Journal of Electromyography and Kinesiology 12 (2002) 471–477

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Force enhancement following an active stretch in skeletal muscle

Dilson E. Rassier, Walter Herzog ∗
Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, 2500 University Drive, Calgary (AB), Canada T2N 1N4

Abstract

When skeletal muscle is stretched during a tetanic contraction, the resulting force is greater than the purely isometric force
obtained at the corresponding final length. Several mechanisms have been proposed to explain this phenomenon, but the most
accepted mechanism is the sarcomere length non-uniformity theory. This theory is associated with the notion of instability of
sarcomeres on the descending limb of the force–length relationship. However, recent evidence suggests that this theory cannot
account solely for the stretch-induced force enhancement. Some of this evidence is presented in this paper, and a new mechanism
for force enhancement is proposed: one that is associated with the engagement of a passive force during stretch. We speculate that
this passive force enhancement may be caused by titin, a protein associated with passive force production at long sarcomere lengths.
 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Active force; Passive force; Sarcomeres; Stability; Force-length relation; Titin

1. Introduction

It has been known for a long time that when skeletal

muscle is stretched during a tetanic contraction, the force
following the stretch is greater than the purely isometric
force obtained at the corresponding final length [1,2].
This phenomenon has been observed in single muscle
cells [3–7], whole muscles [8,9], and human muscles
that are electrically stimulated [10] or contracted volun-
tarily [11].
The force enhancement observed after active stretch
cannot be readily explained by the original cross-bridge
theory of muscle contraction, as the theory does not
incorporate history-dependent effects of force production
[12,13]. Also, it cannot be predicted by the degree of
thick and thin filament overlap [14], as isometric force
following stretch at a small average overlap between
myofilaments might be greater than the isometric force
at a great average myofilament overlap (Fig. 1) [5].
Therefore, much research has focused on the pursuit of
understanding the mechanisms of the stretch-induced
force enhancement.
Several mechanisms have been proposed to explain
∗
Corresponding author. Tel.: +1-403-220-8525; fax: +1-403-284-
3553.
E-mail address: walter@kin.ucalgary.ca (W. Herzog).
Fig. 1. Schematic representation of the isometric force–length
relationship, and force enhancement after an active stretch. During iso-
metric contractions, force follows the lines in the graph according to
the degree of length in which the contraction starts and the degree of
filament overlap. However, if the muscle is actively stretched during
a contraction, e.g. from the initial to the final length (䊊), the force
produced (쎲) is higher than the purely isometric force produced at the
final length. Therefore, the degree of filament overlap is reduced, but
the force is increased.
the stretch-induced force enhancement, including cross-
bridge kinetics [15], lattice spacing changes with reor-
dering of thick and thin filaments [16], non-uniformity
and instability of sarcomeres [17,18] associated with the
engagement of parallel passive elements [6], and the role
of titin and nebulin as additional force producers [6,19].
While some of these mechanisms have not been care-
fully tested, the hypothesis that incorporates non-uni-

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PII: S 1 0 5 0 - 6 4 1 1 ( 0 2 ) 0 0 0 4 1 - X
472 D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477

formity of length and instability of sarcomeres

[17,18,20] has been the most accepted theory. However,
some characteristics of force enhancement following
stretch, together with new experimental findings, suggest
that the mechanisms of force enhancement may involve
components other than non-uniformity of sarcomere
length.
The main purpose of this paper is to review the gen-
eral characteristics of stretch-induced force enhance-
ment, to critically evaluate proposed mechanisms of
force enhancement, including the sarcomere length non-
uniformity theory, and to present evidence for an alterna-
tive mechanism that may explain part of the stretch-
induced force enhancement. It is expected that this
review will motivate new studies on the mechanisms
responsible for the stretch-induced force enhancement
observed in skeletal muscle.

