Force enhancement following stretching of skeletal muscle : a new mechanism
Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada T2N 1N4
* e-mail: walter{at}kin.ucalgary.ca
Accepted 6 February 2002
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Summary |
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Key words: skeletal muscle, force enhancement, sarcomere length, passive elastic element, mechanism of contraction
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Introduction |
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Despite the general acceptance of force enhancement following stretch,
there has been little systematic study as to the mechanism underlying this
phenomenon. Force enhancement has typically been observed on the descending
limb of the forcelength relationship (Edman et al.,
1978,
1982
;
Morgan et al., 2000
).
Furthermore, the descending limb has been associated with sarcomere length
instabilities (Hill, 1953
;
Zahalak, 1997
). Therefore, it
was convenient to relate history-dependent force properties of muscle, such as
`creep' (Gordon et al., 1966
),
force depression following muscle shortening, and force enhancement following
muscle stretch, to the development of sarcomere length non-uniformities
(Edman and Tsuchiya, 1996
;
Morgan, 1990
,
1994
;
Morgan et al., 2000
).
Associating history-dependent force properties of muscle with structural
non-uniformities at the sarcomere level has the advantage that it leaves
contraction at the molecular level history-independent, as it has been since
the initial mathematical formulation of the cross-bridge theory
(Huxley, 1957
;
Huxley and Simmons, 1971
).
History independence in this context means that the steady-state results of
the mathematical solutions of the cross-bridge theory are independent of the
preceding contractile conditions.
The sarcomere length non-uniformity theory gives the following testable hypotheses: (1) there should be no force enhancement on the ascending limb of the forcelength relationship; and (2) the steady-state force following muscle stretching on the descending limb of the forcelength relationship cannot be greater than the isometric reference force at the initial muscle length (the length at which the muscle stretch was started; Fig. 1).
|
The first purpose of this study was to test these two hypotheses.
Furthermore, Noble (1992) and
Edman and Tsuchiya (1996
)
suggested that the strain of passive elastic components may play an essential
part in the development of the steady-state force enhancement following muscle
stretching. This idea was also proposed for human muscle
(DeRuiter et al., 2000
), and
was used in a theoretical model of muscle force enhancement following stretch
(Forcinito et al., 1998
).
However, there has been no direct evidence of such a passive, elastic
contribution to force enhancement. Therefore, the second purpose of this study
was to determine if there was passive force enhancement following muscle
stretching on the descending limb of the forcelength relationship.
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Materials and methods |
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A second cut was made on the posterior, lateral thigh and the tibial nerve was exposed and implemented with a bipolar cuff-type electrode for soleus stimulation. The cat was secured in a prone position in a hammock and the pelvis, thigh and shank of the experimental hindlimb were fixed with bilateral bone pins to a stereotaxic frame. The bone piece at the distal end of the soleus tendon was attached with sutures to a muscle puller (MTS, Eden Prairie, MN, USA; natural frequency >10kHz). The soleus forces (100 N=10 V) and excursions (50 mm=10 V) were measured continuously by the muscle puller and sampled at a frequency of 200 Hz.
Nerve stimulation was performed using a voltage that exceeded the -
motoneuron threshold by a factor of three (3T) to ensure full soleus
stimulation (Herzog and Leonard,
1997
). Stimulation pulses were of 0.1 ms duration and monopolar.
Stimulation frequency was 30 Hz or 5 Hz, and the duration of stimulation
varied as a function of the test protocol. The stimulation frequency of 30 Hz
was chosen because it gave fused tetanic contractions of the cat soleus in all
cases without causing appreciable fatigue. The 5 Hz frequency was chosen to
allow direct comparison of the results from unfused tetani with those
published by Morgan et al.
(2000
). Muscle temperature was
monitored continuously and kept at 35±1°C using a regular drip of
warm saline (0.9%) and an adjustable infrared heat lamp.
