VOL
(4, 38, 44). A major part of series elastic component is
located in tendinous structures (32). As shown in Fig. 2
and Table 1, only a little lengthening (8 mm) and
storage of elastic energy (0.3 J) were found in the
tendinous structures during the downward phase.
Fukashiro and Komi (21) as well as Bobbert et al. (9)
indicated that there was no substantial difference of
plantar flexion moment between CMJ and SQJ and
that joint moments peaked almost at the same time
during those motions. Table 1 summarizes the mechanical work outputs of the MTC, fascicle, and tendinous structure of the MG in CMJ compared with those
of SQJ (39) (in Ref. 39, the identical subjects as were
recruited in this study performed squat jumping motions under the identical experimental setup in the
same day). Positive work performed by the MTC, fascicles, and tendinous structures was calculated to be
5.4, 8.0, and 3.8 J in CMJ, and 5.3, 5.5, and 4.3 J in
SQJ, respectively. On the other hand, negative work of
them was calculated to be 0, 0, and ⫺6.6 J in CMJ, and
0, 0, and ⫺4.9 J in SQJ, respectively. Considering this
study and our previous study (39), total elastic energy
stored in, and released from, tendinous structures during CMJ was qualitatively (Fig. 2) and quantitatively
(Table 1) very similar to that of SQJ (P ⬎ 0.1). In the
MG, therefore, this mechanism may not contribute to
work enhancement through counter movement. Work
enhancement by making a counter movement in CMJ
might be mainly attributed to enhancement of muscular work output from monoarticular muscles.
On the other hand, it has been suggested that knee
extensors and plantar flexors during SSC exercise
(such as hopping and running) may behave in the
manner of concerted contraction, i.e., a contraction
where the MTC is lengthened but muscle fibers remain
isometric or even shortened during counter movement
(5, 29, 33). Thus, if concerted contraction could occur in
monoarticular muscles, there might be no work enhancements induced by potentiation and/or stretch reflex. Storage and reutilization of elastic energy by tendinous structures were expected as the result of concerted contraction. Further studies need to focus on the
behavior of fascicles and tendinous structures of monoarticular muscles such as Sol, vastus lateralis, and
gluteus maximus muscle during human natural/complex movements.
According to kinetic analysis, increase of MCB velocity during the upward-II phase was closely related to
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(Figs. 1 and 2). These results agreed well with those of
previous animal and human experiments (22, 27, 35).
It can be stated that neither MTC nor fascicles of the
MG had a stretching phase during the downward
phase in CMJ. In the previous study that investigated
SQJ, Kurokawa et al. (39) reported that the MTC and
fascicles of the MG shortened by 5 and 26% of the
initial length of the standing position. The shortenings
of the MTC and fascicles in CMJ were quite similar to
those of SQJ. Because the MG is a biarticular muscle,
it can be stated that its behavior during movements is
similar in both SQJ and CMJ.
Several possible mechanisms have been proposed to
account for the performance enhancement through
making a counter movement. The first one is that
counter movement results in the development of a
higher level of muscular force preceding the start of
concentric action (9). The second one is that active
muscles prestretched during the counter movement
store elastic energy, which is reused during the following concentric action (4, 8, 31, 38). The third one is that
prestretching of active muscle during the counter
movement alters the properties of the contractile machinery through the mechanism called “potentiation”
(13, 14, 17, 18), by which force generation by active
muscle is enhanced. The fourth one is that prestretching of active muscle during counter movement triggers
spinal reflexes (16, 46) as well as longer latency responses (42) that help increase muscle stimulation
during concentric action to the maximal level. To induce potentiation of the contractile machinery and/or
stretch reflex, muscle fibers have to be stretched during counter movement.
Results of the present study exhibited that fascicles
shortened by 22.5% of the initial length during counter
movement. Furthermore, enhancement of muscle stimulation in the MG was not observed in CMJ. It was
suggested that potentiation and/or stretch reflex induced by prestretch did not contribute to work enhancement through making a counter movement.
Thus, these two mechanisms (potentiation and stretch
reflex) might contribute to work enhancement through
counter movement only in the monoarticular plantar
flexor muscles (not in the biarticular MG) and more
proximal knee and hip extensor muscles.
Many researchers asserted that storage and reutilization of elastic energy help to enhance the maximum
work produced during the following concentric action
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MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
higher ankle joint power output (Fig. 1), i.e., a combination of high angular velocity of the ankle joint with
relatively large ankle plantar flexion moment (11).
