Characterization of the passive component of force enhancement following active stretching of skeletal muscle
University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada
* Author for correspondence (e-mail: walter{at}kin.ucalgary.ca)
Accepted 17 May 2003
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Summary |
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Key words: passive force, skeletal muscle, stretching, titin, cross-bridge theory, sarcomere length, stability, molecular spring, calcium
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Introduction |
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Edman et al. (1978,
1982
) were the first to propose
that the "residual force enhancement after stretch was compatible
with recruitment of a passive elastic element in parallel with the contractile
system". This notion was further supported by indirect evidence in
single fiber and whole muscle preparations
(Edman and Tsuchiya, 1996
;
DeRuiter et al., 2000
;
Lee and Herzog, 2002
), and was
used in theoretical considerations (Noble,
1992
; Herzog,
1998
; Herzog and Leonard,
2002
) and mathematical modeling of the force enhancement effect
(Forcinito et al., 1998
).
Recently, we reported direct evidence for passive force enhancement in the cat
soleus, in single fibres of frog, and in voluntary contractions of human
adductor pollicis (Herzog and Leonard,
2002
; Rassier et al.,
2003
,
in press
;
Lee and Herzog, 2002
). The
purpose of the present study was to characterize the mechanical properties of
this newly detected passive component that contributes to the steady-state
force enhancement following active muscle stretch, and to determine, or
eliminate, possible candidate structures that may cause this passive force
enhancement.
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Materials and methods |
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Preparation
The procedures for animal preparation, force and length measurements have
been described before (Herzog and Leonard,
1997). Here, only the salient features are repeated. Cats were
anaesthetized using a nitrous oxide, halothane (5%), oxygen mixture, and were
then intubated and maintained at 0.8-1.0% halothane throughout the remainder
of the experiment. Cats were regularly checked for ear, pupil and paw pressure
reflexes, and halothane was adjusted accordingly. The soleus, soleus tendon
and calcaneus were exposed using a single cut on the posterior, lateral shank.
The soleus tendon was isolated from the rest of the Achilles tendon and was
cut from the calcaneus with a remnant piece of bone. The muscles surrounding
the soleus (plantaris and both heads of the gastrocnemius) were bluntly
dissected away from the soleus, and the corresponding tendons were cut leaving
the soleus isolated from any other muscle. 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
(Herzog and Leonard, 1997
).
The nerve was left fully intact to ensure a consistent, long-term preparation.
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 >10 kHz). When attaching the bone piece, about half of the soleus
tendon is wrapped around the attachment clamp on the muscle puller, thus
providing excellent fixation of the distal end of the soleus. The free tendon
was usually about 10 mm long following fixation and provided little compliance
to the preparation because of the great stiffness of the soleus tendon that
makes it virtually rigid within the range of muscle forces
(Baratta and Solomonow, 1990
).
The soleus forces and excursions were measured continuously by the muscle
puller and were sampled at a frequency of 200 Hz, except for tests in which
stiffness was assessed (2000 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 monopolar and of 0.1 ms duration. Stimulation
frequency was 30 Hz, which produces fused tetanic contractions of the cat
soleus, and the duration of stimulation varied as a function of the specific
test. The exposed soleus was covered with saline-soaked gauze, and was heated
with an infrared lamp to keep the muscle temperature between 30-35°C.
Experimental protocol
At the beginning of each experimental protocol, the isometric force-length
relationship of the cat soleus was determined. Peak tetanic forces (30 Hz)
were determined from a length near active insufficiency (zero force) until a
muscle length that was 12 mm longer than the length at which active force
(total force - passive force) was maximal. Length steps were 3 mm, and
typically 12-15 length steps were required to cover the target range. The
muscle length at the right end of the isometric force plateau
(Gordon et al., 1966) was
designated 0 mm. Increases in muscle length are defined as positive; i.e. +9
mm refers to a muscle length that is 9 mm longer than the 0 reference length.
Note that the 0 mmreference length is typically associated with an active
isometric force that is equal or just a little bit smaller (<5%) than the
maximal, active isometric force.
