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Journal of Biomechanics 33 (2000) 659}668

The relationship between force depression following shortening
and mechanical work in skeletal muscle
W. Herzog*, T.R. Leonard, J.Z. Wu
Human Performance Laboratory, The University of Calgary, Faculty of Kinesiology, 2500 University Drive, N.W., Calgary AB T2N 1N4, Canada
Accepted 20 December 1999

Abstract

Force depression following muscle shortening was investigated in cat soleus (n"6) at 373C for a variety of contractile conditions
with the aim to test the hypotheses that force depression was independent of the speed of shortening and was directly related to the
mechanical work produced by the muscle during shortening. Force depression was similar for tests in which the mechanical work
performed by the muscle was similar, independent of the speed of shortening (range of speeds: 4}256 mm/s). On the other hand, force
depression varied signi"cantly at a given speed of shortening but di!erent amounts of mechanical work, supporting the hypothesis
that force depression was not speed * but work dependent. The variations in the mechanical work produced by the muscle during
shortening accounted for 87}96% of the variance observed in the force depression following shortening further supporting the idea
that the single scalar variable work accounts for most of the observed loss in isometric force after shortening. The results of the present
study are also in agreement with the notion that the mechanism underlying force depression might be associated with an inhibition of
cross-bridge attachments in the overlap zone formed during the shortening phase, as proposed previously (Herzog and Leonard, 1997.
Journal of Bimechanics 30 (9), 865}872; MareH chal and Plaghki, 1979. Journal of General Physiology 73, 453}467).  2000 Elsevier
Science Ltd. All rights reserved.

Keywords: Whole muscle mechanics; Mechanism of muscular force production; Concentric contraction; Cat soleus

1. Introduction scribe force depression mathematically. One of the excep-
tions is the work by MareH chal and Plaghki (1979) who
The isometric force in muscle following shortening showed that force depression is linearly related to the
against resistance is lower (depressed) compared to the amount of shortening and that the linearity constant
isometric force obtained at the same length without prior depended on where on the force}length relationship the
shortening. This observation has "rst been described by experiments were performed. They further described that
Abbott and Aubert (1952), and has since been con"rmed force depression was an inverse exponential function of
on many occasions (e.g. Edman et al., 1993; Herzog and the speed of shortening. Similar "ndings have been re-
Leonard, 1997; MareH chal and Plaghki, 1979; Meijer et al., ported by others (Abbott and Aubert, 1952; De Ruiter
1997; Sugi and Tsuchiya, 1988). The mechanism underly- et al., 1998).
ing force depression following shortening is not known, Recently, based on results in cat soleus, it was pro-
although several mechanisms have been proposed in the posed that force depression may be independent of the
past (Edman et al., 1993; Granzier and Pollack, 1989; speed of shortening, but rather may depend on the force
Herzog and Leonard, 1997; MareH chal and Plaghki, 1979). during shortening (Herzog and Leonard, 1997). This
Because of the lack of a generally accepted mechanism "nding led to the suggestion of a mechanism of force
for force depression following muscle shortening, re- depression following shortening based on the mechanical
searchers have largely refrained from attempting to de- deformation of actin "laments entering the actin-myosin
overlap zone during shortening (MareH chal and Plaghki,
1979), and a corresponding change in the relative orienta-
* Corresponding author. Tel.: #1-403-220-8525; fax: #1-403-284- tion between myosin cross-bridges and actin-binding
3553. sites that might reduce the probability for cross-bridge
E-mail address: walter@kin.ucalgary.ca (W. Herzog). attachments in the newly formed overlap zone. Since

0021-9290/00/$ - see front matter  2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 1 - 9 2 9 0 ( 0 0 ) 0 0 0 0 8 - 7
660 W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668

