|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online October 18, 2006
Journal of Experimental Biology 209, 4379-4388 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02434
Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion
1 Structure and Motion Laboratory, Institute of Orthopaedics and
Musculoskeletal Sciences, University College London, Royal National Orthopedic
Hospital, Brockley Hill, Stanmore, Middlesex, HA7 4LP, UK
2 Structure and Motion Laboratory, The Royal Veterinary College, Hawkshead
Lane, North Mymms, Hatfield, Hertfordshire, AL9 7TA, UK
* Author for correspondence (e-mail: glichtwark{at}rvc.ac.uk)
Accepted 10 July 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: walking, running, efficiency, Vmax, elasticity
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Ker et al., 1987;
Fukunaga et al., 2001). To
achieve versatility, however, the amount of energy stored in the elastic
tissues must be modulated by muscular contraction. Here we investigate how the
muscle fascicles of the gastrocnemius medialis (GM) interact with the elastic
Achilles tendon (AT) to achieve this versatility under different locomotion
conditions.
Although there are energetically optimal speeds for each type of
terrestrial gait, animals need to perform these gaits under a wide range of
conditions. These include differing speeds, accelerations and terrains. Each
of these different conditions requires altered forces and moments at each
joint to maintain steady locomotion
(Roberts and Scales, 2004;
Roberts and Belliveau, 2005).
Therefore the muscles responsible for producing these forces are required to
have a versatile mechanical function. Muscles must have the ability to either
produce or absorb work at different periods of the stride depending on the
conditions of locomotion. For instance, it has been demonstrated that during
downhill running, the turkey gastrocnemius muscle absorbs work and,
conversely, is required to generate power during uphill running
(Gabaldon et al., 2004).
Similarly, these muscles must produce more work in proportion to acceleration
on level ground (Roberts and Scales,
2004).
The ability of a muscle to perform or absorb mechanical work is highly
dependent on interactions between the muscle's contractile component and the
elastic structures that it attaches to. Compliant tendons and aponeurosis
enable fascicle length changes to be uncoupled from that of the whole
muscle-tendon unit (MTU) length
(Griffiths, 1991;
Fukunaga et al., 2000).
Numerous investigations on different terrestrial species have demonstrated
that during locomotion, the ankle extensor muscles act nearly isometrically
(constant length) or concentrically (shorten) whilst the whole MTU lengthens
(Griffiths, 1991;
Ishikawa et al., 2005;
Fukunaga et al., 2001;
Hof et al., 2002;
Lichtwark and Wilson, 2005d).
This acts to stretch the relatively compliant tendon of this muscle group
during the stance phase. Because tendon is an elastic material, energy is
stored in the tendon whilst it is stretched and this energy is returned late
in the stance phase when the tendon (and subsequently the entire MTU) shortens
rapidly. This is elegantly demonstrated in a recent publication by Ishikawa
and colleagues (Ishikawa et al.,
2005), who simultaneously recorded length changes of the human MG
and soleous muscles along with direct measures of AT force to demonstrate the
catapult action of these muscles acting on the tendon.
Utilisation of elastic strain energy within the series elastic element has
been suggested to make muscles more efficient, particularly during cyclical
movements like locomotion (Roberts,
2002; Lichtwark and Wilson,
2005b). Tendon stretch and recoil reduces the mechanical work
required from muscle fascicles, and also allows muscle fascicles to operate at
speeds more favourable for work production and efficiency. By performing near
isometric contractions during the stance phase of gait when the MTU is
stretching, a muscle reduces both the mechanical work required and the excess
heat involved in shortening a muscle
(Ettema, 2001;
Lichtwark and Wilson, 2005a).
In addition, high MTU speeds can be achieved in excess of the maximum fascicle
velocities. The high speeds of recoil of tendon and other series elastic
structures prevents the muscle from operating at unfavourable high velocities
during the take-off phase of the stride.