Following the determination of the force-length relationship, seven tests
were performed. Test 1 was aimed at determining the long-term
stress-relaxation rate of the passive component of force enhancement and
comparing it to the stress-relaxation rate of the passive component following
purely isometric contractions. Passive force enhancement (the force
enhancement measured after deactivation of the muscle) was produced by
stretching the active muscle from 0 mm to +9 mm (i.e. approx. 9% of the total
muscle length or approx. 21% of the optimal fiber length;
Herzog and Leonard, 2002) at a
speed of 3 mm s-1 (i.e. about 7% of optimal fiber length
s-1), deactivating the muscle 5 s after the end of stretch, and
then measuring the passive force decay for a period of >25 s
(Fig. 1). Note that 5 s after
deactivation of the muscle, all deactivation force transients have subsided
(Huxley, 1957
;
Huxley and Simmons, 1971
). The
loss of force of the passive elements at this point in time reflects the
viscoelastic properties of the tissues involved in passive force
production.
|
Test 2 was aimed at determining the stiffness of the passive component of force enhancement and comparing it to the corresponding stiffness of the passive force following a purely isometric contraction or a passive stretch. Passive force enhancement was obtained by stretching the muscle as described in test 1, and stiffness of the passive components was assessed by a quick stretch (1 mm at 50 mm s-1) at 5 s following deactivation of the muscle (Fig. 2).
|
Test 3 was aimed at quantifying the amount of loss of passive force enhancement by a quick shortening of the muscle. Passive force enhancement was obtained by stretching the muscle as described in test 1. 5 s following deactivation, the muscle was shortened by 4.5 or 9 mm (i.e. 50 or 100% of the active stretch amplitude), at a speed of 18 mm s-1, and immediately stretched back to its original length at a speed of 18 mm s-1. The passive force enhancements at 0.2 s prior to and 2 s following this passive shortening-stretch cycle were compared (Fig. 3).
|
Test 4 was aimed at isolating the passive component of force enhancement from the total force enhancement (active plus passive component). Passive force enhancement was obtained as in test 1. 5 s following deactivation of the muscle, the muscle was activated again isometrically for 5 s, and any remnant force enhancement was quantified at 4.8 s after reactivation of the muscle (label 3, Fig. 4).
|
Test 5 was aimed at determining whether shortening the muscle prior to the
stretch protocol influenced total and passive force enhancement. All stretches
were identical to those described in test 1 (9 mm amplitude at 3 mm
s-1). Preceding the stretches, the muscle was shortened by 3, 6 and
9 mm at a speed of 9 mm s-1, and total force enhancement (the force
enhancement measured while the muscle was still activated at 4.8 s following
the stretch) and passive force enhancement (5 s following deactivation) were
compared for the different conditions (Fig.
5). Note that 4.8 s following the active stretch, all force
transients associated with the dynamic stretch have mostly subsided (e.g.
Huxley, 1957;
Huxley and Simmons, 1971
;
Herzog and Leonard, 2002
).
Therefore, the force enhancement observed at this point in time may be
considered a steady-state value. We have shown previously that the force
enhancement at 4.8 s following the active stretch is virtually identical to
that at 25-30s following the active stretch
(Herzog and Rassier, 2002
), as
the force-time curves of the test and reference contraction are virtually
`parallel' to each other. Parallelism in this study was assessed by
approximating the force-time curves of the test contraction by a best-fitting
straight line from 4.3-4.8 s following the active stretch and comparing this
slope statistically to that obtained for the corresponding period of time of
the isometric reference contraction
(Wakeling et al., 2000
). To
our knowledge, all force enhancements described in the literature on mammalian
muscle at or near physiological temperatures were made at times <4.8 s
following the active stretch. Even in single fibers at low temperatures, where
contractile processes occur at a much reduced rate, force enhancement
measurements are rarely made at
4.8 s following the stretch (e.g.
Edman et al., 1978
: 179 ms, 478
ms and about 4.5 s; Edman et al.,
1982
: 4.5-6.0 s).
|
In test 6, the stiffness at the time of steady-state force enhancement following stretch was determined and compared to the stiffness of a purely isometric contraction at the same length. Force enhancement was obtained as described in test 1. Stiffness was determined using a quick stretch of 1mm amplitude at a speed of 50 mm s-1 at 4.8 s following the end of the stretch phase (Fig. 6).
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Finally, test 7 was aimed at determining whether or not the steady-state force-enhanced values could exceed the isometric force values at optimal length. For these tests, the muscles were stretched actively from an initial length of -6 mm to a final length of +3 mm. The activation was maintained for 5 s following the end of the stretch, and comparisons of values from the force-enhanced tests and the isometric reference tests at optimal muscle length were made at 4.8 s following the stretch.