actin myo"laments are known to be compliant (Gold- A second cut was made on the posterior, lateral thigh
man and Huxley, 1994; Higuchi and Goldman, 1995; and the tibial nerve was exposed and implemented with
Huxley et al., 1994; Kojima et al., 1994; Wakabayashi a bipolar cu!-type electrode (Herzog et al., 1995) for
et al., 1994), and since this compliance is associated with soleus stimulation. The cat was secured in a prone posi-
changes in the three-dimensional orientation of actin and tion in a hammock and the pelvis, thigh, and shank of the
myosin "laments (Daniel et al., 1998), a stress-dependent experimental hindlimb were "xed with bilateral bone
inhibition of cross-bridges in the overlap zone formed pins to a stereotaxic frame. The bone piece at the distal
during shortening becomes an attractive (and possible) end of the soleus tendon was attached with sutures to
mechanism (Herzog, 1998). Results on isolated frog "bres a muscle puller (MTS, Eden Prairie, MN, natural fre-
show that sti!ness decreases in parallel with the amount of quency '10 kHz). The soleus forces (100 N"10 V) and
force depression following shortening (Sugi and Tsuchiya, excursions (20 mm"10 V) were measured continuously
1988), supporting the idea that force depression may be by the muscle puller and were collected at a frequency of
associated with a decrease in the number of attached 200 Hz, except for tests exceeding a shortening speed of
cross-bridges compared to purely isometric contractions. 64 mm/s for which data were collected at 1000 Hz. The
If force depression following shortening is caused by muscle length corresponding to the 803 included ankle
a stress-dependent deformation of actin (and possibly angle was taken as zero length; shortening from that
myosin) "laments, force depression should be indepen- length was taken as negative, lengthening as positive. For
dent of the speed of shortening, but should depend on the example, a muscle length of !4 mm corresponds to
amount of shortening and the stress (force) acting on the a length 4 mm shorter than the reference length.
myo"laments during shortening. Furthermore, force de- Six series of tests were performed. In the "rst series of
pression should occur continuously during the shorten- tests, an isometric contraction at a given length was
ing phase. Therefore, it appears that force depression followed by a shortening contraction at a given speed
following shortening might depend primarily on a single and constant activation but varying amount of shorten-
scalar variable, the work performed by the muscle during ing, followed by a second isometric contraction at the
the shortening phase. Although it has been suggested new (shortened) length. The "nal length was always
that work may be associated with force depression (De !4 mm; the starting lengths were (typically) !2, 0,
Ruiter et al., 1998; Granzier and Pollack, 1989; Herzog, #2, #4, and #6 mm. The speed of shortening was
1998), no systematic study has been conducted to investi- 4 mm/s and the stimulation of the tibialis nerve was three
gate the possible relationship between work and force times the a-motoneuron threshold (3 T), 30 Hz, 0.1 ms
depression in skeletal muscle. pulse duration, and 8 s train duration. For the cat soleus
The purpose of this study was to test whether or not (a primarily slow twitch "bred muscle (Ariano et al.,
the single scalar variable work could account for most of 1973)), this stimulation protocol resulted in a fused teta-
the observed force depression following skeletal muscle nic contraction of (likely) all motor units.
shortening under a variety of conditions. Speci"cally, In the second series of tests, isometric-shortening-
shortening contractions were performed by keeping two isometric contractions were performed with constant ac-
of the three determinant variables of shortening (amount tivation (3 T, 30 Hz, 0.1 ms, 8 s) and constant amount of
of shortening, speed of shortening, and muscle activation shortening (8 mm) but varying speeds (typically, 4, 8, 16,
during shortening) constant, while the third variable was 32, 64, 128 and 256 mm/s).
varied in a systematic way. Furthermore, tests were per- In the third series of tests, isometric-shortening-
formed with variable speeds and variable activation of isometric contractions were performed at a constant
the muscle during the shortening phase. speed (4 mm/s) over a constant shortening range (8 mm)
but varying levels of activation during the shortening
phase ranging from 0 to 3 T in about 4}8 steps. The exact
2. Methods current provided to the tibial nerve for the varying levels
of activation were di!erent from muscle to muscle and
Force depression following shortening was determined changed within a muscle for di!erent tests because of the
in cat soleus (n"6) using a setup that has been described ever changing threshold level for a-motoneuron stimula-
earlier (Herzog and Leonard, 1997; Herzog, 1998). Brie- tion. The activation of the muscle was constant for the
#y, cats were anaesthetized using a nitrous oxide, halo- initial and "nal isometric contractions (3 T, 30 Hz,
thane, oxygen mixture. The soleus, soleus tendon and 0.1 ms).
calcaneus were exposed using a single cut on the poste- The fourth series of tests was identical to the third,
rior, lateral shank. The soleus tendon was isolated from except there was no shortening, and therefore no work
the rest of the Achilles tendon and was cut from the performed by the muscle, when the level of activation was
calcaneus with a remnant piece of bone after a reference changed.
length (corresponding to an 803 included ankle angle) In the "fth series of tests, shortening over a given
had been determined. distance (8 mm) and constant activation (3 T, 30 Hz,
W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668 661