To better understand the mechanics and energetics of human muscle
contraction it is important to distinguish the roles of the contractile
components and also the elastic components. Here we have combined ultrasound
imaging and motion analysis techniques to assess the length changes of the GM
fascicles, the entire series elastic element and the AT during locomotion
under different incline conditions and with different gaits (walking and
running). These techniques allow us to assess the contribution of this muscle
to force production during gait. By varying the grade of incline and the speed
of locomotion (and the gait) we have varied the net external mechanical work
produced by the body (Gabaldon et al.,
2004) and hence been able to study how GM muscle mechanics alter
under these different conditions. We hypothesised that the GM muscle fascicles
will interact differently with the AT as a result of changes in the required
external work.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Participants were asked to walk (at 5 km h-1) and run (at 10 km h-1) on a treadmill at different grades while measurements were made. Participants walked at grades of -10, 0 and 10% (negative grades indicate decline/downhill) and ran at grades of 0 and 10%. A walking warm-up period of 2 min was initially used and a period of 1 min was allowed at each condition for the participant to normalise their gait. This period preceded two 10 s data collection periods for walking and one 10 s collection period for running, which ensured that at least ten strides of good data were collected for each individual. The order of the walking and running and the grades of incline were randomised between subjects. This protocol was applied twice in the same session so that muscle fascicle and tendon length measurements could be made using one ultrasound machine.
Kinematics and muscle activity
Active CODA light emitting diodes (LEDs) were attached to the following
body landmarks: head of the fifth metatarsal, calcaneous, lateral malleolus,
head of the fibula, lateral epicondyle of the knee, iliotibial band (halfway
between knee marker and greater trochanter) and the greater trochanter
(Fig. 1B). The three
dimensional (3D) position of these LEDs was determined with an accuracy of
±1 mm by using a CODA motion analysis system (Charwood Dynamics,
Rothley, Leics, UK) at rate of 100 Hz. Simultaneous muscle activity was
measured using EMG and collected with a sampling frequency of 2000 Hz into the
16-bit A/D board of the CODA system.
|
), with
shank length defined as the length of the lower length segment as defined
above. This calculation assumes a rigid foot and ignores any shape change or
compression of the foot during the stance phase. The vertical velocity of the calcaneus marker was used to determine when the foot contacted the ground. Foot contact was defined as the time when the vertical velocity crossed from negative to positive. The beginning of swing phase was defined as the time when the calcaneus marker had a positive vertical velocity and the fifth metatarsal marker changed from a negative to a positive horizontal velocity. This technique provided a consistent predictor of the time of foot on and foot off under the conditions of both walking and running.
Electromyography (EMG) was used to assess the muscle activity of the GM and its antagonist, the tibialis anterior. Surface electrodes were placed on the muscle bellies of the GM and TA using round bipolar electrodes (12 mm diameter, 18 mm spacing) with reference electrodes placed in between. The EMG signals were preamplified at the source with a frequency bandwidth of 20 Hz-20 kHz (MA-310-surface EMG, Motion Lab Systems, Inc, Los Angeles, CA, USA) and synchronously collected with the motion analysis data at 2000 Hz. The EMG data were rectified and low pass filtered with a fourth order, 5 Hz low pass Butterworth filter to create an EMG envelope.
Ultrasound measurement 1 - muscle fascicle and angle
A PC based ultrasound system (Echoblaster 128, UAB `Telemed', Vilnius,
Lithuania) was used to image the GM muscle fascicles and also the
muscle-tendon junction. We used a 128-element, linear, multifrequency
ultrasound probe at a frequency of 7 MHz and with a field of view of 60 mm in
B-mode. Images were collected at 25 frames s-1.
The probe was attached to the GM muscle such that it imaged a sagittal
section to the leg. The probe was aligned to the midline of the muscle so that
it was approximately in the same plane that the muscle fascicles ran in
(Fig. 1A). Measurements of
muscle fibre length and pennation angle were made at a mid-belly position as
described in previous work (Lichtwark and
Wilson, 2005d). During measurements the rotation of the probe was
minimised due to the flat shape of the probe (approximate range of 10°
rotation relative to the leg axis frame) and the image plane stayed in good
alignment with the muscle fascicles. This was assessed by continuous, clear
fascicle images obtained throughout the entire period of each stride. A
digital output signal from the CODA motion analysis system that signified when
data were being collected was passed to a control signal generator. The signal
generator produced a 5 MHz pulse (amplitude 2.5 V) that was fed to a
sonomicrometry crystal attached to the probe (Sonometrics Corp., London, ON,
Canada) along the cable of the ultrasound probe. This produced a white signal
on the bottom of the ultrasound image for a short period of time and thus
allowed synchronisation between the motion analysis and ultrasound data.