All test contractions, in all seven experimental protocols, were preceded and followed by isometric reference contractions at the corresponding final length. If these two reference contractions were not within 0.1 N (i.e. approx. 0.4% of the maximal isometric force), the test trial was rejected, therefore any damage or fatigue effect could not have produced the observed force enhancement or passive force enhancement.
Data analysis
The force enhancement was determined as the difference between the
isometric force following the stretch and the isometric reference force at the
corresponding length. Force values were taken 4.8 s after the end of the
stretch, when a near steady-state force had been reached
(Herzog and Leonard, 2002).
Similarly, the passive force enhancement was assessed as the difference
between the passive isometric force following the stretch test and the passive
isometric force following the corresponding isometric reference contraction.
Force values were taken 5 s following deactivation of the muscle, when the
transient force decay following deactivation had subsided
(Herzog and Leonard, 2002
).
Non-parametric, repeated measures statistics (Wilcoxon matched-pair;
Hinkle et al., 1979
) were used
to test for force enhancement and passive force enhancement. The level of
significance was chosen at
=0.05.
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Results |
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Stiffness of the passive muscle tendon unit following active stretching was significantly greater (31%) than the stiffness following an isometric contraction at the corresponding muscle length or passive stretching of the muscle (Table 1). Anexample result of the stiffness assessment is shown in Fig. 2. This result suggests that the passive force enhancement is associated with the recruitment of an additional passive element, or the change in stiffness of a passive element.
When a muscle that has a substantial amount of passive force enhancement was quickly released (and immediately stretched back) by an amount that was equal to the active stretch that was used to produce the passive force enhancement (i.e. 9 mm in our case), all passive force enhancement was abolished instantaneously. When the same muscle was only released (and immediately stretched back) by 50% of the initial active stretch (i.e. 4.5 mm in our case), the passive force enhancement was almost completely retained (Table 1, Fig. 3). This behaviour is not consistent with that of a viscoelastic material, but could be explained with a material whose stiffness properties can change in a discontinuous way.
Following a 9 mm stretch of the active muscle from its zero reference length, we always observed a substantial amount of force enhancement at 4.8 s following the active stretch, and we always observed a corresponding passive force enhancement (Fig. 4, Table 1). Upon reactivation of the muscle, there remained a certain amount of force enhancement that was smaller than both the initial total force enhancement and the passive force enhancement. Following deactivation after the second stimulation period, passive force enhancement was still present in all muscles (Fig. 4, Table 1).
When shortening the muscle by 3, 6 and 9 mm prior to the 9 mm stretch, it was found that total and passive force enhancement decreased with increasing magnitudes of shortening (Table 1, Fig. 5). When subtracting the passive force enhancement value from the total force enhancement value, the remaining (active) force enhancement was independent of the amount of shortening preceding the stretch (Table 1). This last result suggests that the decrease in total force enhancement may be explained completely by the decrease in passive force enhancement. Therefore, it appears that the amount of shortening preceding the stretch directly affects the passive but not the active component of force enhancement.
Reports in the literature of stiffness measurements following active muscle
stretch, when a steady-state force enhancement has been achieved, have not
been consistent. Sugi and Tsuchiya
(1988) reported no increase in
stiffness in the force-enhanced state compared to the isometric reference
value, whereas Linari et al.
(2000
) found such an increase
in single fibres from frog. Unfortunately, the results by Linari et al.
(2000
) must be interpreted
with caution, as they were obtained very quickly following the stretch (175
ms), and therefore may not be relevant for the steady-state conditions
discussed here. Interestingly, the sarcomere length non-uniformity theory of
force enhancement predicts a decrease in stiffness in the force-enhanced state
compared to the isometric reference state
(Morgan et al., 2000
). We
found a consistent, and statistically significant, increase in muscle
stiffness in the steady, force-enhanced state compared to the isometric
reference value (Table 1,
Fig. 6). The average increase
in stiffness (11.5%) was similar in magnitude to the average steady-state
force enhancement (15.3%) observed in this study.
Finally, we detected force values in the force-enhanced state that exceeded the active isometric forces at optimal muscle length (Fig. 7). Although these force-enhanced values did not exceed the isometric plateau forces by a great amount (5.3±2.7%), this observation was made consistently in all ten muscles (P<<0.05), and was statistically significant, for all muscles when stretched by 9 mm at a speed of 3 mm s-1 to a final length of +3 mm.