0.1 ms) was performed using a variety of changing speeds.
The changes in speed were controlled by the computer
that controlled the muscle puller. In our setup, any speed
change that can be expressed as a function of time can be
implemented. The speci"c speed changes chosen for this
experiment are shown as part of Fig. 5 in the results
section. In the last series of tests, the amount of shorten-
ing (8 mm) and the speed of shortening (4 mm/s) were
kept constant whereas activation during the shortening
phase was varied.
In all six series of tests, two identical isometric-
shortening-isometric tests were preceded and followed
by an isometric reference contraction at the "nal length.
Force depression was determined as the di!erence in
force between the isometric reference contraction and the
steady-state isometric force following shortening (i.e.
3 s after the end of any shortening contraction in a given
experiment). This di!erence in force was determined
at the same instant in time for the reference and the
experimental contractions to avoid any bias caused by
fatigue-related loss of force. Work performed by the
muscle was calculated as the area under the muscle
force}length change graph. Calculating the work for each
trial of all six series of tests gave, on average, about 50}60
values per muscle that could be related to the force
depression values. These 50}60 values represent 25}30
independent measurements that were repeated once.
Since the repeat measurements were nearly identical in
all cases, they were not used for deriving the relation
between work and force depression. A least-squares "t-
ting power function that was forced through the origin
(zero force depression, zero work) was used to describe
Fig. 1. Representative force}time histories of isometric reference con-
the relationship between work and force depression. tractions at a muscle length of !4 mm, and force}time histories for
Also, force depression values were plotted as a function of isometric-shortening-isometric contractions (a) in which the shortening
the speed of shortening. All experimental procedures distance was varied from 2 to 10 mm as shown (b). Shortening speed
were approved by the animal ethics committee of the (4 mm/s) and activation (maximal) were kept constant. The correspond-
University of Calgary. ing work}time histories for the above contractions (c).

3. Results shortening phase, and since the amount and speed of
shortening were kept constant, the work performed by
Force depression following muscle shortening was dir- the muscle during shortening was also increased for in-
ectly related to the amount of shortening (Fig. 1a); sim- creased tibial nerve stimulations (Fig. 3c). When activa-
ilarly, the work performed by the muscle was increased tion was decreased for a 2 s period without any
with increasing amounts of shortening (Fig. 1c). shortening of the muscle, no work was performed in the
Force depression was inversely related to the speed of process and there was no force depression upon full
shortening (Fig. 2a), and, for a given amount of shorten- reactivation (Fig. 4).
ing and constant activation, work of the muscle was Performing isometric-shortening-isometric contrac-
decreased with increasing speeds of shortening (Fig. 2c). tions at variable speeds or variable stimulation of the
This latter result is caused by a decrease in the force tibial nerve during the shortening phase resulted in force
during the shortening phase as the speed of shortening depressions that were directly related to the di!erent
increases. It is merely a re#ection of the force}velocity amounts of work performed by the shortening muscle
property of skeletal muscle (Hill, 1938). (Figs. 5 and 6, respectively).
Force depression was increased for increasing levels The work performed by the muscle during shortening
of tibial nerve stimulation (Fig. 3a). Increased accounted, on average, for 92% ($3% S.D.) of the force
stimulation caused an increase in the force during the depression for all six muscles with a range from 87 to
662 W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668