2. Characteristics of force enhancement after

stretch
The basic features of force enhancement observed
after stretch are shown in Fig. 2. The muscle is first tet-
anized at a given sarcomere/muscle length, and after the
muscle reaches maximal isometric force, it is stretched
to a new length. The force produced at this new length
is greater than the purely isometric force at the corre-
sponding muscle length. Therefore, two contractions at
the same muscle (fiber, average sarcomere) length result
in different force, depending on whether the muscle was
actively stretched during contraction, or not (Fig. 1).
Force enhancement has two components: (1) a sudden
increase in force that is observed during the stretch and
that dissipates gradually after the stretch is finished; and
(2) a stable residual increase in force that remains con-
stant until the end of the contraction [5,6]. This second
component will be called force enhancement after stretch
[15]. The first component of force enhancement is well
understood, and is related to the negative part of the
force–velocity relationship [21]; that is, force increases
with higher speeds of stretch (Fig. 2B) [4,20]. This
component has been explained by an increased number
of attached cross-bridges during the stretch [7], and by
an increased strain of cross-bridges when sarcomeres are
forcibly extended during a tetanic contraction [22].
Therefore, force enhancement during stretch has been
associated with regular cross-bridge properties, as
described in the cross-bridge theory [12].
Force enhancement after stretch has characteristics
that seem unrelated to cross-bridge properties. Most
notably, the force is enhanced (compared to the purely
isometric force and compared to the force predicted by
the average overlap of filaments) during the entire period
during which the fiber is activated. In this paper, we will
concentrate on the characteristics and proposed mech-
anisms of the residual force enhancement after stretch.
Fig. 2. Stretch-induced force enhancement observed during a typical
experiment performed with a single muscle fiber from the frog on the
descending limb of the force–length relationship. (A) shows contrac-
tions in which the fiber was stretched 5, 10 and 15% from an initial
length (Li) on the descending limb of the force–length relationship, at
a speed of 0.8 mm/s. It also shows an isometric contraction (Lf) perfor-
med at a length 15% greater than Li. (B) shows contractions in which
the fiber was stretched 15% from Li on the descending limb of the
force–length relationship, at speeds of 0.4, 0.8 and 2.0 mm/s, and an
isometric contraction (Lf) performed at a length 15% greater than Li.
Force enhancement increases with the amplitude of stretch but is inde-
pendent of the speed of stretch.
The enhanced force observed after stretch is stable at
苲4.5 s following the length change [5,6]. The amount of
force enhancement depends on the amplitude of stretch
(Fig. 2A), but is independent (or at least nearly so) of the
speed of stretch (Fig. 2B). Increasing stretch amplitude
results in greater force enhancement [1,4,5,23]. Excep-
tions to these findings are the studies by Julian and Mor-
gan [20] and Morgan et al. [9], in which the level of
force enhancement was interpreted to be independent of
the amplitude of stretch.
The degree of force enhancement after stretch depends
on the initial sarcomere length from which the muscle
is stretched. It has been shown that, along the descending
limb of the force–length relationship, force enhancement
is increased when the muscle fiber is stretched from
greater muscle lengths [5]. Most studies on force
enhancement were performed on the descending limb of
the force–length relationship, and it has been suggested
 D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477
that force enhancement is observed only in this region
[4,5,20]. However, little effort has been made to evaluate
force enhancement on the ascending limb of the force–
length relationship. Recent studies show steady-state
force enhancement following active muscle stretch on
the ascending limb of the force–length relationship (later
in this paper).
Using whole cat soleus, Herzog and Leonard [24]
observed that muscle shortening that immediately pre-
ceded stretching affected the amount of force enhance-
ment. More precisely, they observed that for a given
stretch (speed, amplitude), force enhancement was
decreased in a dose-dependent manner with the amount
of shortening preceding the stretch. However, in experi-
ments with single cells from the frog, Edman et al. [5]
found that force enhancement was not affected by short-
ening that preceded stretching, when a brief pause was
given between the length changes. This difference
between the two studies is conspicuous, and it may be