Ultrasound measurement 2 - Achilles tendon length
AT length was measured as the distance from the calcaneous marker to the
projected 3D position of the GM muscle-tendon junction (MTJ)
(Fig. 1B). This was done by
using the same ultrasound probe as previously mentioned to image the two
dimensional position of the MTJ and tracking the movement of the probe so that
the two dimensional measurement could be projected into the 3D laboratory
space (Fig. 1A). This
technique, including accuracy determination, is detailed elsewhere
(Lichtwark and Wilson, 2005c).
The position and orientation of the probe was determined using three CODA
markers rigidly attached to the probe. The position of the image relative to
these markers was predetermined such that measurements made in this plane
could be embedded back into the 3D laboratory space - the projected 3D
position of the GM MTJ. This measurement was made in separate trials to those
of the muscle fascicle length and pennation angle for all conditions. A stick
figure animation of the leg and the AT length measurement during walking is
shown in supplementary material (Animation 1).
The AT length change was measured relative to the slack length. The slack
length of each individual was defined as the average length (across all
strides) of the AT at toe-off for the level walking condition. This was
calculated for each participant. This event was chosen because the Achilles
tendon force should have dropped to zero at foot-off and hence there will be
both zero stress and zero strain (Ishikawa
et al., 2005; Komi,
1990). AT strain was calculated from the length change of the
tendon divided by the slack length.
Series elastic element and aponeurosis length measurement
The length of the series elastic elements (SEE, including tendon and
aponeurosis) was determined by subtracting the length of the muscle fascicles
in the direction of the tendon from the change in whole muscle-tendon unit
length:
 | (1) |
where LSEE is the length of the SEE,
LFascicle is the length of the muscle fascicle and 
is the pennation angle (Fukunaga et al.,
2001; Lichtwark and Wilson,
2005d). Length change of the SEE was reported relative to the
average length of the SEE at toe-off for each condition.
An approximation of the total stretch of the combined proximal tendon and
the aponeurosis in series with the muscle was also made as follows:
 | (2) |
where 
LAPO is the length change of the
aponeurosis plus the proximal tendon and LAT is the
length change of the AT using the previously described ultrasound method.
Statistical analysis and force estimations
Muscle fascicle length and pennation angle were recorded for three strides
for each participant and each incline condition. AT length was recorded
simultaneously with joint angles, whole muscle length and EMG data for five
complete strides for each participant and each incline condition. All of these
data were interpolated to 100 points across each individual stride (from one
heel contact to the next) and an average for each participant and each
condition was determined at each one percent of the stride. The data from each
participant were then pooled to get a group average and standard error for
each variable across one complete stride.
Individual mean values for each condition were evaluated using a general linear model in Statistica v 6.0 (Statsoft Inc, Tulsa, OK, USA). Gait and incline were analysed as fixed factors and subject as a random factor since the mean value of dependent variables varied between subjects, but we were not interested in determining the actual properties for the individual subjects. In the analysis comparing walking and running we only used data collected on flat and incline (and had slope as a fixed factor). In the analysis of slope, we created two separate models; one using the data for walking and one using the data for running. For the walking state we then undertook two post hoc paired t-tests comparing the data for incline and decline to the data for level walking. Dependent variables were evaluated independently. A P-value of 0.05 was taken as indicating statistical significance except in the post hoc tests, where a P-value of 0.025 was taken to indicate significance, since two comparisons were performed.
