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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 Fig. 1. Schematic representation of the isometric force–length
theory of muscle contraction, as the theory does not relationship, and force enhancement after an active stretch. During iso-
incorporate history-dependent effects of force production metric contractions, force follows the lines in the graph according to
the degree of length in which the contraction starts and the degree of
[12,13]. Also, it cannot be predicted by the degree of
filament overlap. However, if the muscle is actively stretched during
thick and thin filament overlap [14], as isometric force a contraction, e.g. from the initial to the final length (䊊), the force
following stretch at a small average overlap between produced (쎲) is higher than the purely isometric force produced at the
myofilaments might be greater than the isometric force final length. Therefore, the degree of filament overlap is reduced, but
at a great average myofilament overlap (Fig. 1) [5]. the force is increased.
Therefore, much research has focused on the pursuit of
understanding the mechanisms of the stretch-induced the stretch-induced force enhancement, including cross-
force enhancement. bridge kinetics [15], lattice spacing changes with reor-
Several mechanisms have been proposed to explain 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

Corresponding author. Tel.: +1-403-220-8525; fax: +1-403-284- of titin and nebulin as additional force producers [6,19].
3553. While some of these mechanisms have not been care-
E-mail address: walter@kin.ucalgary.ca (W. Herzog). fully tested, the hypothesis that incorporates non-uni-

1050-6411/02/$ - see front matter.  2002 Elsevier Science Ltd. All rights reserved.
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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- Fig. 2. Stretch-induced force enhancement observed during a typical
sponding muscle length. Therefore, two contractions at experiment performed with a single muscle fiber from the frog on the
the same muscle (fiber, average sarcomere) length result descending limb of the force–length relationship. (A) shows contrac-
in different force, depending on whether the muscle was 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
actively stretched during contraction, or not (Fig. 1). a speed of 0.8 mm/s. It also shows an isometric contraction (Lf) perfor-
Force enhancement has two components: (1) a sudden med at a length 15% greater than Li. (B) shows contractions in which
increase in force that is observed during the stretch and the fiber was stretched 15% from Li on the descending limb of the
that dissipates gradually after the stretch is finished; and force–length relationship, at speeds of 0.4, 0.8 and 2.0 mm/s, and an
(2) a stable residual increase in force that remains con- isometric contraction (Lf) performed at a length 15% greater than Li.
Force enhancement increases with the amplitude of stretch but is inde-
stant until the end of the contraction [5,6]. This second pendent of the speed of stretch.
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 The enhanced force observed after stretch is stable at
force–velocity relationship [21]; that is, force increases 苲4.5 s following the length change [5,6]. The amount of
with higher speeds of stretch (Fig. 2B) [4,20]. This force enhancement depends on the amplitude of stretch
component has been explained by an increased number (Fig. 2A), but is independent (or at least nearly so) of the
of attached cross-bridges during the stretch [7], and by speed of stretch (Fig. 2B). Increasing stretch amplitude
an increased strain of cross-bridges when sarcomeres are results in greater force enhancement [1,4,5,23]. Excep-
forcibly extended during a tetanic contraction [22]. tions to these findings are the studies by Julian and Mor-
Therefore, force enhancement during stretch has been gan [20] and Morgan et al. [9], in which the level of
associated with regular cross-bridge properties, as force enhancement was interpreted to be independent of
described in the cross-bridge theory [12]. the amplitude of stretch.
Force enhancement after stretch has characteristics The degree of force enhancement after stretch depends
that seem unrelated to cross-bridge properties. Most on the initial sarcomere length from which the muscle
notably, the force is enhanced (compared to the purely is stretched. It has been shown that, along the descending
isometric force and compared to the force predicted by limb of the force–length relationship, force enhancement
the average overlap of filaments) during the entire period is increased when the muscle fiber is stretched from
during which the fiber is activated. In this paper, we will greater muscle lengths [5]. Most studies on force
concentrate on the characteristics and proposed mech- enhancement were performed on the descending limb of
anisms of the residual force enhancement after stretch. the force–length relationship, and it has been suggested
D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477 473

