ARTICLE IN PRESS

Journal of Biomechanics 38 (2005) 2190–2197

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Does the speed of shortening affect steady-state force

depression in cat soleus muscle?
T.R. Leonard, W. Herzog
Human Performance Laboratory, University of Calgary, 2500 University Drive N.W., Calgary, Canada AB T2N 1N4
Accepted 27 September 2004

Abstract

It has been stated repeatedly for the past 50 years that the steady-state force depression following shortening of an activated
muscle depends on the speed of shortening. However, these statements were based on results from experiments in which muscles
were shortened at different speeds but identical activation levels. Therefore, the force during shortening was changed in accordance
with the force–velocity relationship of muscles: that is, increasing speeds of shortening were associated with decreasing forces, and
vice versa. Consequently, it is not possible at present to distinguish whether force depression is caused by the changes in speed, as
frequently stated, or the associated changes in force, or both. The purpose of this study was to test if force depression depends on the
speed of shortening. We hypothesized that force depression was dependent on the force but not the speed of contraction. Our
prediction is that the amount of force depression after shortening contractions at different speeds could be similar if the force during
contraction was controlled at a similar level. Cat soleus muscles (n ¼ 7) were shortened by 9 or 12 mm at speeds of 3, 9, and 27 mm/s,
first with a constant activation during shortening (30 Hz), then with activation levels that were reduced (o30 Hz) for the slow speeds
(3 and 9 mm/s) to approximate the shortening forces of the fast speed contractions (27 mm/s). If done properly, force depression
could be precisely matched at the three different speeds, indicating that force depression was related to the force during the
shortening contraction but not to the speed. However, in order to match force depression, the forces during shortening had to be
systematically greater for the slow compared to the fast speeds of shortening, suggesting that force depression also depends on the
level of activation, as force depression at constant activation levels can only be matched if the force during shortening, evaluated by
the mechanical work, is identical. Therefore, we conclude that force depression depends on the force and activation level during
shortening, but does not depend on the speed of shortening as has been assumed for half a century. These results support, but do not
prove, the current hypothesis that force depression is caused by a stress-related cross-bridge inhibition in the actin–myosin overlap
zone that is newly formed during muscle shortening.
r 2004 Elsevier Ltd. All rights reserved.

Keywords: Muscle; Force depression; Cat; Soleus; History dependence

1. Introduction referred to as steady-state, or residual, force depression

It has been known for a long time, and is universally
accepted, that the steady-state isometric force of a
muscle is decreased if the isometric contraction is
preceded by shortening of the activated muscle (e.g.
Abbott and Aubert, 1952). This property is typically
Corresponding author. Tel.: +1 403 220 8525; fax:
+1 403 284 3553.
E-mail address: walter@kin.ucalgary.ca (W. Herzog).
(Fig. 1). Force depression is known to increase with
increasing magnitudes of shortening (Abbott and
Aubert, 1952; Maréchal and Plaghki, 1979; Meijer
et al., 1998; Josephson and Stokes, 1999). Furthermore,
force depression is long lasting (i.e., in excess of 20 s;
(Abbott and Aubert, 1952; Herzog et al., 1998)) and is
associated with a decrease in the stiffness of the muscle
or single fibre in the force-depressed compared to the
isometric reference state (Sugi and Tsuchiya, 1988; Lee
and Herzog, 2003). Also, force depression following