Fig. 2. Representative force}time histories of isometric reference con- Fig. 3. Representative force}time histories of isometric reference con-
tractions at a muscle length of !4 mm, and force}time histories for tractions at a muscle length of !4 mm, and force}time histories of
isometric-shortening-isometric contractions (a) at di!erent speeds of isometric-shortening-isometric contractions at four levels of activation
shortening varying from 4 to 128 mm/s (b). Shortening distance (8 mm) varying from zero to maximal during the shortening phase (a) Note,
and activation (maximal) were kept constant. The corresponding that the magnitude of force depression increased with increasing work
work}time histories for the above contractions (c). performed by the muscle; i.e. the amount of force depression increased
from trace b to c, to d, to e, as expected. The shortening distance (8 mm)
and shortening speed (4 mm/s) were kept constant (b). The correspond-
ing worktime histories for the above conditions (c).
96% Figs. 7(a}f). Although, a casual glance at Figs. 7(a}f)
might give the impression that the force depression-work
relationships vary much across muscles, it should be 4. Discussion
noted that the raw data for all muscles are remarkably
similar. When combining all force depression and work Force depression following shortening in skeletal
values shown in Figs. 7(a}f) in a single graph, the result- muscles has been associated primarily with the amount
ing power relationship is still strong (Fig. 8; r"0.85), i.e. of shortening, and the shortening speed (Abbott and
85% of the variance in force depression across all six Aubert, 1952; MareH chal and Plaghki, 1979). The most
muscles and all six tests was explained by the variance in common mechanism related to force depression has been
the mechanical work of the muscle. sarcomere length non-uniformity (Edman et al., 1993).
When plotting force depression as a function of the For a variety of reasons, shortening speed and sarcomere
shortening speed, two observations were made: "rst, length non-uniformity appear less attractive as candidate
force depression was similar for experiments performed mechanisms at present than they might have in the past.
at vastly di!ering speeds provided that the work during For example, it has been demonstrated earlier (Herzog
shortening was similar, and second, force depression var- and Leonard, 1997), and in this study, that force depress-
ied greatly for a given speed of shortening, provided that ion may vary substantially in tests in which the shorten-
the work varied as well (Fig. 9). ing distance and speed are kept constant and force during
W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668 663

Fig. 4. Representative force}time histories of isometric contractions in
which activation was changed for a 2 s period following full force
development. Note, no work was performed during this process as there
was no muscle shortening. There was no force depression associated
with the change in activation levels.

Fig. 6. Representative force}time histories of isometric reference
contractions at a muscle length of !4 mm, and force}time histories
of isometric-shortening-isometric contractions (a). The activation
during the shortening phase was varied systematically, here, for
example, by deactivating the muscle for the "rst 500, 1000, 1500, and
2000 ms of the shortening phase and then reactivating it maximally.
The distance (8 mm) and speed of shortening (4 mm/s) were kept con-
stant (b). The corresponding work}time histories for the above condi-
tions (c).

shortening is varied (Fig. 3). Furthermore, we found
consistently that force depression was similar when the
mechanical work performed by the muscle during
shortening was similar, even if the speed of shortening
was changed from the low (4 mm/s) to the high extreme
(256 mm/s) tested in this study (Fig. 9). These results
suggest that it is the work rather than the speed of
shortening that is related to the force depression.
Similarly, the sarcomere length non-uniformity mecha-
Fig. 5. Representative force}time histories of isometric reference con- nism cannot explain the observation by Granzier and
tractions at a muscle length of !4 mm, and force-time histories of Pollack (1989) that force depression is virtually identical
isometric-shortening-isometric contractions (a). The speed of shorten-
ing was varied continuously in these contractions, whereas the shorten- for "xed end and sarcomere length controlled contrac-
ing distance (8 mm) and activation (maximal) were kept constant (b). tions in isolated frog skeletal muscle "bres. Also, sar-
The corresponding work}time histories for the above conditions (c). comere length non-uniformity has been suggested as
664 W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668

Fig. 7. Relationship between the amount of depressed force as a function of the work performed by the muscle during the shortening phase for all six
muscles (a}f) and for all six experimental conditions (the di!erent symbols are associated with the di!erent experimental conditions). Also, shown is the
best-"tting power function that goes through the origin (0, 0) of the force}work plot and the corresponding coe$cient of variation, R.

a mechanism for force enhancement following eccentric Recently, it has been found that actin myo"laments are
contractions (Edman and Tsuchiya, 1996), and it is hard compliant (Goldman and Huxley, 1994; Higuchi and
to reconcile how a single mechanism may explain two Goldman, 1995; Huxley et al., 1994; Kojima et al., 1994;
opposite phenomena (force depression and force en- Wakabayashi et al., 1994) and may account for as much
hancement) simultaneously. as 50}70% of the total sarcomere compliance (Daniel
W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668 665