caused by the preparations (whole muscle vs single
cells), or by the protocols (with and without pauses
between shortening and stretching phases). Julian and
Morgan [20] showed that an interruption of the contrac-
tion introduced after the stretch changes the enhanced
force in a time-dependent manner, such that a short inter-
ruption does not abolish force enhancement, but a long
interruption eliminates all force enhancement. Future
research is needed to better understand how force
enhancement is affected by shortening preceding the
stretching phase.
An important feature of force enhancement after
stretch that still needs to be carefully investigated is its
association (or not) with an increased stiffness, as con-
tradictory results exist in the literature. Assuming that
stiffness is directly related to the number of cross-
bridges attached to actin [25,26], an increased stiffness
in the force-enhanced state could be related to a higher
number of attached cross-bridges after stretch. Sugi and
Tsuchiya [23] performed a series of experiments in
which they measured fiber stiffness by applying sinus-
oidal vibrations to the cells during isometric contractions
and stretch contractions. It was observed that, although
the force was increased (as expected) after the stretch,
the stiffness was the same as observed during isometric
contractions produced at that final length. However, Lin-
ari et al. [7] observed an increased stiffness in single
muscle cells just after stretch, which was directly asso-
ciated with an increased force enhancement. It should be
cautioned that in their experiments force never reached
a steady-state condition, as contractions were very short
(1–3 s). In order to evaluate their results critically in
terms of steady-state force enhancement, experiments
with longer contraction times should be performed.
473
3. Mechanisms of force enhancement after stretch
Force enhancement after stretch has been related to
an increased number of attached cross-bridges, to
changes in the cross-bridge dynamics, or to some non-
cross-bridge sarcomeric properties. A mechanism asso-
ciated with the cross-bridge dynamics would have to
assume an increased average force per attached cross-
bridge [15]. A mechanism associated with non-cross-
bridge properties may be associated with sarcomere
mechanics and/or the involvement of sarcomeric pro-
teins, independent of the proportion of attached cross-
bridges.
A hypothesis related to the cross-bridge dynamics was
introduced by Amemiya et al. [16]. These authors used
X-ray diffraction to measure filament position after
stretch, and observed a disordering of the myofilament
lattice without significant changes in the mean inter-
filament spacing. This disordering was characterized as
a displacement of the thin filaments from their initial
position to a position closer to the thick filaments. This
arrangement persisted while the muscle was stimulated.
Such a decrease in lattice spacing could enhance the
probability of cross-bridge attachment, and consequently
force generation.
Although it is difficult to directly evaluate the mech-
anism proposed by Amemya et al. [16], a similar result
is observed when a twitch contraction is potentiated by
phosphorylation of the myosin regulatory light chains.
In this case, myosin phosphorylation moves the cross-
bridges towards the thin filament [27]. This approxi-
mation of the cross-bridge heads to potential actin
attachment sites is believed to increase the probability
of myosin/actin interactions, and consequently force
generation at a given sub-maximal Ca2+ concentration
[28]. Due to the difficulty of testing cross-bridge hypoth-
eses experimentally, they should be considered in theor-
etical models, in which force production can be simu-
lated using cross-bridges with different rates of
attachment/detachment before and after stretch.
Another possibility is that the level of phosphorylation
of the regulatory light chains is enhanced during stretch,
as suggested by Edman [3]. Since the rate constant for
dephosphorylation of the light chains is very slow, myo-
sin would remain phosphorylated after muscle stretch-
ing, and could produce the long lasting force enhance-
ment following stretching. However, there is no evidence
that an active stretch enhances the biochemical steps
involved in myosin light chain phosphorylation, (e.g.
enhancement of the myosin light chain kinase activity),
but this hypothesis should be tested in the near future.
4. The theory of sarcomere length non-uniformity
The mechanism of force enhancement after stretch
that has received more attention in the scientific com-
474 D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477
munity than any other mechanism is the sarcomere
length non-uniformity theory [20]. This idea has been