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doi:10.1016/j.jbiomech.2004.09.028
 ARTICLE IN PRESS
T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197
Fig. 1. An isometric-shortening-isometric contraction and a purely
isometric reference contraction at the same final muscle length. The
difference in force after the test contraction has reached steady-state
force following shortening is defined as the steady-state force
depression.
shortening can be abolished instantaneously by deacti-
vating the muscle just long enough for force to drop to
zero (Abbott and Aubert, 1952; Herzog and Leonard,
1997).
It has also been argued that force depression is
directly influenced by the speed of shortening (Abbott
and Aubert, 1952; Maréchal and Plaghki, 1979; Sugi
and Tsuchiya, 1988; Meijer et al., 1997; Herzog and
Leonard, 1997; Morgan et al., 2000; De Ruiter et al.,
2000; Lee and Herzog, 2003). This argument has been
based on experiments in which a muscle was shortened
by a given magnitude and with a given activation, but at
different speeds, and the force depression was observed
to consistently increase with decreasing speeds of
shortening. However, for these experimental conditions,
the changes in speed of shortening would also be
associated with changes in the force during shortening,
in accordance with the force–velocity properties of
skeletal muscles ((Hill, 1938); Fig. 2). Maréchal and
Plaghki (1979) used a modified form of the Hill
force–velocity relationship to relate the observed force
deficit to the shortening speed of the muscle. They
suggested that the force deficit was related to the force
during release. Their experiments were performed on the
sartorius muscle of the frog at 0 1C. Morgan et al. (2000)
reported that given the shape of the force–velocity
curve, faster shortening would reduce the force deficit
2191
Fig. 2. Force time histories of an isometric reference contraction (r)
and two isometric-shortening-isometric test contractions performed at
a slow (s—3 mm/s) and a fast (f—27 mm/s) shortening speed. Note
how the fast shortening contraction (f) is associated with much lower
forces than the slow shortening contraction (s), a result that is perfectly
explained with the force–velocity properties of muscle (Hill, 1938).
However, because of the force–velocity relationship, it is not clear if it
is the speed, the force or both the speed and force that produce the
difference in force depression for the two test contractions. FDs=force
depression for the slow contraction. FDf=force depression for the fast
contraction. FDs4FDf.
and that this was most likely due to differences in
shortening speed between strong and weak sarcomeres
being reduced at high compared to slow speeds of
shortening. The experiments by Morgan et al. (2000)
were performed on cat soleus muscle.
However, in both sets of experiments, muscle activa-
tion was held constant during the contraction, and so
the force during shortening changed as a function of the
speed of shortening. Therefore, it was not possible to
determine whether the observed changes in force
depression were associated with the changes in speed
or the changes in force during shortening, or both.
Recently, we performed experiments in which the cat
soleus muscle was shortened by a given amount and a
fixed speed, but force was changed, either by altering the
voltage or the frequency of nerve stimulation (Herzog
and Leonard, 1997). Force depression for these condi-
tions was directly proportional to the force produced
during the shortening phase, providing direct evidence
that the force during shortening influences force
depression (Fig. 3). However, these results gave no
information about the possible effect of the speed of
 ARTICLE IN PRESS
2192 T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197
Fig. 3. Force time histories for an isometric reference contraction (r)
and four isometric-shortening-isometric test contractions (b, c, d, e)
performed at identical speeds and for identical magnitudes of
shortening but at different activation (voltage) levels. Note that the
highest force during shortening (e) gives the greatest force depression,
and force depression decreases with decreasing forces during the
shortening phase. These results indicate that force depression depends
on the force during shortening. Normalized level of activation is shown
in the third panel with 1 indicating full activation and 0 referring to no
activation.
shortening on force depression. Such information would
be valuable for providing insight into the possible
mechanisms responsible for force depression in skeletal
muscles.
Therefore, the purpose of this study was to test if
force depression was truly influenced by the speed of
shortening, as currently assumed, or if the changes in
force depression observed with changing speeds were
merely a by-product of the changes in force in
accordance with the force–velocity properties. In order
to address this question, we used an in situ cat soleus
preparation and performed shortening contractions at
different speeds, but similar forces. This was accom-
plished by changing the activation of the muscle so that
the effects of the force–velocity property were compen-
sated for by activation, and forces during shortening
were similar despite the different speeds. We hypothe-
sized that the speed of shortening did not influence force
depression. In other words, force depression should be
the same if the forces during shortening were the same,
independent of the speed of shortening. Stated another
way, if force depression was the same for different