This implies high shortening velocity of the MG with
large MTC force. This high-power output around the
ankle joint in upward-II phase is obtained as an interaction between the force-length-velocity relationship of
fascicles, tendon, and MTC. It is commonly known that
the length of sarcomere in vertebrate striated muscle
influences the force that can be generated (25). Figure
4 depicts the averaged sarcomere length-force relationship observed during CMJ/SQJ and force-length relationship of human muscle derived from the data of
Walker and Schrodt (48). Sarcomere length was estimated by dividing the fascicle length by the average
number of sarcomeres in series within the fascicle (11).
As fascicles generated relatively large force during
CMJ, sarcomeres operated over the plateau and upper
part of the ascending limb of the force-length relationship where fascicles could generate more than 75% of
the maximal force. Kawakami et al. (36) indicated that
the MG and Sol operated over the plateau and upper
part of the ascending/descending limbs of the forcelength relationship under passive condition of plantar
flexors. However, when the MG and Sol contracted in
an isometric manner with a maximal effort, the state of
the system moved into the ascending limb of the forcelength curve because of the fiber shortening. Considering the results of Kawakami et al. (36), the MG operated
in the optimal region of the force-length relationship in
natural human movements. Similar phenomena have
been reported during wallaby hopping (Fig. 6 of Ref. 7).
This condition is advantageous for muscle fibers to
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Fig. 4. Average sarcomere force-length relationship observed during
CMJ (B) and squat jumping (SQJ; A) (39). Average sarcomere length
during CMJ and SQJ was estimated and superimposed on the
force-length relationship for human muscle derived from the data
reported in Walker and Schrodt (48). During CMJ, the MG operated
over the shaded portion of sarcomere force-length relationship where
more than 75% of maximum force is generated. This phenomenon is
identical to what has been observed in SQJ (39).
generate relatively high force, which is required to
accelerate the MCB during the latter half of the pushoff phase, despite the slightly lower maximum force
generation at the initial length.
On the other hand, it is well known that force generation capability of muscle fibers decreases with increasing shortening velocity of muscle fibers. During
upward-II phase, where relatively large force was required, shortening velocity of fascicles began decreasing and became near zero (Fig. 3). This is realized as an
effect of the compliant nature of tendinous structures,
which allows fascicles to generate large force. Also,
high shortening velocity of the MTC during upward-II
phase predominantly comes from shortening of tendinous structures, of which peak shortening velocity was
three times as high as the corresponding velocity of
fascicles. This high shortening velocity of the tendinous
structures was realized by elastic recoil (Figs. 2 and 3)
so called “catapult action” (30). Thus, interaction between fascicles and tendinous structures is essential in
building up a combination of high shortening velocity
of the MTC with relatively large fascicle force. It can be
stated that the behavior of the MTC during CMJ was
mechanically quite similar to that of SQJ (39).
The possibility of energy storage in elastic structures
has been discussed in the literature (1, 12, 28). Although this issue has been well documented for animals (7, 13), more speculative discussions have been
reported for humans. In recent studies (15, 29, 31),
series elastic stiffness of human plantar flexors was
measured in vivo with the quick release method, and
thereby elastic energy stored in the triceps surae was
calculated during walking, running, and jumping. Hof
(29) found a stretch of series elastic components corresponding to ⬃0.52 rad with a joint moment of 114 N 䡠 m,
which is equivalent to a strain of 8% assuming a
moment arm length of 50 mm and a total length of
tendinous structures of 350 mm. De Zee and Voigt (15)
also found a stretch of ⬃0.3 rad with a moment of 104
N 䡠 m, which is equivalent to a strain of 4.3% using the
same assumptions. In this study, we found a strain of
6.6% with the peak plantar flexion moment of 113
N 䡠 m, which was generated by a single leg during CMJ.
A strain value of 6.6% found during CMJ lay in the
range between values reported in these preceding studies. Additionally, assuming that the distribution of
muscle force among plantar flexors is proportional to
their PCSAs, recalculation of the data reported by Hof
(29, 31) revealed that the amount of elastic energy
stored in the tendinous structures of MG in SQJ and
slow running was roughly of the same magnitude as
that during CMJ. The result of this study indicates
that energy saving by elastic energy occurs during
human natural jumping and running.