An approximate average AT force (FAT) was estimated for
each condition using the average length change of the AT
(LT) and the average stiffness of the AT (k
180
N mm-1) as calculated elsewhere
(Lichtwark and Wilson, 2005c)
using the same method of length measurement:
 | (3) |
The contribution of the GM to the total AT force was estimated based on the
physiological cross-sectional area (PCSA) of this muscle relative to all other
plantar flexors (Kurokawa et al.,
2003). An average PCSA of 15.4% of the total PCSA has been
estimated (Fukunaga et al.,
1992) and therefore the force contribution of the GM
(FGM) was calculated as follows:
 | (4) |
The average force applied by the muscle fascicles
(FFascicle) was then calculated in the direction of the
muscle fascicles as measured by the pennation angle () at each time
instant and therefore the GM fascicle force were calculated as follows:
 | (5) |
Fascicle length was normalised (LFo) to a resting
fascicle length of 60 mm (mean fascicle length at foot contact during walking
trials) and average fascicle force was normalised (FFo) to
a maximum isometric force of 1200 N, based on a physiological cross-sectional
area of 42 cm2 and an average pennation angle of 15°
(Narici, 1996). The average
instantaneous velocity of the muscle fascicles (VFascicle)
was also calculated by differentiating the average relative fascicle length
with respect to time (LFo s-1).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
Muscle fascicle length, pennation angle and excitation
The average change in muscle fascicle length and pennation angle for each
grade during both walking and running is shown in
Fig. 3. In both walking and
running stance phase, incline seemed to make little difference to how the
muscle fascicles changed length and pennation angle. The results indicate that
slope had no significant effect on the length of the muscle fascicles at mid
stance phase for both walking and running (P=0.2 and P=0.3,
respectively, at 50% stance). Mean (± s.e.m.) walking muscle fascicle
length at mid stance was 56.8±2.3 mm, 57.7±2.3 mm and
58.1±2.3 mm for downhill, flat and uphill walking, respectively, while
running fascicle lengths were 53.4±1.7 mm and 54.5±1.5 mm for
flat and uphill running, respectively. During the running conditions the
muscle fascicles were on average 4 mm shorter at heel strike and 6.5 mm
shorter at toe-off than for walking; however, this was not statistically
significant (P=0.07 and P=0.09, respectively). The fascicles
also shortened more through the stance phase, in contrast to the walking
conditions where muscle fibres acted relatively isometrically except at
initial heel strike and just prior to toe-off. The muscle fascicles shortened
to a mean of 40.1±0.6 mm during the swing phase for both running
conditions, whilst the shortest mean muscle fascicle length for the walking
conditions was 44.1±1.0 mm (P=0.02).
|
The GM muscle fascicles actively shortened while the whole MTU lengthened during the first half of the stance phase. When the GM began to deactivate, the muscle fascicles shortened along with the MTU in both walking and running. In both gaits, the EMG signal from the GM increased throughout stance until the MTU began to shorten. In walking the total GM EMG level increased with incline, whilst the maximum EMG level was similar in both running conditions. The tibialis anterior EMG signal showed some coactivation with the GM muscle at the beginning of the stance phase in both walking and running, and also at the end of the swing phase during running.
There was little variation in pennation angle with the change in incline for both walking and running (P=0.12 and P=0.20, respectively). However, the muscle fascicles acted at a significantly higher pennation angle during running than for walking (P=0.001), with a maximum pennation angle of 20.8±1.0° in running compared to 17.5±1.2° in walking. During walking at all grades the muscle fascicles acted at a relatively constant pennation angle throughout stance with a mean range of 4.4±0.8°, compared to a running range of 5.8±0.7°. The relationship between muscle fascicle length and pennation angle is shown in Fig. 4. We found an inverse linear relationship between muscle fascicle length and pennation angle; however, there were differences between shortening and lengthening of the muscle fascicles and also some difference between walking and running conditions.
|
|
Achilles tendon and SEE length changes
The length change of the AT across the gait cycle for all conditions
(Fig. 5) showed that a greater
stretch is achieved during running than walking. There was little difference,
however, between maximum length changes with changes in grade. The average
maximum strain measured during the walking conditions was 4.6%
(10.9±1.7 mm, mean ± s.e.m.), whilst it averaged 5.8%
(13.8±1.4 mm) during the running conditions, which was not found to be
significant (P=0.11). The uphill conditions for both walking and
running, however, showed a longer length of the AT throughout the first half
of stance phase compared to the level results (P=0.002 and
P=0.01 for walking and running, respectively, at 25% of stance). The
post hoc t-test found this difference to be significant only between
the flat and uphill conditions (P=0.01). The AT length shortened to
below the slack length before the approximate toe-off in both running
conditions. The results also show that the AT was strained during the swing
phase with an average maximum strain of 2.9% during walking and 3.8% during
running (P=0.14).
|
Fig. 5 also shows the estimated change in length of the SEE for each condition. The SEE stretched in a similar way to that of the AT; however, the amplitude of the total length change was greater in the SEE. The maximum stretch for all grade conditions in both walking and running was similar, with a higher strain achieved during the running trials. The maximum length change estimated with the model was 23.4 mm during walking and 25.2 mm during running. This estimate is based on a zero length for each condition, defined as the length measured at toe-off under that condition, rather than a fixed zero length for the SEE. Subtraction of the AT length change from the overall SEE length change gave an estimate of other elastic strain (aponeurosis, proximal tendon, other muscle fascia), termed aponeurosis strain for simplicity. The estimated maximum length changes in the aponeurosis were similar for both walking and running, with an average maximum elongation of 13.8 mm and 12.8 mm, respectively (Fig. 5).