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Discussion |
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Edman and Tsuchiya (1996)
found steady-state force enhancement after stretch of frog muscle fibres. This
force enhancement was linearly related to the slow component of tension rise
during stretch. In addition, when released against a small load, the
shortening 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 as originating from the
elongation of a passive, elastic, cytoskeletal protein.
Recently, we found direct evidence for passive force contribution to force
enhancement following active stretch in the cat soleus
(Herzog and Leonard, 2002).
This passive force enhancement was found as a persistent force enhancement
following deactivation of an actively stretched muscle. Passive force
enhancement was independent of the stretch speed, was directly dependent on
stretch magnitude, and contributed as much as 84% to the total force
enhancement for the greatest stretch amplitudes tested. Similar results to
those obtained for cat soleus have also been obtained for single fibres from
frog Rana pipiens (Rassier et al.,
2003
,
in press
) and for in
vivo human adductor pollicis (Lee and
Herzog, 2002
). Although not impossible, it might prove difficult
to identify the exact structure(s) responsible for the passive force
enhancement. As a first step in this direction, we determined the mechanical
properties of the passive force enhancement following active muscle stretch.
By doing this, we hoped to gain insight into what structural models might be
useful in explaining the passive force enhancement.
Out of the seven tests performed in this study, we felt that the results of
three were particularly revealing. The first of these results was the fact
that the passive force enhancement was long-lasting and persisted for >25 s
in all cases (Fig. 1, Table 1). Edman and Tsuchiya
(1996) had proposed a model of
passive force enhancement based on strain of elastic elements and variations
in filament overlap caused by nonuniform length changes within the fibre
volume. They argued that regions with greater filament overlap are likely to
generate the steady-state force enhancement following active stretch. The
elastic elements that were recruited during stretch were presumed to support
regions in which filament overlap had been reduced, thereby providing a force
equilibrium. However, in their model, deactivation of the muscle (fibre),
which results in a loss of the active force, would also result in the loss of
the passive component of the force enhancement because of the proposed
in-series arrangement of the passive and active component (fig. 9B in
Edman and Tsuchiya, 1996
).
However, we found in all cases that passive force enhancement persisted for a
long time following deactivation, thereby eliminating the passive force
enhancement model by Edman and Tsuchiya
(1996
), at least for the
conditions and the muscle tested here.
The second result that we judged important was that passive force
enhancement was reduced in a dose-dependent manner with the magnitude of
shortening preceding muscle stretch, whereas the active component of force
enhancement was unaffected by shortening
(Fig. 5,
Table 1). This result suggests
that `engagement' of the passive component of force enhancement occurs at the
length at which the muscle is activated. If stretched after activation, the
passive component will provide additional force. If shortened, the effect of
the passive component of force enhancement decreases in a dose-dependent
manner with the magnitude of shortening preceding the stretch. This result is
in contrast to the findings by Edman et al.
(1982), who reported that force
enhancement in single frog fibres was independent of shortening preceding
fibre stretching. However, aside from the obvious difference in preparations
(cat soleus vs. frog tibialis anterior fibres), there was a
methodological difference between the two studies that we thought might be
crucial. Edman et al. (1982
)
separated the stretch from the shortening by a 1 s delay, whereas in our
experiments, stretch of the soleus followed the shortening instantaneously. It
seemed quite possible that the 1 s delay used by Edman et al.
(1982
) may have reset the
`initial' length of the structures contributing to the passive force
enhancement, and may have produced the result that shortening preceding
stretch does not influence force enhancement. However, in the meantime we have
repeated the shortening-stretch experiments with various delays between the
shortening and the stretch phase, as was done by Edman et al.
(1982
), but we could not
reproduce Edman's results, neither in single fibres of frog (N=12)
(Herzog and Rassier, 2003
) nor
in the cat soleus (N=6) (Herzog,
2002
).
Probably the most important result of this study was the fact that the passive force enhancement could be eliminated `instantaneously' by shortening (and stretching back) the deactivated, passive muscle by 9 mm (i.e. 100% of the stretch amplitude) (Fig. 3, Table 1). In contrast, shortening (and stretching back) by 4.5 mm (50% of the stretch amplitude) left the passive force enhancement virtually unaffected. This result is evidence that the passive force enhancement is not caused by a purely viscoelastic component that is stretched and whose force is slowly decaying following the active stretch. Rather, it appears that a structural protein is either `engaged' at the initial muscle length, or that the `stiffness' of a structural protein is changed by active muscle stretch. This event is reversible by shortening the passive muscle to its original length, but is not significantly altered by shortening the muscle by 50% of its active stretch amplitude.