speeds of shortening, then the forces during shortening
had to be the same as well.
2. Methods
2.1. Animal preparation
Experiments were performed with the cat soleus
(n ¼ 7) as described previously (Herzog and Leonard,
1997; Herzog et al., 2000). Animals were anaesthetized
using an Isoflurane/O2/N2O mixture. Adult male cats
ranging in mass from 3.2 to 6.4 kg were used. A silicone
nerve cuff-type electrode was implanted on the tibial
nerve. The soleus muscle was exposed and the calca-
neous cut with a remnant bone chip attached to the
distal end of the Achilles tendon. All plantar-flexors,
except for the soleus, were cut at the Achilles tendon.
The animal was placed in a stereotaxic device and
the pelvis, femur and tibia were fixed with bone pins at
the posterior iliac spine, the femoral condyles and the
malleoli, respectively. The soleus tendon with the bone
chip was attached to a hydraulic muscle puller (MTS,
Eden Prairie, Minnesota, USA) which measured the
force and could be programmed to induce the required
length changes to the muscle. Control of the length and
speed of shortening of the muscle was accomplished
using TestWare SX. This is the proprietary software
package supplied by MTS for the control of the
hydraulic servo-actuator. Individual procedures were
designed to operate inside this software shell but would
output in real time, the LVDT displacement signal,
the load cell force signal and a synchronization pulse.
The synchronization pulse initiated the onset of nerve
activation and the pre-selected stimulation parameters
were then executed. Muscle temperature was monitored
and radiant heat applied to maintain a constant muscle
temperature of 31–33 1C. All experiments were approved
by the animal ethics review committee of the University
of Calgary.
2.2. Muscle stimulation and data collection
The nerve stimulating electrode was connected to a
Grass S8800 stimulator (Grass-Telefactor, West War-
wick, RI, USA) where the stimulation parameters could
be precisely controlled. Stimulation parameters such as
pulse duration, stimulus train duration, inter-pulse
interval and voltage were adjusted directly on the
stimulator and not controlled by software. The onset
of the stimulation was triggered by the synchronization
signal sent from the muscle puller computer. The
a-motor unit threshold was determined and all stimula-
tions were preformed at three times this threshold to
ensure full activation of the muscle (Herzog and
 ARTICLE IN PRESS
T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197
Leonard, 1997). Pulse duration was set at 0.1 ms. All
isometric reference contractions and all isometric
components of the force depression experiments were
performed at 30 Hz; only the muscle shortening phase of
the force depression experiments was subject to varia-
tions in stimulation frequency (see below—experimental
protocol). All data were collected at 1000 Hz on a
computer running real-time display and storage hard-
ware and software (Dataq Instruments, Akron, OH,
USA). This dedicated data display and collection system
emulates a scrolling chart recorder and so we were able
to determine whether a test had been successful
immediately after a contraction had finished. No
filtering or smoothing of the data was performed
2.3. Preliminary tests
All experiments were performed on the descending
limb of the force–length relationship to maximize the
amount of force depression (Schachar et al., 2004). The
force–length relationship for the muscle was determined
using 3 s isometric contractions at different muscle
lengths. Contractions were performed for 2 mm incre-
ments at lengths ranging from active insufficiency (i.e.,
the muscle was so short that it could not produce active
force) to a length where the active force (total minus
passive force) was clearly and consistently decreasing. A
zero reference length was defined as the longest muscle
length on the plateau region (Gordon et al., 1966).
Therefore, all lengths less than the zero reference length
were considered to be on the plateau or ascending limb,
and all lengths above the reference length were
considered on the descending limb of the force–length
relationship (e.g., Morgan et al., 2000). All experiments
for this study were performed on the descending limb of
the force–length relationship; that is, at lengths greater
than the zero reference length. A 45 s interval was
provided between contractions to prevent fatigue of the
soleus in accordance with previous experience (Herzog
and Leonard, 1997).
2.4. Test protocol
Two basic test protocols were performed. The first
protocol was aimed at verifying that force depression
changed with changing speeds of shortening if the
magnitude of shortening and activation were kept
constant. All tests consisted of active shortening of the
soleus on the descending limb of the force–length
relationship by either 9 or 12 mm. Large force depres-
sion values with respect to the isometric reference were
desirable and three muscles required a shortening of
12 mm to produce a useful amount of force depression
while the remaining four required only 9 mm of short-
ening. Regardless of whether the shortening was 9 or
12 mm, all tests were conducted with a stimulation
2193
Fig. 4. (a) Schematic representation of the shortening protocol used in
this study. Soleus was always shortened by 9 or 12 mm at speeds of 3, 9
and 27 mm/s. (b) Schematic representation of the reduced muscle
activation used during the shortening phase of test contractions.
Slower shortening (3 mm/s) produced more force during shortening