Muscle work
The average length change of the muscle fascicle relative to the average
length change of the tendon during the stance phase for each condition is
shown in Fig. 6. The
approximate force applied by the muscle fascicles, calculated using the
stretch of the AT and Eqn 3-5, is also shown. The length of the muscle
fascicles during the rise of force was different for each condition. As grade
increased for both gait types, the muscle fascicle length during force
production increased. The muscle fascicles were, however, shorter during force
production in running than walking and developed force before heel contact. In
all cases, force development was associated with little change in length of
the muscle fascicles and is hence isometric during this period. Shortening of
the fascicles occurred during force decline in all conditions.
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In the present study we demonstrate that when the MTU trajectory changes
with change in grade and gait (speed), the muscle fascicle length trajectory
also changes. In particular, the length of the muscle fascicles during force
development varies as a function of grade and gait. As has previously been
demonstrated, the muscle fascicles act relatively isometrically during the
stance phase of walking (Fukunaga et al.,
2001), and shorten during the stance phase of running
(Lichtwark and Wilson, 2005d).
Here we have found, however, that there is an increase in muscle fascicle
length associated with the increase in grade. This is likely to be due to the
increase in whole MTU length occurring as a result of the increased
dorsi-flexion throughout stance. The force-length properties of the muscle
fascicle, including the contribution of parallel elastic elements, may
therefore be important in determining the muscle power output.
In all conditions the AT strain and hence force was developed with very
little change in muscle fascicle length; the contractile element acted almost
isometrically during this period (Fig.
6). The results demonstrate that the muscle fascicles shortened at
speeds below 1/3 of the estimated maximum muscle shortening velocity [assuming
a maximum shortening velocity of between 8 and 14 Lo
s-1 (Epstein and Herzog,
1998)]. This is both energetically efficient and is also
advantageous in being able to produce high forces
(Roberts, 2002;
Woledge et al., 1985). A
similar result has previously been predicted using indirect methods
(Hof et al., 2002); however,
that study estimated the entire contractile component length change (which is
largely influenced by muscle shape changes) rather than length measurements of
individual fascicles.
Most of the work done by the muscle fascicles was done during deactivation,
when the elastic tissues were also recoiling and doing the majority of the
work of the MTU. The rate of muscle fascicle shortening increased with an
increase in speed; however, the rate of shortening was typically around 25-30%
of the total MTU shortening speed. Therefore the elastic recoil of the tendon
and aponeurosis contributed most of the MTU shortening. A similar finding has
been demonstrated during walking (Fukunaga
et al., 2001; Ishikawa et al.,
2005). This raises the question as to why the muscles do not
deactivate at a faster rate, remain isometric, and allow the tendon to do all
of the work whilst recoiling. Perhaps if the muscle were to relax too fast
then the high forces would stretch the muscle and absorb some of the work of
the whole MTU, which is an inefficient method of performing whole muscle work.
Also, perhaps the muscle must maintain a short length during the swing phase
so as to ensure foot clearance, and therefore the muscle fascicles must be at
a shorter length. Alternatively, this may be an efficient way to perform
muscular work (Woledge et al.,
1985) or perhaps the neuromuscular system is unable to control
such a precise method of deactivation.
During walking there was an increase in the muscle excitation (based on
EMG) with an increase in incline. However, there was not an increase in muscle
fascicle force or a significant change in the area under the GM fascicle
length-AT length curve. Throughout the stance phase, however, the muscle
fascicles act at a longer length during force development as incline
increases. Therefore, perhaps the muscle moves along the descending limb of
the force-length curve here and requires more activation to produce the
required force and stretch the AT. This is probably unlikely, however, due to
the effect of parallel elasticity. Alternatively, the muscle fascicles also
contract at a higher velocity in the uphill conditions, which would require a
higher activation to achieve the same force according to the force-velocity
relationship of muscle. In contrast to walking, the running conditions showed
a higher excitation but this level was very similar between grade conditions.