An unavoidable limitation of inverse dynamics is
that MG, LG, Sol, and other plantar flexors cannot be
considered separately. The force generated by the muscle fiber is determined by the PCSA, muscle activation,
length, and shortening velocity. Additionally, the muscle architecture (e.g., fiber length/tendinous length ratio) might affect the force-generating properties of the
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
J Appl Physiol • VOL
as power amplifier. The interaction between fascicles
and tendinous structures has an essential role when
considering the generation of higher joint power during
late push-off phase.
REFERENCES
1. Alexander RM and Bennet-Clark HC. Storage of elastic
strain energy in muscle and other tissues. Nature 265: 114–117,
1977.
2. Allinger T and Herzog W. Calculated fiber length in cat gastrocnemius muscle during walking. In: Proc NACOBII The Second North American Congress on Biomechanics. Chicago, IL:
University of Chicago, 1992, p. 81–82.
3. Anderson FC and Pandy MG. Storage and utilization of elastic strain energy during jumping. J Biomech 26: 1413–1427,
1993.
4. Asmussen E and Bonde-Petersen F. Storage of elastic strain
energy in skeletal muscle in man. Acta Physiol Scand 91: 385–
392, 1974.
5. Belli A and Bosco C. Influence of stretch-shortening cycle on
mechanical behaviour of triceps surae during hopping. Acta
Physiol Scand 144: 401–408, 1992.
6. Bergel DN, Brown MC, Butler RG, and Zacks RM. The effect
of stretching a contracting muscle on its subsequent performance
during shortening. J Physiol 225: 21–22, 1972.
7. Biewener AA, Konieczynski DD, and Baudinette RV. In
vivo muscle force-length behavior during steady-speed hopping
in tammar wallabies. J Exp Biol 201: 1681–1694, 1998.
8. Bobbert MF. Dependence of human squat jump performance on
the series elastic compliance of the triceps surae: a simulation
study. J Exp Biol 204: 533–542, 2001.
9. Bobbert MF, Gerritsen KGM, Litjens MCA, and Soest van
AJ. Why is counter movement jump height greater than squat
jump height? Med Sci Sports Exerc 28: 1402–1412, 1996.
10. Bobbert MF, Huijing PA, and Ingen Schenau GJ van. An
estimation of power output and work done by the human triceps
surae muscle-tendon complex in jumping. J Biomech 19: 899–
906, 1986.
11. Bobbert MF, Huijing PA, and Ingen Schenau GJ van. A
model of the human triceps surae muscle-tendon complex applied to jumping. J Biomech 19: 887–898, 1986.
12. Butler DL, Grood ES, Noyes FR, and Zernicke RF. Biomechanics of ligaments and tendons. In: Exercise Sports Science
Reviews, edited by Hutton RS. Philadelphia, PA: The Franklin
Institute Press, 1978, p. 125–181.
13. Cavagna GA and Citterio G. Effect of stretching on the elastic
characteristics and the contractile component of frog striated
muscle. J Physiol 239: 1–14, 1974.
14. Cavagna GA, Dusman B, and Margaria R. Positive work
done by a previously stretched muscle. J Appl Physiol 24: 21–32,
1968.
15. De Zee M and Voigt M. Moment dependency of the series
elastic stiffness in the human plantar flexors measured in vivo.
J Biomech 34: 1399–1406, 2001.
16. Dietz V, Schmidtbleicher S, and Noth J. Neuronal mechanisms of human locomotion. J Physiol 238: 139–155, 1978.
17. Ettema GJC, Huijing PA, and Haan de A. The potentiating
effect of prestretch on the contractile performance of rat gastrocnemius medialis muscle during subsequent shortening and isometric contractions. J Exp Biol 165: 121–136, 1992.
18. Ettema GJ, Soest van AJ, and Huijing PA. The role of series
elastic structures in pre-stretch-induced work enhancement during isotonic and isokinetic contractions. J Exp Biol 154: 121–
136, 1990.
19. Fellows SJ and Rack PMH. Relation of the length of the
electrically stimulated human biceps to elbow movement.
J Physiol 376: 58, 1986.
20. Fukashiro S, Ito M, Ichinose Y, Kawakami Y, and Fukunaga T. Ultrasonography gives directly but noninvasively elastic characteristics of human tendon in vivo. Eur J Appl Physiol
71: 555–557, 1995.