used by several researchers [6,9] and was ultimately
associated with the ‘popping sarcomeres’ theory [18].
The first experimental observation related to the sarco-
mere length non-uniformity theory was made by Julian
and Morgan [20]. They observed that during stretch of
single cells, sarcomere lengths did not change by the
same amount: sarcomeres near the center of the cells
stretched more than average, while sarcomeres near the
end of the cell stretched less than average. Julian and
Morgan [20] suggested that this non-uniformity of sarco-
mere lengths was responsible for the force enhancement
after stretch. However, in a subsequent study, Edman et
al. [5] observed that force enhancement was not only
produced by muscle fibers as a whole, but also by indi-
vidual clamped segments of the fiber, and by isolated
sarcomere populations. Edman et al. [5] concluded that
force enhancement was possible, independently of the
development of sarcomere length non-uniformity.
Morgan [18] incorporated observations of sarcomere
length non-uniformity [20] and sarcomere instability on
the descending limb of the force–length relationship [17]
to provide an explanation for the force enhancement
after stretch. Morgan [18] argued that when fibers are
actively stretched on the descending limb of the force–
length relationship, sarcomeres located near the center
of the fiber are stretched more than sarcomeres near the
end of the fiber. As the stretch continues, these sarcom-
eres are stretched until actin–myosin overlap is lost (i.e.
they ‘pop’). Sarcomeres located near the end of the fibers
do not stretch as much, and may in fact stay almost iso-
metric during the elongation of the cell. These sarcom-
eres produce the active force in the fiber. The ‘popped’
sarcomeres are supported by the passive tension present
on the descending limb of the force–length relationship.
The two groups of sarcomeres need to have equal force
to attain equilibrium. At equilibrium, the force produced
by the two groups of sarcomeres is greater than the iso-
metric force at the corresponding length, which is
assumed to have a relatively uniform (average) sarco-
mere length distribution. The sarcomere length non-uni-
formity theory can explain some experimentally
observed features of force enhancement after stretch.
5. Instability and non-uniformity of sarcomeres
Naturally, the theory of ‘popping’ sarcomeres is based
on the notion of an inherent instability of sarcomere
lengths that is present on the descending limb of the
force–length relationship [17,20]. Instability would be
responsible for the non-uniform length changes in sar-
comeres, which in turn causes sarcomere dispersion and
heterogeneity in sarcomere lengths during contractions.
The notion of instability was first introduced by Hill
[29], who suggested that sarcomeres were unstable on
the descending limb because of the negative slope of the
force–length relationship in that region. However, the
force–length relationship is obtained by isolated contrac-
tions at different lengths, e.g. Gordon et al. [14], and it
is not necessarily correct to infer dynamic instability
from a static observation. In fact, it is quite easy to
design systems in which the static force decreases while
the dynamic force increases with increasing length
[30,31].
Several researchers suggested that sarcomere lengths
are stable during contractions over the whole physiologi-
cal range of lengths, including the descending limb of
the force–length relationship [30,32–34]. It has been
shown that force following stretch is, in some situations,
not only greater than the isometric force obtained at the
final length (as discussed previously), but also greater
than the force recorded at the initial length from which
the muscle was stretched [4,5]. This force enhancement
above the initial isometric force can be observed after
the force reaches a steady-state following stretch [35,36].
In this case, the dynamic force–length trace has a posi-
tive slope that is characteristic of a stable system that
exhibits hardening properties. This idea agrees with
observations that a fiber that is stretched on the
descending limb of the force–length relationship has a
positive stiffness during the stretch [37,38]. Along those
lines, Allinger et al. [39] showed that the dispersion of
sarcomere length decreases during a tetanic contraction,
which is a property of a stable system.
Therefore, sarcomere lengths may be stable on the
descending limb of the force–length relationship, thereby
questioning the origin of the popping sarcomere and the
sarcomere length non-uniformity theories. Although it is
difficult to directly evaluate the sarcomere length non-
uniformity theory experimentally, its well-defined math-
ematical framework allows for the derivation of testable