Again, the muscle fascicle lengths were much shorter and the contraction
velocities were greater uphill running condition. The differences in
excitation level (EMG) may also be due to variations in the force sharing
between the other muscles of the triceps surae
(Arndt et al., 1998).
During both walking and running the AT length was greater than its slack length at heel strike (Fig. 5). This suggests that some force was developed in the AT during the swing phase. During walking this occurred during periods of inactivity in the GM muscle and is likely to be due to parallel elastic structures, other muscles or measurement errors in this portion of the stride (probe rotations etc.). However in the running condition, where greater strain was developed and maintained throughout the heel contact period, the GM was co-activated with an antagonist, the tibialis anterior. This suggests that there is indeed some requirement for tension to be developed in the AT during foot contact. This may act to stabilise the ankle joint for impact with the ground. Activating the GM muscle before foot strike also alters the length of the muscle fascicle in preparation for force development during stance, and may optimise the length of the muscle for force production during stance.
During steady state locomotion on the level, the requirement for whole body
work is zero across the period of a stride; however, here we have demonstrated
that the GM muscle does positive work even when travelling downhill. This is
in contrast to the findings of Gabaldon and colleagues
(Gabaldon et al., 2004), who
found that the work output of the lateral gastrocnemius and peroneous longus
muscles of the turkey more closely resemble that of the whole body work
output. Perhaps the role of the human GM is different to that of the muscles
examined in the turkey. It is not possible to present accurate and validated
calculations that compare the external work and power output of the body to
that of the muscle fascicles from this data set (due to estimations of
individual muscle forces and errors likely associated with the ultrasound
technique). Perhaps future studies will explore these relationships.
In our estimates of muscle fascicle force, we assumed that the three
muscles of the triceps surae contribute equally to the whole tendon force
based on PCSA. This may not be the case, however, and the contribution to
whole tendon force may vary with different conditions (as mentioned above).
Direct measures of AT strain suggest that the strain distribution of the
muscles attaching to the tendon may not be equal and can cause differential
strain patterns in the tendon and aponeurosis
(Finni et al., 2003;
Bojsen-Moller et al., 2004;
Arndt et al., 1998). The large
variation in Achilles tendon stiffness between individuals is also likely to
have an effect on individual estimates of muscle fascicle force
(Lichtwark and Wilson, 2005c;
Hof, 1998;
Maganaris and Paul, 2002).
Previously it has been suggested that the primary function of biarticular
muscles with opposite actions at each joint, such as the GM, is to transfer
energy from the more powerful and proximal muscles of the knee and hip and
hence may not be required to produce large amounts of work
(Bobbert and Ingen Schenau,
1988; Neptune et al.,
2004). However the action at both joints must be considered in
examining the amount of energy that can be transferred. It has recently been
demonstrated in human running, that although the maximum plantar flexion ankle
joint moment does not vary between level and uphill running, the knee extensor
moment actually decreases when running uphill
(Roberts and Belliveau, 2005).
Therefore the GM, which acts as a knee flexor, may produce less force in
counteracting the knee extensors during uphill running. The results from this
study are therefore consistent of those of Roberts and Belliveau, who
concluded that the extra power for uphill running is generated mostly at the
hips; not the knee and ankle (Roberts and
Belliveau, 2005).
This study has also demonstrated the importance of strain of other elastic
tissues (e.g. aponeurosis) in producing muscular force. The large difference
between the strain of the AT and the calculated SEE length
(Fig. 5) demonstrates that
other tissues must be stretching. This was shown experimentally by Magnusson
and colleagues (Magnusson et al.,
2003), who demonstrated that the aponeurosis strain is
significant, although it appears to be stiffer than the AT. Hof and coworkers
(Hof, 1998) have also argued
that series elastic tissue such as the aponeurosis may be selectively
recruited based on muscle activation levels and that this may alter the
stiffness of the entire elastic component. This again would influence our
estimations of fascicle force, work and power output.