and so was subjected to lower frequencies of stimulation than faster
shortening tests (9 and 27 mm/s). The tests at the fastest speed of
shortening (27 mm/s) were always performed at a stimulation
frequency of 30 Hz during shortening, those at 9 mm/s were performed
at about 10–18 Hz, and those at 3 mm/s at 5–12 Hz (for matching
27 mm/s) and 8–12 Hz (for matching 9 mm/s).
frequency of 30 Hz. The three speeds of shortening used
were 3, 9 and 27 mm/s.
The second protocol was identical to the first, except
that the activation during the shortening phase only was
decreased for decreasing speeds of shortening. Decreases
in activation were achieved by changing the stimulation
frequency in such a way that the resulting steady-state
force depression at the different speeds would be
identical. This typically took 3–4 trials before the right
stimulation frequency was identified (Fig. 4).
All experimental shortening tests were immediately
preceded and followed by an isometric reference
contraction at the length corresponding to the final
length of shortening; that means force depression was
determined for steady-state isometric contractions at
identical muscle lengths.
2.5. Data analysis
For the first protocol, force depression was calculated
as the difference in force between the isometric reference
contraction and the corresponding shortening test
contraction at 5.5 s following the end of shortening
(Fig. 5).
For the second protocol, only experimental tests at
different shortening speeds whose force depression was
 ARTICLE IN PRESS
2194 T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197
Fig. 5. Example of force time histories for an isometric reference
contraction (r) and three isometric-shortening-isometric test contrac-
tions performed at speeds of shortening of 3 mm/s (3), 9 mm/s (9) and
27 mm/s (27). Force depression increases with slower speeds of
shortening and increasing force during shortening. The larger forces
during slow shortening are attributed to the force–velocity relation-
ship. Activation in all trials was at a frequency of stimulation of 30 Hz
and all shortening was over a distance of 9 mm.
the same (i.e. within 0.2 N) were used for analysis. These
matched pairs were then used to calculate the work
performed during the shortening phase by integrating
the force-shortening part of the test contractions
(Herzog et al., 2000). As a single measure of the force
of shortening, the minimum force at the end of the
shortening phase was also used for the matched pair
analysis.
Statistical analysis was performed using the Wilcoxon
signed rank test (Stata software, Stata Corp., College
Station, TX, USA) to test for differences between the
force depressions of matched trials to determine whether
the trials were truly matched. The sign test was used to
test for differences in force or work performed for
the matched test trials, that is, all trials for which
the speed of shortening was different but force depres-
sion was the same. The null hypothesis was that the
speed of shortening does not influence force depression.
In other words, it was expected that for the matched
pair trials, the minimum force during shortening and
the work performed during shortening were the same.
All statistical analyses were performed at a level of
significance of a ¼ 0:05:
Table 1
Mean force depression as a percentage of the isometric reference force
for trials at three speeds of shortening; 3, 9 and 27 mm/s
Force depression (%)
3 mm/s 9 mm/s 27 mm/s
Mean 7.1 5.4 3.8
Standard deviation 2.0 1.3 0.8
Activation during shortening was the same for all trials (30 Hz), and
the magnitude of shortening was the same for a given muscle (either 9
or 12 mm). Force depression decreases with increasing speeds of
shortening (po0:05) for these experimental conditions in agreement
with published findings.
3. Results
3.1. First test protocol
When the cat soleus was shortened by a given amount
(9 or 12 mm) and a given activation (30 Hz), but at
different speeds (3, 9, and 27 mm/s), and therefore
different forces (Hill, 1938), force depression increased
with decreasing speeds of shortening, or equivalently
with increasing forces during the shortening phase
(Fig. 5, Table 1). These results confirm previous findings
published in the literature (Abbott and Aubert, 1952;
Maréchal and Plaghki, 1979; Sugi and Tsuchiya, 1988;
Meijer et al., 1997; Herzog and Leonard, 1997; Morgan
et al., 2000; De Ruiter et al., 2000; Lee and Herzog,
2003).
3.2. Second test protocol
In the seven muscles, 26 matched pair tests were
found for which the steady-state force depression
was the same (i.e. within 0.2 N—Fig. 6) for two different
speeds of shortening. A total of 74 trials where
the stimulation frequency was manipulated were per-
formed to obtain the 26 successfully matched pairs.
Twenty-six matched pair tests were deemed sufficient
to proceed with further data analysis due to the
high quality of the data traces obtained. Statistical
analysis revealed that force depression in the slow and
fast speed trials was the same (p ¼ 0:708), that means
there was no consistent bias towards any of the
experimental speeds.
However, the minimum force during shortening and
the work performed during shortening was always
greater in the slow compared to the fast speed for each
matched pair (po0:05; Figs. 6 and 7). Therefore, the
null hypothesis that force and work during shortening
would be the same for tests with the same steady-state
force depression was rejected.
 ARTICLE IN PRESS
T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197 2195