depends on the amount of force during shortening. The
higher the force, the greater the elongation of the actin
"lament, and the larger the force depression, presumably
because of the increased actin "lament deformation. If
the amount of force is constant, the work performed
depends exclusively on the amount of shortening. For
this situation, the larger the amount of shortening, the
greater the newly formed overlap zone (Fig. 11, n) and the
larger the force depression, presumably because there is
an increased area of overlap between actin and myosin
"laments containing deformed actin "laments with a re-
duced probability for cross-bridge attachments com-
pared to the same zone of overlap in an isometric
contraction.
Although it has been mentioned anecdotally that
work might be related to force depression (De Ruiter
Fig. 8. Relationship between the amount of depressed force as a func- et al., 1998; Granzier and Pollack, 1989; MareH chal
tion of the work performed. Data from all six muscles and all six and Plaghki, 1979), no systematic study has ever been
experimental tests were combined, illustrating the similarity of the performed to explore the possible relationship between
relationship across muscles and tests. Note, that neither the force nor these two variables. Here, we show that the work per-
the work data were normalized in any way, suggesting that the relation-
ship holds independent of the size or maximal force of the muscle. formed by the muscle explains virtually the entire vari-
ation in force depression for a variety of di!erent tests
(Figs. 7 and 8). In addition, the relationship between the
et al., 1998). Furthermore, it has been demonstrated that absolute force depression and the absolute work across
actin "laments undergo the largest deformation in the all six muscles was similar (Fig. 8), resulting in a strong
non-overlap region (Forcinito et al., 1997) and that relationship across all muscles and all tests (r"0.85).
these deformations cause an altered orientation between We conclude from these results that work is a good
the actin-binding sites and the myosin cross-bridges descriptor of force depression, that force depression is
which may alter the probability of cross-bridge attach- likely not related to the speed of shortening but rather to
ment (Daniel et al., 1998). Therefore, the idea that the force or work that is changed with changing speeds
force depression is related to a stress-induced cross- (Fig. 9), and that work might not only be a descriptor of
bridge inhibition in the actin}myosin overlap zone that force depression but may point directly to an underlying
is formed during shortening (Herzog and Leonard, mechanism.
1997; Herzog, 1998; MareH chal and Plaghki, 1979) If force depression following muscle shortening is
becomes a distinct possibility. This mechanism requires caused by stress-induced inhibition of cross-bridge at-
that force depression following muscle shortening is inde- tachments in the newly formed actin}myosin overlap
pendent of the speed of shortening, but depends both on zone, two so far untested hypotheses should hold: (1)
the amount of shortening and the force during shorten- muscle in the force-depressed state should be less sti!
ing. Furthermore, this mechanism requires that force than muscle in the normal isometric state. Although,
depression is a process that starts immediately upon such a correlation between sti!ness and depressed force
shortening and is cumulative during the shortening has been demonstrated in an earlier study on frog "bre
phase. All these requirements suggest that there must be preparations (Sugi and Tsuchiya, 1988), single "bres
a direct and strong link of force depression with muscular might behave distinctly di!erent than whole mammalian
work. skeletal muscle. (2) Force depression should be abolished
The way force depression may be associated with the instantaneously if the stress in the muscle is completely
amount of work performed by the muscle through actin released. Although such stress release experiments have
"lament deformation may be explained as follows. Work, been performed in the past (Abbott and Aubert, 1952; De
by de"nition, is the area under the force}displacement Ruiter et al., 1998; Herzog and Leonard, 1997), they were
curve (Fig. 10). It is a function of the amount of force and accomplished by interrupting the stimulation during the
shortening the muscle undergoes. The higher the force for force-depressed phase. Therefore, one might argue that
a given amount of shortening, or the larger the amount of the recovery of force was related to the interruption of
shortening for a given force, the larger the mechanical stimulation and the muscle's reactivation after a su$-
work produced. If the amount of shortening is constant, cient period of time, rather than the release of force
one would expect the newly formed overlap zone be- accompanying the interruption of stimulation. In order
tween actin and myosin "laments to be constant, on to test whether a stress release without a change in
average (Fig. 11). For this situation, force depression just activation will abolish force depression, a muscle should
666 W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668

Fig. 9. Relationship between the amount of depressed force as a function of the speed of shortening for all six muscles (a}f) and for the tests shown in
Figs. 1 and 2 (diamonds and squares, respectively), plus a series of shortening contractions performed at di!erent constant speeds and a shortening
distance of 4 mm (crosses). Note, that the amount of depressed force varies greatly for a given speed of shortening when the work produced during
shortening is di!erent (vertical dashed line), and further, how di!erent speeds of shortening (4}256 mm/s) result in similar force depression when the
work performed during shortening is similar (horizontal dashed line).

be shortened "rst to produce force depression. Then, the at zero external force, and so, no stress on the contractile
muscle should be allowed to shorten a second time at myo"laments. Based on the stress-dependent cross-
a speed exceeding its maximal speed of shortening, there- bridge inhibition mechanism, the force depression that
fore, most of the second shortening contraction is made was present following the "rst shortening contraction
W. Herzog et al. / Journal of Biomechanics 33 (2000) 659}668 667

Fig. 11. Schematic illustration of the increase in thick/thin myo"lament
overlap during shortening. The unlabelled arrow represents the com-
mon overlap zone at the long and short sarcomere length. The arrow
labelled `na represents the new overlap zone between a thick/thin
myo"lament pair which was formed because of sarcomere shortening.