In conclusion, the interaction of the GM muscle with the AT and other elastic tissues varies with both gait and grade of incline. Force is typically developed isometrically and work is done by the fascicles during force decline. The fascicle length at which force is developed, however, does vary with incline. This is likely due to the change in force requirements and the change in whole MTU length trajectory resulting from kinematic changes. To achieve this pattern of muscle contraction, the AT and other elastic elements are strained substantially, which allows the muscle fascicles to act at velocities that maximise power output of the muscle. Our results also indicate that the GM produces positive work during all incline conditions.
|
Acknowledgments |
|---|
|
Footnotes |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alexander, R. M. (1988). Elastic Mechanisms in Animal Movement. Cambridge: Cambridge University Press.
Arndt, A. N., Komi, P. V., Bruggemann, G. P. and Lukkariniemi, J. (1998). Individual muscle contributions to the in vivo achilles tendon force. Clin. Biomech. Bristol Avon 13,532 -541.
Bobbert, M. F. and Ingen Schenau, G. J. (1988). Coordination in vertical jumping. J. Biomech. 21,249 -262.[CrossRef][Medline]
Bojsen-Moller, J., Hansen, P., Aagaard, P., Svantesson, U.,
Kjaer, M. and Magnusson, S. P. (2004). Differential
displacement of the human soleus and medial gastrocnemius aponeuroses during
isometric plantar flexor contractions in vivo. J. Appl.
Physiol. 97,1908
-1914.
Epstein, M. and Herzog, W. (1998). Theoretical Models of Skeletal Muscle. Chichester: John Wiley & Sons.
Ettema, G. J. (2001). Muscle efficiency: the controversial role of elasticity and mechanical energy conversion in stretch-shortening cycles. Eur. J. Appl. Physiol. 85,457 -465.[CrossRef][Medline]
Finni, T., Hodgson, J. A., Lai, A. M., Edgerton, V. R. and
Sinha, S. (2003). Nonuniform strain of human soleus
aponeurosis-tendon complex during submaximal voluntary contractions in vivo.
J. Appl. Physiol. 95,829
-837.
Fukunaga, T., Roy, R. R., Shellock, F. G., Hodgson, J. A., Day, M. K., Lee, P. L., Kwong-Fu, H. and Edgerton, V. R. (1992). Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. J. Orthop. Res. 10,928 -934.[Medline]
Fukunaga, T., Kubo, K., Kawakami, Y. and Kanehisa, H. (2000). Effect of elastic tendon properties on the performance of stretch-shortening cycles. In Skeletal Muscle Mechanics: From Mechanisms to Function (ed. W. Herzog), pp.289 -303. Chichester: John Wiley & Sons.
Fukunaga, T., Kubo, K., Kawakami, Y., Fukashiro, S., Kanehisa, H. and Maganaris, C. N. (2001). In vivo behaviour of human muscle tendon during walking. Proc. R. Soc. Lond. B Biol. Sci. 268,229 -233.[Medline]
Gabaldon, A. M., Nelson, F. E. and Roberts, T. J.
(2004). Mechanical function of two ankle extensors in wild
turkeys: shifts from energy production to energy absorption during incline
versus decline running. J. Exp. Biol.
207,2277
-2288.
Grieve, D. W., Pheasant, S. and Cavanagh, P. R. (1978). Preduction of gastrocnemius length from knee and ankle joint posture. In Proceedings of the Sixth International Congress of Biomechanics. Vol. VI-A (ed. E. Asmussen and K. Jorgensen), pp, 405-412. Baltimore: University Park Press.
Griffiths, R. I. (1991). Shortening of muscle
fibres during stretch of the active cat medial gastrocnemius muscle: the role
of tendon compliance. J. Physiol.
436,219
-236.
Hof, A. L. (1998). In vivo measurement of the series elasticity release curve of human triceps surae muscle. J. Biomech. 31,793 -800.[CrossRef][Medline]
Hof, A. L., van Zandwijk, J. P. and Bobbert, M. F. (2002). Mechanics of human triceps surae muscle in walking, running and jumping. Acta Physiol. Scand. 174, 17-30.[CrossRef][Medline]
Ishikawa, M., Komi, P. V., Grey, M. J., Lepola, V. and
Bruggemann, G. P. (2005). Muscle-tendon interaction and
elastic energy usage in human walking. J. Appl.
Physiol. 99,603
-608.