4. Discussion Aubert, 1952; Maréchal and Plaghki, 1979; Sugi and

The steady-state force depression observed following
active shortening of skeletal muscles has been thought to
directly depend on the speed of shortening (Abbott and
Fig. 6. Example of force time histories of an isometric reference
contraction (r) and two isometric-shortening-isometric test trials
performed at a speed of shortening of 3 mm/s (3) and 9 mm/s (9).
Note that force depression is the same for both test trials (FD3=FD9)
but the minimum force at the slow shortening speed, F3, was greater
than that for the fast shortening speed, F9. The shortening magnitude
was 9 mm and the shortening phases of each contraction were
performed at stimulation frequencies of 10 and 12.5 Hz for the 3 and
9 mm/s shortening speeds, respectively.
Tsuchiya, 1988; Meijer et al., 1997; Herzog and
Leonard, 1997; Morgan et al., 2000; De Ruiter et al.,
2000; Lee and Herzog, 2003). However, when it was
discovered that force depression is strongly influenced
by the force and work during shortening (Herzog and
Leonard, 1997; Herzog et al., 2000), the effect of speed
on force depression was not clear anymore, as speed and
force are intimately related through the force–velocity
relationship (Hill, 1938). Here, we were successful in
performing experiments in which speed was system-
atically varied, while simultaneously, force was adjusted
to match the steady-state force depression. The basic
premise for these sets of experiments was that if force
depression was only speed dependent then it should not
be possible to change the speed of shortening and obtain
identical force depression values. Conversely, if force
depression was not dependent on speed, but just on
force, then it should be possible to match force
depression at different speeds by adjusting the force
through appropriate changes in the activation levels
(frequency of stimulation).
Here, we demonstrate for the first time that the same
force depression can be achieved for different speeds of
shortening, if force is adjusted in the appropriate way
(Fig. 6). In contrast to this result, we showed in a
previous study that it was impossible to obtain the same
force depression for a given magnitude and speed of
shortening when force was altered (Herzog and Leo-
nard, 1997). Therefore, we conclude from the results of
this and our previous study that force depression does
not depend on the speed of shortening, or if it does, the
effect is very small compared to that of the force during
shortening, and thus, can be easily compensated for.
If force depression only depended on the magnitude
and force of shortening, and not the speed, one would
expect that the force profiles during shortening for the
matched pair trials should have been the same. In order