Experimental protocol
Three series of tests were performed with each of the eight muscles. In the
first series, the forcelength relationship of the soleus was determined
for stimulation frequencies of 5 Hz and 30 Hz. Forcelength
relationships were obtained by finding first the length of active
insufficiency (zero force) and then increasing length in increments of 2 mm
until the (active) descending limb was identified. The length at which the
largest active force (total forcepassive force) for the 30 Hz
stimulations was measured was called 0 mm. Lengths beyond 0 mm were defined as
the descending limb (Morgan et al.,
2000), as active force decreased with increasing muscle length,
and were designated by positive length changes (i.e. a length of +4 mm refers
to a muscle length 4 mm greater than optimal length, 0 mm). Similarly, lengths
below 0 mm were defined as the ascending limb, as active force increased with
increasing muscle length. All contractions were maintained for 3 s. A 1 min
rest was given between contractions. Note that the 0 mm length defined in this
way was always part of the ascending limb of the 5 Hz forcelength
relationship.
In the second series of tests, force enhancement following stretching was assessed on the ascending limb of the forcelength relationship. In order to quantify force enhancement, four contractions were performed: (i) an isometric reference contraction for 8 s at a muscle length of -2 mm; (ii) a 1 s isometric contraction at a muscle length of -10 mm followed by stretching from -10 mm to -2 mm at 4 mm s-1, followed by a 5 s isometric contraction at -2 mm (Fig. 2); (iii) an isometric contraction for 8 s at a muscle length of -10 mm; and (iv) a repeat of (i). If the repeat isometric reference contractions did not produce the same force (±0.1 N), trials were not used for analysis. This series of four contractions was performed with a stimulation frequency of 5 Hz and 30 Hz.
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In the third series of tests, force enhancement was determined on the
descending limb of the forcelength relationship. The amount of
stretching (3, 6 and 9 mm; i.e. approximately 3-9 % of total muscle length and
approximately 7-21 % of optimal fibre length) and the speed of stretching (3,
9 and 27 mm s-1, i.e. approximately 7, 21 and 63 % of optimal fibre
length s-1) were systematically varied
(Fig. 3). The magnitude of
stretching was varied as there is a controversy whether or not increasing
stretch magnitude influences force enhancement in cat soleus
(Morgan et al., 2000). Stretch
speeds were changed as it appears that fibre preparations do not show a speed
dependence of force enhancement (Edman et
al., 1978
; Sugi and Tsuchiya,
1988
), whereas muscle preparations do
(Abbott and Aubert, 1952
). In
order to obtain a single data point of force enhancement, six tests were
performed: (i) isometric reference contraction at the initial length; (ii)
isometric reference contraction at the final length; (iii) stretching from the
initial to the final length with the muscle fully activated; (iv) stretching
from the initial to the final length with the muscle not activated (passive
tests); (v) and (vi) repeat isometric reference contractions at the initial
and final lengths, respectively. If the repeat isometric reference
contractions did not produce the same force (±0.1 N), trails were not
used for analysis. All tests were performed at a stimulation frequency of 30
Hz. All tests at the 9 mm s-1 speed were then repeated using a
stimulation frequency of 5 Hz.
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Determination of force enhancement following stretching
Following all stretching of muscles, activation was maintained for an
additional 5s. A 4s period was typically sufficient for force transients to
disappear. Therefore, steady-state force enhancement was determined 4.5s after
the end of stretching (Figs 2
and 3, first arrowhead).
Similarly, following deactivation of the muscle, isometric measurements of the
passive forces were continued for at least 5s. Deactivation force transients
disappeared within 2s. Therefore, passive force enhancement measurements were
made 3s following deactivation when the force curves had reached a
steady-state (Figs 2 and
3, second arrowhead).
Statistics
Because of the sample size (N=8), all statistical analyses were
performed using a non-parametric, sign-rank test based on the
2-distribution. The null hypotheses were those presented in
the introduction, and all testing was done with a single alternative
hypothesis. The level of significance was chosen as P=0.05 in all
cases. Therefore, by definition, any observation that is statistically
significant must be made in at least seven out of the eight independent
observations (muscles).