Fig. 10. De"nition and calculation of work. Work was calculated as the
area under the force}displacement curve.
Ariano, M.A., Armstrong, R.B., Edgerton, V.R., 1973. Hindlimb muscle
"ber populations of "ve mammals. Journal of Histochemistry and
Cytochemistry 21 (1), 51}55.
should be abolished completely following the second Daniel, T.L., Trimble, A.C., Chase, P.B., 1998. Compliant realignment
shortening contraction. of binding sites in muscle: transient behaviour and mechanical
tuning. Biophysical Journal 74, 1611}1621.
Summarizing, this study provides "rst systematic evid- De Ruiter, C.J., de Haan, A., Jones, D.A., Sargeant, A.J., 1998. Shorten-
ence that force depression is largely accounted for by the ing-induced force depression in human adductor pollicis muscle.
mechanical work performed by the muscle during Journal of Physiology 507 (2), 583}591.
shortening (Figs. 7 and 8). Furthermore, the results of this Edman, K.A.P., Caputo, C., Lou, F., 1993. Depression of tetanic force
study indicate that force depression following shortening induced by loaded shortening of frog muscle "bres. Journal of
Physiology 466, 535}552.
at a wide variety of speeds is the same provided the work Edman, K.A.P., Tsuchiya, T., 1996. Strain of passive elements during
performed during the shortening phase is about the same force enhancement by stretch in frog muscle "bres. Journal of
(Fig. 9). Finally, the muscle work during the shortening Physiology 490 (1), 191}205.
phase may directly point to a mechanism of force de- Forcinito, M., Epstein, M., Herzog, W., 1997. Theoretical consider-
pression based on cross-bridge inhibition caused by ations on myo"bril sti!ness. Biophysical Journal 72, 1278}1286.
Goldman, Y.E., Huxley, A.F., 1994. Actin Compliance: are you pulling
mechanical deformation of myo"laments. Although the my chain?. Biophysical Journal 67, 2131}2136.
present study cannot rule out the most popular mecha- Granzier, H.L.M., Pollack, G.H., 1989. E!ect of active pre-shortening
nism associated with force depression: sarcomere length on isometric and isotonic performance of single frog muscle "bres.
non-uniformity; it provides support for a mechanism Journal of Physiology 415, 299}327.
based on myo"lament deformation (Herzog and Leo- Herzog, W., 1998. Muscle modelling. Journal of Electromyography
Kinesiology 8, 59}60.
nard, 1997; Herzog, 1998; MareH chal and Plaghki, 1979) Herzog, W., Leonard, T.R., 1997. Depression of cat soleus forces follow-
and the associated change in three-dimensional geometry ing isokinetic shortening. Journal of Biomechanics 30 (9), 865}872.
of cross-bridge attachment (Daniel et al., 1998). Herzog, W., Leonard, T.R., Stano, A., 1995. A system for studying the
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Acknowledgements Higuchi, H., Goldman, Y.E., 1995. Sliding distance per ATP molecule
hydrolyzed by myosin heads during isotonic shortening of skinned
This study was supported by an operating grant from muscle "bers. Biophysical Journal 69, 1491}1507.
Hill, A.V., 1938. The heat of shortening and the dynamic constants
the Natural Sciences and Engineering Research Council
of muscle. Proceedings of the Royal Society of London, pp.
of Canada (NSERC), and a postdoctoral fellowship grant 136}195.
for J.Z. Wu from the Alberta Heritage Foundation for Huxley, H.E., Stewart, A., Sosa, H., Irving, T., 1994. X-ray di!raction
Medical Research (AHFMR). measurements of the extensibility of actin and myosin "laments in
contracting muscles. Biophysical Journal 67, 2411}2421.
Kojima, H., Ishijima, A., Yanagida, T., 1994. Direct measurement of
sti!ness of single actin "laments with and without tropomyosin by
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