Fig. 7. Box and whisker plot showing median, 25th percentile and 75th percentile values for parameter differences for all force depression matched
pairs (n ¼ 26). Differences were calculated as follows: test parameter (force depression (a) or minimum force (b) or work performed (c)) for the slow
speed of shortening minus the test parameter for the faster speed of shortening. Note that the median difference in force depression for the matched
pairs (a) is close to zero and the whiskers extend into both positive and negative zones. Differences for both work production (b) and minimum force
(c) were positive for all 26 independent observations.
 ARTICLE IN PRESS
2196 T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197
to evaluate this expectation, we quantified the minimum
force at the end of the shortening phase as a single force
indicator, and also determined the work performed by
soleus during shortening as a global indicator of the
force profile. We found that the minimum force during
shortening, as well as the work performed was always
greater in the matched pair trials for the slow compared
to the fast speed (i.e. always greater for 3 mm/s
compared to 9 or 27 mm/s, and always greater for 9
compared to 27 mm/s; Fig. 7). Therefore, aside from the
force during shortening, it appears that another factor
plays a role in force depression, albeit a small one. The
present experiment was not designed to determine the
origin of this other effect. However, we would like to
tentatively suggest that it is associated with the amount
of activation and not the speed of shortening. We
eliminate the speed of shortening as a candidate because
there is a very tight relationship between the work
performed by a muscle and the amount of force
depression for tests at different speeds but constant
activation (Herzog et al., 2000). This relationship does
not hold here at all as the same force depression is
achieved for vastly different amounts of mechanical
work (Fig. 7). Thus, activation seems to be the prime
candidate for these observations. In order to obtain the
same amount of force depression in a slow compared to
a fast shortening trial, force had to be decreased which
was achieved by decreasing the activation to the muscle.
The level of activation and therefore force during the
shortening contraction influences the amount of force
depression after the contraction.
The findings of this study maybe useful in the search
for the as yet unknown mechanisms causing force
depression. Maréchal and Plaghki (1979) suggested that
force depression might be caused by a stress-induced
inhibition of cross-bridge attachments in the overlap
zone that is formed between actin and myosin filaments
as the muscle shortens. Herzog (1998) refined this idea
by speculating that the compliant actin filaments
(Amemiya et al., 1988; Goldman and Huxley, 1994;
Kojima et al., 1994; Wakabayashi et al., 1994) might be
stretched in the isometric contraction prior to short-
ening, and that this stretching would cause a reorienta-
tion of the actin attachment sites (Daniel et al., 1998)
which in turn would decrease the probability of cross-
bridge attachments. This theory would require that force
depression is dependent on the force and work
performed in the shortening phase and is independent
of the speed of shortening. The results of this study
support this particular theory.
5. Conclusion
In this study, we showed for the first time that the
steady-state force depression following shortening of an
active muscle can be the same for different speeds of
shortening if force is adjusted appropriately. These
results strongly suggest that force depression does not
depend on the speed of shortening as stated throughout
the literature of the past 50 years, but that force
depression depends directly on the force during short-
ening, and that the association with speed is merely an
artifact of the force–velocity relationship which causes
changes in force during the shortening phase when
experiments are performed at different speeds of short-
ening (Hill, 1938). Therefore, in the search for mechan-
isms, force should be considered whereas speed does not
appear to have an effect on force depression.
Acknowledgements
Funding for this project was provided by the Natural
Sciences and Engineering Research Council of Canada
(NSERC).
References
Abbott, B.C., Aubert, X.M., 1952. The force exerted by active striated
muscle during and after change of length. Journal of Physiology
117, 77–86.
Amemiya, Y., Iwamoto, H., Kobayashi, T., Sugi, H., Tanaka, H.,
Wakabayashi, K., 1988. Time-resolved X-ray diffraction studies on
the effect of slow length changes on tetanized frog skeletal muscle.
Journal of Physiology 407, 231–241.
Daniel, T.L., Trimble, A.C., Chase, P.B., 1998. Compliant realignment
of binding sites in muscle: transient behaviour and mechanical
tuning. Biophysical Journal 74, 1611–1621.
De Ruiter, C.J., Didden, W.J.M., Jones, D.A., de Haan, A., 2000. The
force–velocity relationship of human adductor pollicis muscle
during stretch and the effects of fatigue. Journal of Physiology
526.3, 671–681.
Goldman, Y.E., Huxley, A.F., 1994. Actin compliance: are you pulling
my chain? Biophysical Journal 67, 2131–2136.
Gordon, A.M., Huxley, A.F., Julian, F.J., 1966. The variation in
isometric tension with sarcomere length in vertebrate muscle fibres.
Journal of Physiology 184, 170–192.
Herzog, W., 1998. History dependence of force production in skeletal
muscle: a proposal for mechanisms. Journal of Electromyography
and Kinesiology 8, 111–117.
Herzog, W., Leonard, T.R., 1997. Depression of cat soleus forces
following isokinetic shortening. Journal of Biomechanics 30 (9),
865–872.
Herzog, W., Leonard, T.R., Wu, J.Z., 1998. Force depression
following skeletal muscle shortening is long lasting. Journal of
Biomechanics 31, 1163–1168.
Herzog, W., Leonard, T.R., Wu, J.Z., 2000. The relationship between
force depression following shortening and mechanical work in
skeletal muscle. Journal of Biomechanics 33, 659–668.
Hill, A.V., 1938. The heat of shortening and the dynamic constants of
muscle. Proceedings of the Royal Society of London 126, 136–195.
Josephson, R.K., Stokes, D.R., 1999. Work-dependent deactivation of
a crustacean muscle. Journal of Experimental Biology 202 (18),
2551–2565.
Kojima, H., Ishijima, A., Yanagida, T., 1994. Direct measurement of
stiffness of single actin filaments with and without tropomyosin by
 ARTICLE IN PRESS
T.R. Leonard, W. Herzog / Journal of Biomechanics 38 (2005) 2190–2197 2197