hypotheses. If the sarcomere length non-uniformity
theory is the sole mechanism responsible for the steady-
state force enhancement after stretch, and if sarcomeres
behave as proposed by Morgan [18], then the following
should be true: (1) force enhancement after stretch
should not be observed on the ascending limb of the
force–length relationship, as this region is not associated
with instability of sarcomeres and the development of
sarcomere length non-uniformities; and (2) force follow-
ing stretch should never exceed the isometric force pro-
duced on the plateau of the force–length relationship.
We performed experiments with the cat soleus and with
single cells dissected from the frog, in which we tested
the above hypotheses.
Using single muscle cells dissected from the frog
(Rana pipiens) we observed that, on the ascending limb
of the force–length relationship, the steady-state force
following stretch was greater than the purely isometric
force produced at the final length. The amount of force
 D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477
enhancement was generally smaller on the ascending
compared to the descending limb of the force–length
relationship. The same observation was made in the in
situ cat soleus. In these experiments, soleus was stimu-
lated at 5 and 30 Hz, and we observed a small but con-
sistent force enhancement on the ascending limb of the
force–length relation [8]. Force enhancement on the
ascending limb of the force–length relationship was also
reported by De Ruiter et al. [10] in human adductor pol-
licis muscle.
Other investigators, using single cells from frog or
whole muscles from the cat, failed to find force enhance-
ment on the ascending limb of the force–length relation-
ship [6,9,20]. They may have used amplitudes of stretch
that were too short to observe a measurable force
enhancement.
In another series of experiments performed with single
muscle cells from frogs, we were interested in determin-
ing if force enhancement could be observed at levels
above the isometric force produced on the plateau of the
force–length relationship. Our interest was based on pre-
viously reported results. Edman et al. [5] (their Fig. 3),
showed force enhancement of about 1–2% greater than
the isometric force produced at the plateau of the force–
length relationship. The authors credited the results to
measurement error, and did not persist to evaluate their
finding. Results from one experiment from our study are
shown in Fig. 3. In this case, force following stretch
exceeded the isometric force produced at the initial
length, showing stable properties as explained above.
Even more important for the present discussion, force
after stretch also exceeded the isometric force produced
at the plateau of the force–length relationship. This result
was statistically confirmed in more than 30 separate
experiments. In some cases, force was 苲10% higher than
Fig. 3. Active and passive force enhancement observed during a typical experiment performed with a single muscle fiber from the frog on the
descending limb of the force–length relationship. After stretch, active force is higher than the isometric force recorded at the initial length (Li),
and is also higher than the isometric force recorded at the plateau (Lo) of the force–length relation. The passive force is greater when the stretch
is performed during contraction than when the muscle is stretched passively.
475
the maximal isometric force on the plateau of the force–
length relationship. An unstable system, or a theory
based on the sarcomere length non-uniformity idea
alone, cannot explain this result. If some sarcomeres
‘pop’ during stretch, and others are maintained isometric
(or stretch only by a small amount) during the stretch of
the whole fiber, force cannot exceed the maximal iso-
metric force produced at the plateau of the force–
length relationship.
6. Alternative mechanism of force enhancement
after stretch
Since the sarcomere length non-uniformity and the
popping sarcomere theory cannot account for the force
enhancement above the plateau forces, other mech-
anisms should be considered. An alternative, or
additional, mechanism of force enhancement after
stretch should incorporate all the characteristics
observed in the experiments described, and should
assume that the muscular system is stable under contrac-
tion.
One possibility that has been often mentioned in the
literature but has not received direct experimental sup-
port is the idea that a passive elastic element is engaged
during an active stretch [6,19]. Edman and Tsuchiya [6]
performed a series of experiments in which single mus-
cle fibers were released to shorten against a small load
at different times after a stretch, and also after tetanic