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Results |
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The second hypothesis tested here was that the steady-state active force
following stretch cannot exceed the isometric force at the muscle length from
which the stretch was started (Morgan et
al., 2000). This hypothesis was rejected. All stretches of 9 mm
and at a speed of 3 mm s-1 showed greater steady-state active
forces following the stretch (P<0.05) than the corresponding
active isometric forces at the initial muscle length
(Fig. 5). The average
enhancement of force above the initial isometric force was 1.7±1.2 N
(mean ± S.D., N=8) (or 8.5 % greater than the average
isometric force at the initial length for stretches of 9 mm and performed at 3
mm s-1). This force enhancement above the initial isometric force
was not as pronounced for the faster speeds of stretch (i.e. 9 mm
s-1 and 27 mm s-1); however, all tests but one, at any
speed, showed enhancement of force above the initial isometric force
(1.3±1.1 N, or 6.5 % greater than the average isometric force at the
initial length; P<0.05); the one exception had the same force as
the initial isometric force.
|
There has been controversy as to whether or not the amount of force
enhancement is dependent on the magnitude of stretching
(Morgan et al., 2000). For cat
soleus, total force enhancement increased (P<0.05) with increasing
magnitudes of stretch on the descending limb of the forcelength
relationship (Fig. 6). This
result was observed for all eight muscles consistently, at all tested speeds
(3, 9 and 27 mm s-1) and for both frequencies of stimulation (5 Hz
and 30 Hz) (Table 2).
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When stretching cat soleus on the descending limb of the forcelength relationship, we observed a consistent passive force enhancement. This passive force enhancement was seen as an increase in force after the muscle had been deactivated in the active stretching trials compared to the isometric or the passive stretching trials (passive forces following isometric contractions and passive stretching trials were similar, Fig. 7A-C). This passive force enhancement reached a steady state and persisted until the muscle was shortened. Passive force enhancement was not observed on the ascending limb of the forcelength relationship.
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Discussion |
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Rejection of these two hypotheses does not imply that sarcomere length non-uniformity is not a factor in force enhancement following stretching. However, it implies that sarcomere length non-uniformity alone cannot explain all of the force enhancement following muscle stretch.
Active isometric force decreases with increasing length on the descending
limb of the forcelength relationship. Because of this isometric
behavior, muscles on the descending limb of the forcelength
relationship have been said to have `softening' properties
(Zahalak, 1997), and as a
consequence, force production was said to be unstable. However, an apparent
`softening' property obtained during static testing, e.g. when determining the
isometric forcelength relationship of a muscle or fibre
(Gordon et al., 1966
) does not
imply that a material is indeed softening. The result that the active force
enhancement following stretch typically exceeded the active isometric force at
the initial muscle length supports the idea that the active force-producing
mechanism provides stability on the descending limb of the forcelength
relationship. This stability is further enhanced in some muscles, including
the cat soleus tested here, by passive forces that come into play at lengths
corresponding to the optimal length of the muscle and on the descending limb
of the forcelength relationship.
A novel mechanism for force enhancement
The steady-state passive force following deactivation of an actively
stretched muscle was always greater than the steady-state passive force at the
same muscle length following an isometric contraction or a passive stretching
of the muscle (Fig. 7,
Table 3). If we assume that
this passive force enhancement is caused by the active stretch, as suggested
by DeRuiter et al. (2000), it
would account for more than 50 % of the total force enhancement for all
stretches of 6mm and beyond. For a 9 mm stretch at 3 mm s-1,
passive force enhancement was, on average, 4.1 N and accounted for 83.7 % of
the total force enhancement. It should be noted here that the passive force
enhancement always persisted for the 5-10 s period for which the muscle was
held at the final length following active stretching. Once the muscle was
shortened to its recovery length (-10 mm) and reactivated for the next test,
all passive force enhancement had been abolished in all tests and for each
muscle. This result indicates that the passive force enhancement was not
caused by structural damage to the muscle associated with stretching. The idea
that damage did not contribute to the passive force enhancement is further
supported by the fact that only trials in which the isometric reference
contractions before and after the stretching were the same (±0.1 N)
were used for analysis.