in vitro nanomanipulation. Proceedings of the National Academy
of Science USA 91, 12,962–12,966.
Lee, H.D., Herzog, W., 2003. Force depression following muscle
shortening of voluntarily activated and electricallystimulated
human adductor pollicis. Journal of Physiology 551, 993–1003.
Maréchal, G., Plaghki, L., 1979. The deficit of the isometric tetanic
tension redeveloped after a release of frog muscle at a constant
velocity. Journal of General Physiology 73, 453–467.
Meijer, K., Grootenboer, H.J., Koopman, B.F.J.M., Huijing, P., 1997.
Fully isometric length–force curves of rat muscle differ from those
during and after concentric contractions. Journal of Applied
Biomechanics 13, 164–181.
Meijer, K., Grootenboer, H.J., Koopman, B.F.J.M., van der Linden,
B.J.J.J., Huijing, P., 1998. A Hill type model of rat medial
gastrocnemius muscle that accounts for shortening history effects.
Journal of Biomechanics 31, 555–563.
Morgan, D.L., Whitehead, N.P., Wise, A.K., Gregory, J.E., Proske,
U., 2000. Tension changes in the cat soleus muscle following slow
stretch or shortening of the contracting muscle. Journal of
Physiology 522.3, 503–513.
Schachar, R., Herzog, W., Leonard, T.R., 2004. The effects of muscle
stretching and shortening on isometric forces on the descending
limb of the force–length relationship. Journal of Biomechanics 37
(6), 917–926.
Sugi, H., Tsuchiya, T., 1988. Stiffness changes during enhance-
ment and deficit of isometric force by slow length changes
in frog skeletal muscle fibres. Journal of Physiology 407,
215–229.
Wakabayashi, K., Sugimoto, Y., Tanaka, H., Ueno, Y., Takezawa, Y.,
Amemiya, Y., 1994. X-ray diffraction evidence for the extensibility
of actin and myosin filaments during muscle contraction.
Biophysical Journal 67, 2422–2435.