95 • DECEMBER 2003 •
www.jap.org
Downloaded from jap.physiology.org on March 16, 2008
muscle (50). In this study, the information regarding
the factors determining the force sharing among plantar flexors is not available except for the MG. Therefore, in this study, the force sharing among plantar
flexors was determined simply according to the ratio of
PCSA. This methodology has been commonly used in
previous studies by many researchers (31). In reality,
however, there is a possibility that the distribution of
muscle forces among plantar flexor muscles might not
be proportional to their PCSAs during push-off phase
in jumping. The shortening velocity of the MTC of the
m. gastrocnemius is lower than that of the MTC of the
Sol during the upward-I and -II phases in jumping.
This difference is caused by the reducing influence of
knee extension on the shortening velocity of the biarticular m. gastrocnemius MTC. This influence might
cause the shortening velocity of the muscle fiber of m.
gastrocnemius to be lower than that of the muscle
fibers of monoarticular plantar flexors such as the Sol.
Therefore, there is a possibility that m. gastrocnemius
could contribute relatively greater force during the
upward-I and -II phases in jumping (i.e., using only the
ratio of PCSA may lead to an underestimation of the
force and power contribution of the MG during the
upward-I and -II phases in jumping). On the contrary,
during downward phase, the MTC of the Sol lengthened, whereas the MTC of the m. gastrocnemius shortened slightly. Furthermore, the m. gastrocnemius is
more compliant than the Sol because of the higher
tendinous structure length and muscle fiber length
ratio in the MG (50). Hence, the muscle fibers of the m.
gastrocnemius could contract faster than the muscle
fibers of the Sol and other plantar flexors; thereby the
contribution of muscle force generated by the m. gastrocnemius might be lower than that of Sol and other
plantar flexors during the downward phase (i.e., using
only the ratio of PCSA may lead to an overestimation of
the force and power contribution of MG during the
downward phase). However, as the length measurements are assumed to be reliable and the muscle force
and tendon force are roughly equivalent, the general
characteristics of Figs. 3 and 4 will remain unaltered.
Consequently, the interpretation of the functional role
of muscle fibers and tendinous structures will remain
unchanged in the MG.
To summarize the findings of this study, mechanical
power generated by fascicles of MG is absorbed in
tendinous structures and stored in them as elastic
energy during the downward phase and upward-I
phase. Subsequently, this elastic energy is reused during upward-II phase where high peak power of tendinous structures and the MTC was observed. The rate
at which elastic energy was released by tendinous
structures during upward-II phase is higher than the
rate at which it was stored into tendinous structures by
shortening of fascicles during downward phase and
upward-I phase. These results support the suggestion
reported in previous studies (1, 8, 10, 30, 31, 41).
Therefore, it follows from the present investigation
that fascicles function as force generator and tendinous
structures function not only as energy storage but also
2313
2314
MUSCLE-TENDON COMPLEX DESIGNED FOR COUNTER-JUMPING
J Appl Physiol • VOL
36. Kawakami Y, Kumagai K, Huijung PA, Hijikata T, and
Fukunaga T. The length-force characteristics of human gastrocnemius and soleus muscle in vivo. In: Skeletal Muscle Mechanics: From Mechanisms to Function, edited by Herzog W.
New York: John Wiley and Sons, 2000, p. 327–341.
37. Komi PV. Stretch-shortening cycle. In: Strength and Power in
Sport, edited by Komi PV. Oxford, UK: Blackwell Scientific,
1992, p. 169–179.
38. Komi PV and Bosco C. Utilization of stored elastic energy in
leg extensor muscle by men and women. Med Sci Sports Exerc
10: 261–265, 1978.
39. Kurokawa S, Fukunaga T, and Fukashiro S. Behavior of
fascicles and tendinous structures of human gastrocnemius during vertical jumping. J Appl Physiol 90: 1349–1358, 2001.
40. Lieber RL, Leonard ME, Brown CG, and Trestik CL. Frog
semitendinosis tendon load-strain and stress-strain properties
during passive loading. Am J Physiol Cell Physiol 261: C86–C92,
1991.
41. Marsh RL and John-Alder HB. Jumping performance of hylid
frogs measured with high-speed cine film. J Exp Biol 188: 131–
141, 1994.
42. Melvill Jones G and Watt DGD. Observation on the control of
stepping and hopping movements in man. J Physiol 219: 702–
727, 1971.