contractions. The force transients of the contractions in
which a stretch was applied exhibited a greater and
steeper decrease in force than those obtained during an
isometric contraction. These findings were interpreted as
resulting from the elongation of a passive elastic struc-
476 D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477
ture. The authors suggested that some half-sarcomeres
would stretch more than others during the elongation,
and these overstretched regions of the sarcomere would
be supported by the engagement of an elastic, passive
structure.
Alternatively, the engagement of a passive element
could be directly responsible for the increase in force.
Although this possibility has not been directly tested,
it has been observed that under some conditions, force
enhancement is accompanied by an increase in the pass-
ive force (Fig. 3) [8]. This increase in passive force pro-
duced by stretching an active muscle is not observed
when the muscle is passively stretched (Fig. 3). We refer
to this phenomenon as ‘passive force enhancement’. The
passive force enhancement appears to persist for as long
as the muscle is not shortened, and we speculate that the
passive force enhancement may account for part of the
total force enhancement observed after stretch. Such a
hypothesis has been shown to work in theory in a rheol-
ogical muscle model that incorporated a passive compo-
nent to explain the steady-state force enhancement after
stretch [40].
The origin of this passive force enhancement is
unknown, but based on the structure of the sarcomeres
and the origin of passive force during a non-activated
stretch, the protein titin seems a prime candidate. Titin
connects thick filaments to the Z-line, and titin is respon-
sible for passive force in skeletal and cardiac muscles
when stretched to a great length [41,42]. If, upon acti-
vation, the increased level of myoplasmic Ca2+ somehow
increases the stiffness of titin, either by binding to the
protein or by changing the biochemical environment in
the myoplasm, then the passive force in titin would be
increased compared to a non-activated stretch.
7. Conclusions
Force enhancement after stretch has been observed in
a variety of skeletal muscle preparations, ranging from
single muscle cells to human muscles during voluntary
contractions. Although the sarcomere length non-uni-
formity theory has been used primarily to explain the
steady-state force enhancement, the theory is based on
the notion of instability of sarcomeres on the descending
limb of the force–length relationship. However, there is
evidence that skeletal muscle is stable on the descending
limb of the force–length relationship. Furthermore, force
enhancement has been observed by different research
groups on the ascending limb of the force–length
relationship. Finally, we have presented experimental
data showing force enhancement above plateau forces in
cat soleus and single fibers from the frog. Together with
the demonstration of a persistent passive force enhance-
ment following active stretch, we must conclude that the
sarcomere length non-uniformity theory cannot be the
sole mechanism to explain all these observations.
With the possibility of measuring force in isolated
myofibrils [43], one could evaluate the behavior of each
sarcomere in a myofibril during contraction. With such
measurements, it should be possible to accompany the
behavior of individual sarcomeres along a myofibril and
investigate, at that level, if the system is unstable or
stable. If such measurements were made before and after
an active stretch, then the question of non-uniformity of
sarcomeres in association with the force enhancement
observed after stretch could be clearly answered.
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Dilson Rassier is a post-doctoral fellow under
supervision of Walter Herzog, at the University
of Calgary (Canada). He received his BS in
Physical Education from the Federal University
of Pelotas (Brazil), his MSc in Exercise Physi-
ology from the Federal University of Rio
Grande do Sul (Brazil), and his PhD in Muscle
Physiology from the University of Calgary
(Canada). His research examines the mech-
anisms of muscle contraction and force regu-
lation.
Walter Herzog is Professor of Biomechanics
with Joint Appointments in Kinesiology, Engin-
eering and Medicine at the University of Cal-
gary. He serves as the Associate Dean for
Research in Kinesiology and holds a Canadian
Research Chair in Cellular and Molecular
Biomechanics. He received his Bachelor’s
degree from the Federal Technical Institute in
Zurich, Switzerland, his Master’s/PhD degree
from the University of Iowa, USA, and pursued
postdoctoral training at the University of Cal-
gary, Canada. In 1987, he accepted his current
position in Calgary.