Based on the passive force enhancement results, we conclude that total residual force enhancement of cat soleus on the descending limb has two components: an active and a passive force enhancement component. The absolute and the percentage force contribution of the active component of force enhancement decreases while the corresponding passive component of force enhancement increases with increasing magnitude of stretching. No passive force enhancement was observed in any of the stretches performed on the ascending limb of the forcelength relationship.
During normal locomotion (walking, trotting), the cat soleus muscle
operates on the ascending limb and the plateau of the forcelength
relationship. Soleus length changes for walking, trotting, and galloping are
approximately 10 mm, 13 mm and 15 mm, respectively, during the stance phase,
and the corresponding rates of muscle length changes are approximately 25 mm
s-1, 130 mm s-1 and 300 mm s-1, respectively
(Goslow et al., 1973).
Therefore, the magnitudes and speeds of stretch are well within
physiologically relevant values. Although corresponding data are not available
for tree climbing and full-speed galloping, there is no evidence that cat
soleus ever operates on the descending limb of the forcelength
relationship during normal movements. Therefore, the passive force
enhancements observed on the descending limb of the forcelength
relationship might not have immediate relevance to normal cat movement. We
interpret the present results as follows: imagine that a muscle is actively
stretched to a length exceeding its normal operating length. Such active
stretching is associated with a distinct possibility of muscle injury and
severe tearing of soft tissue structures. In this situation, a passive force
beyond that observed during passive stretching develops and prevents, to a
certain extent, the overstretching of the active muscle. Therefore, the
additional passive force enhancement observed here may not represent a normal
physiological response of muscle. Rather, it may represent a safety mechanism
intended to prevent tearing and injury of an actively stretched muscle.
The idea that force enhancement has the properties of a passive elastic
element has been proposed, but not demonstrated, before. Noble
(1992) and Edman and Tsuchiya
(1996
) suggested that force
enhancement behaves like an elastic structure that engages at the length of
initial muscle activation. Forcinito et al.
(1998
) used this idea in a
rheological muscle model to account for force depression and force enhancement
following shortening and stretching, respectively. However, this is the first
report to demonstrate experimentally and evaluate systematically the
contribution of passive force enhancement to the total force enhancement. We
observed a similar passive force enhancement to that shown in
Fig. 7 in pilot studies using
single fibres of frog Rana pipiens tibialis anterior
(Wakeling et al., 2000
), and
in cat semitendinosus and human adductor pollicis
(Lee et al., 2001
;
Schachar et al., 2000
).
The results of the present study do not allow us to determine the origin of
the passive force enhancement. However, the molecular spring titin could
produce the observed results. Titin is a spring whose characteristic length
and stiffness changes with the unfolding of molecular bonds in the so called
immunoglobulin domain (Kellermayer et al.,
1997; Marszalek et al.,
1999
; Rief et al.,
1997
). If we assume, for example, that these molecular bonds
increase in strength when the biochemical environment is that of an active
muscle (increase in free Ca2+ levels) compared to that of a passive
muscle, fewer molecular bonds in titin might be broken when the muscle is
pulled to a given length under active compared to passive conditions. Evidence
in support of this theory has been reported by Tatsumi et al.
(2001
) and Yamasaki et al.
(2001
). Therefore, the
stiffness of titin might increase (because the characteristic molecular length
is decreased) in active compared to passive muscle stretching. Thus, the
passive force in titin would be greater following active compared to passive
stretching. The same result could be obtained if under active conditions,
molecular unfolding was not as complete as under passive conditions, or if the
characteristic length of titin depends on the sarcomere length at which
activation occurs.