43. Muhl ZA. Active length-tension relation and effect of muscle
pennation on fiber lengthening. J Morphol 173: 285–292, 1982.
44. Svantesson U, Ernstoff B, Bergh P, and Grimby G. Use of a
Kin-Com dynamometer to study the stretch-shortening cycle
during plantar flexion. Eur J Appl Physiol 62: 415–419, 1991.
45. Trestik CL and Lieber RL. Relationship between Achilles
tendon mechanical properties and gastrocnemius muscle function. J Biomech Eng 115: 225–230, 1993.
46. Voigt M, Dyher-Poulesen P, and Simonsen EB. Modulation
of short latency stretch reflexes during human hopping. Acta
Physiol Scand 163: 181–194, 1998.
47. Voigt M, Simonsen EB, Dyhre-Poulsen P, and Klausen K.
Mechanical and muscular factors influencing the performance in
maximal vertical jumping after different prestretch loads. J Biomech 28: 293–307, 1995.
48. Walker SM and Schrodt GR. I Segment length and thin
filament period in skeletal muscle fibers of the Rhesus monkey
and the human. Anat Rec 178: 63–82, 1974.
49. Winter DA. Kinetics: forces and moments of force. In: Biomechanics and Motor Control of Human Movement (2nd ed.). New
York: John Wiley and Sons, 1990, p. 75–102.
50. Zajac FE. Muscle and tendon: properties, models, scaling, and
application to biomechanics and motor control. Crit Rev Biomed
Eng 17: 359–411, 1989.
95 • DECEMBER 2003 •
www.jap.org
Downloaded from jap.physiology.org on March 16, 2008
21. Fukashiro S and Komi PV. Joint moment and mechanical
power flow of the lower limb during vertical jump. Int J Sports
Med 8: 15–21, 1987.
22. Fukunaga T, Ichinose Y, Ito M, Kawakami Y, and
Fukashiro S. Determination of fascicle length and pennation
angle in a contracting human muscle in vivo. J Appl Physiol 82:
354–358, 1997.
23. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, and Edgerton VR. Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80: 158–165, 1996.
24. Gollhofer A, Strojnik V, Rapp W, and Schweizer L. Behavior of triceps surae muscle-tendon complex in different jump
conditions. Eur J Appl Physiol 64: 283–291, 1992.
25. Gordon AM, Huxley AF, and Julian FJ. The variation in
isometric tension with sarcomere length in vertebrate muscle
fibers. J Physiol 184: 170–192, 1966.
26. Grieve DW, Pheasant S, and Cavanagh PR. Prediction of
gastrocnemius length from knee and ankle joint posture. In:
Biomechanics VI-A, International Series on Biomechanics, edited
by Asmussen E and Jorgensen K. Baltimore, MD: University
Park, 1978, p. 405–412.
27. Griffiths RI. Ultrasound transit time gives direct measurement
of muscle fiber length in vivo. J Neurosci Methods 21: 159–165,
1987.
28. Hof AL. Effects of muscle elasticity in walking and running. In:
Multiple Muscle Systems, edited by Winters JM and Woo SL-Y.
New York: Springer-Verlag, 1990, p. 591–607.
29. Hof AL. In vivo measurement of the series elasticity release
curve of human triceps surae muscle. J Biomech 31: 793–800,
1998.
30. Hof AL, Geelen BA, and Van den Berg J. Calf muscle moment, work and efficiency in level walking: role of series elasticity. J Biomech 16: 523–537, 1983.
31. Hof AL, van Zandwijk JP, and Bobbert MF. Mechanics of
human triceps surae muscle in walking, running and jumping.
Acta Physiol Scand 173: 17–30, 2002.
32. Huijing PA. Elastic potentiation of muscle. In: Strength and
Power in Sports, edited by Komi PV. Oxford, UK: Blackwell,
1991, p. 151–168.
33. Jacobs R, Bobbert MF, and Ingen Schenau GJ van. Function of mono- and bi-articular muscles in running. Med Sci
Sports Exerc 25: 1163–1173, 1993.
34. Kawakami Y, Abe T, and Fukunaga T. Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles.
J Appl Physiol 74: 2740–2744, 1993.
35. Kawakami Y, Ichinose Y, and Fukunaga T. Architectural
and functional features of human triceps surae muscles during
contraction. J Appl Physiol 85: 398–404, 1998.