Ker, R. F., Bennett, M. B., Bibby, S. R., Kester, R. C. and Alexander, R. M. (1987). The spring in the arch of the human foot. Nature 325,147 -149.[CrossRef][Medline]
Komi, P. V. (1990). Relevance of in vivo force measurements to human biomechanics. J. Biomech. 23, Suppl. 1, 23-34.[Medline]
Kurokawa, S., Fukunaga, T., Nagano, A. and Fukashiro, S.
(2003). Interaction between fascicles and tendinous structures
during counter movement jumping investigated in vivo. J. Appl.
Physiol. 95,2306
-2314.
Lichtwark, G. A. and Wilson, A. M. (2005a). A
modified Hill muscle model that predicts muscle power output and efficiency
during sinusoidal length changes. J. Exp. Biol.
208,2831
-2843.
Lichtwark, G. A. and Wilson, A. M. (2005b).
Effects of series elasticity and activation conditions on muscle power output
and efficiency. J. Exp. Biol.
208,2845
-2853.
Lichtwark, G. A. and Wilson, A. M. (2005c).
In vivo mechanical properties of the Achilles tendon during
one-legged hopping. J. Exp. Biol.
208,4715
-4725.
Lichtwark, G. A. and Wilson, A. M. (2005d). Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J. Biomech. doi: 10.1016/j.jbiomech.2005.10.035.
Maganaris, C. N. and Paul, J. P. (2002). Tensile properties of the in vivo human gastrocnemius tendon. J. Biomech. 35,1639 -1646.[CrossRef][Medline]
Magnusson, S. P., Hansen, P., Aagaard, P., Brond, J., Dyhre-Poulsen, P., Bojsen-Moller, J. and Kjaer, M. (2003). Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. Acta Physiol. Scand. 177,185 -195.[CrossRef][Medline]
Narici, M. V., Binzoni, T., Hiltbrand, E., Fasch, J., Terrier, F. and Cerretelli, P. (1996). In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J. Physiol. 496,287 -297.[Medline]
Neptune, R. R., Zajac, F. E. and Kautz, S. A. (2004). Muscle force redistributes segmental power for body progression during walking. Gait Posture 19,194 -205.[CrossRef][Medline]
Roberts, T. J. (2002). The integrated function of muscles and tendons during locomotion. Comp. Biochem. Physiol. 133A,1087 -1099.[CrossRef]
Roberts, T. J. and Belliveau, R. A. (2005).
Sources of mechanical power for uphill running in humans. J. Exp.
Biol. 208,1963
-1970.
Roberts, T. J. and Scales, J. A. (2004).
Adjusting muscle function to demand: joint work during acceleration in wild
turkeys. J. Exp. Biol.
207,4165
-4174.
Woledge, R. C., Curtin, N. A. and Homsher, E. (1985). Energetic Aspects of Muscle Contraction. Monogr. Physiol. Soc. Vol. 41. London: Academic Press.
This article has been cited by other articles:
|
|
 |
|
  M. Spanjaard, N. D. Reeves, J. H. van Dieen, V. Baltzopoulos, and C. N. Maganaris Lower-limb biomechanics during stair descent: influence of step-height and body mass J. Exp. Biol., May 1, 2008; 211(9): 1368 - 1375. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. S. Sawicki and D. P. Ferris Mechanics and energetics of level walking with powered ankle exoskeletons J. Exp. Biol., May 1, 2008; 211(9): 1402 - 1413. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Hoffren, M. Ishikawa, and P. V. Komi Age-related neuromuscular function during drop jumps J Appl Physiol, October 1, 2007; 103(4): 1276 - 1283. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. N. Dean, E. Azizi, and A. P. Summers Uniform strain in broad muscles: active and passive effects of the twisted tendon of the spotted ratfish Hydrolagus colliei J. Exp. Biol., October 1, 2007; 210(19): 3395 - 3406. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. A. Biewener and M. A. Daley Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control J. Exp. Biol., September 1, 2007; 210(17): 2949 - 2960. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. J. Roberts, B. K. Higginson, F. E. Nelson, and A. M. Gabaldon Muscle strain is modulated more with running slope than speed in wild turkey knee and hip extensors J. Exp. Biol., July 15, 2007; 210(14): 2510 - 2517. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Spanjaard, N. D. Reeves, J. H. van Dieen, V. Baltzopoulos, and C. N. Maganaris Gastrocnemius muscle fascicle behavior during stair negotiation in humans J Appl Physiol, April 1, 2007; 102(4): 1618 - 1623. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