The idea of titin behaving like an `activatable' spring has been tested
before and was rejected. Horowits et al.
(1989) stated that the elastic
properties of titin are unaltered by activity, Ca2+ and
cross-bridge activity, although the elastic properties were not directly
determined. However, Tatsumi et al.
(2001
) showed that the
secondary structure of the elastic part of titin was changed by the binding of
Ca2+. They concluded from this result that the stiffness of titin
might change during the contractionrelaxation cycle of skeletal muscle.
Similarly, Yamasaki et al.
(2001
) found that cardiac
titin interacted with actin in a dose-dependent manner, based on the
contraction of the soluble calcium-binding protein S100A1. These interactions
were shown to modulate the passive stiffness, and were hypothesized to provide
a mechanism for changing titin-based force prior to active contraction.
The idea that force enhancement might occur by the formation of a parallel
elastic element at the sarcomere length at which the muscle is activated
(Tsuchiya and Edman, 1990)
requires that shortening prior to stretching reduces the force enhancement
following stretching in a dose-dependent manner. When preceding stretches in
single frog tibialis anterior fibres by shortening, Edman et al.
(1982
) found that the residual
force enhancement following the stretches was unaffected by the shortening,
therefore apparently disproving this idea for force enhancement. However, the
shortening-stretch cycles in the experiments by Edman et al.
(1982
) were separated by an
interval of approximately 1 s. When performing shortening-stretch experiments
that follow each other directly (i.e. without a time delay), we found that the
distance of shortening preceding a stretch decreased the amount of force
enhancement in a dose-dependent manner
(Herzog and Leonard,
2000
).
Edman and Tsuchiya (1996)
found residual force enhancement after stretch of frog tibialis anterior
muscle fibres. This force enhancement was linearly related to the slow
component of tension rise during stretch. Furthermore, when released against a
small load, the force transients of the previously stretched fibres exhibited
a greater and steeper decrease than those obtained from isometric contractions
without previous stretching. These results were interpreted by Edman and
Tsuchiya (1996
) as originating
from the elongation of a passive, elastic, cytoskeletal protein. They
speculated that titin or nebulin could fulfil this role.
There is no obvious explanation for the remnant active force enhancement
observed in our study. The sarcomere-length non-uniformity theory does not
provide an easy explanation for this phenomenon, because active force
enhancement (the absolute and percentage values) decreased with increasing
stretching distance, whereas one would expect that sarcomere length should
become more non-uniform with increasing stretching distance and, therefore,
active force enhancement should increase as well, which it does not. A
potentially interesting and novel explanation for the active component of
force enhancement was suggested by Linari et al.
(2000). They studied force
enhancement following stretching in single frog fibres using a mechanical and
an X-ray diffraction approach. Combining results from stiffness and force
measurements with the intensity of the third-order myosin meridional X-ray
reflection, they concluded that active force enhancement was caused by a
residual increase in the number of attached cross-bridges. This result agrees
with our own investigations on cat soleus, where stiffness was increased in
the force-enhanced state following muscle stretching, compared to the
corresponding reference contraction, suggesting that the force enhancement is
caused by an increased number of attached cross-bridges
(Herzog and Leonard, 2000
).
Although this is an exciting result and definitely warrants further
investigation, it would be hard to reconcile long-lasting force enhancement
with a mechanism involving cross-bridge cycling.
Conclusions
Based on the results of this study, we conclude that the sarcomere-length
non-uniformity theory does not explain all of the force enhancement following
stretching of cat soleus on the descending limb of the forcelength
relationship. We further propose that for many contractile conditions,
specifically the stretching tests of 9 mm magnitude, the active force
properties of cat soleus are stable on the descending limb of the
forcelength relationship. Finally, we suggest that part of the force
enhancement of muscles following stretch is caused by an `activatable' passive
element that changes its stiffness, and therefore force output, at a given
length, during active stretching compared to passive stretching.
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Acknowledgments |
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