Finally, all of the remaining results support the idea that the passive component of force enhancement must be in parallel with the contractile component. This suggestion is supported by the increased stiffness of the passive and active muscle following active stretch compared to the purely isometric contractions at the corresponding muscle lengths (Figs 2, 6; Table 1). Furthermore, we found steady-state isometric forces that were in excess of the active isometric forces at optimum muscle length (after accounting for the passive forces associated with the increase in muscle length), suggesting that a parallel force component was added to the contractile force (Fig. 7). Finally, the passive force enhancement prior to and following a second isometric contraction (Fig. 4), was significantly greater than the passive force enhancement during the second isometric contraction1, suggesting that the passive component of force enhancement is in-parallel to the contractile component, and therefore was shorter in the active compared to the passive state. Therefore, passive force enhancement was smaller in the active compared to the passive muscle.
Possible explanation of results
The idea that force enhancement has the properties of a passive `elastic'
element has been proposed, but not directly demonstrated before
(Edman et al., 1982;
Noble, 1992
;
Edman and Tsuchiya, 1996
;
DeRuiter et al., 2000
). The
molecular spring titin has been suggested to fill this role, and although we
do not have direct evidence for a possible contribution of titin to the
passive force enhancement observed here, titin's properties and structural
arrangement appear consistent with the results found in this study.
First, titin is arranged in parallel with the active force producing
cross-bridges, at least if we assume that half-sarocomeres remain uniform in
length. If we assumed that half-sarcomere lengths became non-uniform, as did
Edman and Tsuchiya (1996), the
titin in the elongated half-sarcomere would resist the active forces in the
corresponding shortened half-sarcomere, and in that case, titin would be
arranged in-series with the active force-producing elements, and the
persistent passive force enhancement following deactivation of the stretched
muscle observed in this study, would not be possible.
In order for titin to contribute to the force enhancement, as observed
here, titin's stiffness, or its characteristic length, would need to change
for actively stretching muscle compared to isometrically contracting or
passively stretched muscle. There is no direct evidence that titin changes its
stiffness or characteristic length upon active stretching. However, titin has
been found to change its stiffness under specific conditions. Tatsumi et al.
(2001) showed that the
secondary structures of the elastic part of titin were changed by the binding
of calcium ions. They concluded from this result that the stiffness of titin
changes during the contraction-relaxation cycle. Similarly, Yamasaki et al.
(2001
) found that cardiac
titin interacted with actin in a dose-dependent manner based on the
concentration 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. Summarizing, titin has been found to change its stiffness,
and therefore, characteristic force. This change has been associated with
calcium concentration. Therefore, it appears feasible to hypothesize that
titin's characteristic stiffness may be increased when stretching an active
compared to a relaxed muscle. This increased stiffness may be the reason for
the observed passive component of force enhancement. This thinking would be
consistent with the increased stiffness in the force-enhanced (active and
passive) states compared to the isometric states
(Fig. 6,
Table 1). It would also allow
for the possibility to produce steady-state forces following active stretch
that exceed the peak active isometric forces at muscle optimum length
(Fig. 7). Also, with titin
being arranged in parallel to the contractile element (in uniform
half-sarcomeres), the result that passive force enhancement is smaller in the
active compared to the relaxed muscle (because of contractile element
shortening) is also accounted for (Fig.
4). Finally, it is well known that titin's stiffness is
associated, in part, with the unfolding of molecular knots in the
immunoglobulin region (Rief et al.,
1997
). It has been shown that refolding of the immunoglobulin
domains only occurs when force in titin becomes very low and titin is relaxed
to its initial characteristic length. This property of titin would explain why
a 4.5 mm shortening of the passive muscle did not abolish the passive force
enhancement, but a 9 mm shortening (corresponding to the amount of active
stretch) eliminated all passive force enhancement instantaneously.
In summary, we were able to measure some crucial properties of muscle in
the passive force-enhanced state. These properties can be used to eliminate
possible candidate models, for example, the one proposed by Edman and Tsuchiya
(1996), and include others, for
example, titin, as long as half sarcomeres remain at uniform length. However,
it should be stressed that further experiments must be performed to identify
the true source of the passive component of force enhancement.
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Acknowledgments |
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Footnotes |
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References |
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