that force enhancement is observed only in this region 3. Mechanisms of force enhancement after stretch
[4,5,20]. However, little effort has been made to evaluate
force enhancement on the ascending limb of the force– Force enhancement after stretch has been related to
length relationship. Recent studies show steady-state an increased number of attached cross-bridges, to
force enhancement following active muscle stretch on changes in the cross-bridge dynamics, or to some non-
the ascending limb of the force–length relationship (later cross-bridge sarcomeric properties. A mechanism asso-
in this paper). ciated with the cross-bridge dynamics would have to
Using whole cat soleus, Herzog and Leonard [24] assume an increased average force per attached cross-
bridge [15]. A mechanism associated with non-cross-
observed that muscle shortening that immediately pre-
bridge properties may be associated with sarcomere
ceded stretching affected the amount of force enhance-
mechanics and/or the involvement of sarcomeric pro-
ment. More precisely, they observed that for a given
teins, independent of the proportion of attached cross-
stretch (speed, amplitude), force enhancement was
bridges.
decreased in a dose-dependent manner with the amount
A hypothesis related to the cross-bridge dynamics was
of shortening preceding the stretch. However, in experi- introduced by Amemiya et al. [16]. These authors used
ments with single cells from the frog, Edman et al. [5] X-ray diffraction to measure filament position after
found that force enhancement was not affected by short- stretch, and observed a disordering of the myofilament
ening that preceded stretching, when a brief pause was lattice without significant changes in the mean inter-
given between the length changes. This difference filament spacing. This disordering was characterized as
between the two studies is conspicuous, and it may be a displacement of the thin filaments from their initial
caused by the preparations (whole muscle vs single position to a position closer to the thick filaments. This
cells), or by the protocols (with and without pauses arrangement persisted while the muscle was stimulated.
between shortening and stretching phases). Julian and Such a decrease in lattice spacing could enhance the
Morgan [20] showed that an interruption of the contrac- probability of cross-bridge attachment, and consequently
tion introduced after the stretch changes the enhanced force generation.
force in a time-dependent manner, such that a short inter- Although it is difficult to directly evaluate the mech-
ruption does not abolish force enhancement, but a long anism proposed by Amemya et al. [16], a similar result
interruption eliminates all force enhancement. Future is observed when a twitch contraction is potentiated by
research is needed to better understand how force phosphorylation of the myosin regulatory light chains.
enhancement is affected by shortening preceding the In this case, myosin phosphorylation moves the cross-
stretching phase. bridges towards the thin filament [27]. This approxi-
An important feature of force enhancement after mation of the cross-bridge heads to potential actin
stretch that still needs to be carefully investigated is its attachment sites is believed to increase the probability
association (or not) with an increased stiffness, as con- of myosin/actin interactions, and consequently force
tradictory results exist in the literature. Assuming that generation at a given sub-maximal Ca2+ concentration
stiffness is directly related to the number of cross- [28]. Due to the difficulty of testing cross-bridge hypoth-
bridges attached to actin [25,26], an increased stiffness eses experimentally, they should be considered in theor-
in the force-enhanced state could be related to a higher etical models, in which force production can be simu-
number of attached cross-bridges after stretch. Sugi and lated using cross-bridges with different rates of
Tsuchiya [23] performed a series of experiments in attachment/detachment before and after stretch.
which they measured fiber stiffness by applying sinus- Another possibility is that the level of phosphorylation
oidal vibrations to the cells during isometric contractions of the regulatory light chains is enhanced during stretch,
and stretch contractions. It was observed that, although as suggested by Edman [3]. Since the rate constant for
the force was increased (as expected) after the stretch, dephosphorylation of the light chains is very slow, myo-
the stiffness was the same as observed during isometric sin would remain phosphorylated after muscle stretch-
contractions produced at that final length. However, Lin- ing, and could produce the long lasting force enhance-
ari et al. [7] observed an increased stiffness in single ment following stretching. However, there is no evidence
muscle cells just after stretch, which was directly asso- that an active stretch enhances the biochemical steps
ciated with an increased force enhancement. It should be involved in myosin light chain phosphorylation, (e.g.
enhancement of the myosin light chain kinase activity),
cautioned that in their experiments force never reached
but this hypothesis should be tested in the near future.
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 4. The theory of sarcomere length non-uniformity
with longer contraction times should be performed.
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 [29], who suggested that sarcomeres were unstable on
length non-uniformity theory [20]. This idea has been the descending limb because of the negative slope of the
used by several researchers [6,9] and was ultimately force–length relationship in that region. However, the
associated with the ‘popping sarcomeres’ theory [18]. force–length relationship is obtained by isolated contrac-
The first experimental observation related to the sarco- tions at different lengths, e.g. Gordon et al. [14], and it
mere length non-uniformity theory was made by Julian is not necessarily correct to infer dynamic instability
and Morgan [20]. They observed that during stretch of from a static observation. In fact, it is quite easy to
single cells, sarcomere lengths did not change by the design systems in which the static force decreases while
same amount: sarcomeres near the center of the cells the dynamic force increases with increasing length
stretched more than average, while sarcomeres near the [30,31].
end of the cell stretched less than average. Julian and Several researchers suggested that sarcomere lengths
Morgan [20] suggested that this non-uniformity of sarco- are stable during contractions over the whole physiologi-
mere lengths was responsible for the force enhancement cal range of lengths, including the descending limb of
after stretch. However, in a subsequent study, Edman et the force–length relationship [30,32–34]. It has been
al. [5] observed that force enhancement was not only shown that force following stretch is, in some situations,
produced by muscle fibers as a whole, but also by indi- not only greater than the isometric force obtained at the
vidual clamped segments of the fiber, and by isolated final length (as discussed previously), but also greater
sarcomere populations. Edman et al. [5] concluded that than the force recorded at the initial length from which
force enhancement was possible, independently of the the muscle was stretched [4,5]. This force enhancement
development of sarcomere length non-uniformity. above the initial isometric force can be observed after
Morgan [18] incorporated observations of sarcomere the force reaches a steady-state following stretch [35,36].
length non-uniformity [20] and sarcomere instability on In this case, the dynamic force–length trace has a posi-
the descending limb of the force–length relationship [17] tive slope that is characteristic of a stable system that
to provide an explanation for the force enhancement exhibits hardening properties. This idea agrees with
after stretch. Morgan [18] argued that when fibers are observations that a fiber that is stretched on the
actively stretched on the descending limb of the force– descending limb of the force–length relationship has a
length relationship, sarcomeres located near the center positive stiffness during the stretch [37,38]. Along those
of the fiber are stretched more than sarcomeres near the lines, Allinger et al. [39] showed that the dispersion of
end of the fiber. As the stretch continues, these sarcom- sarcomere length decreases during a tetanic contraction,
eres are stretched until actin–myosin overlap is lost (i.e. which is a property of a stable system.
they ‘pop’). Sarcomeres located near the end of the fibers Therefore, sarcomere lengths may be stable on the
do not stretch as much, and may in fact stay almost iso- descending limb of the force–length relationship, thereby
metric during the elongation of the cell. These sarcom- questioning the origin of the popping sarcomere and the
eres produce the active force in the fiber. The ‘popped’ sarcomere length non-uniformity theories. Although it is
sarcomeres are supported by the passive tension present difficult to directly evaluate the sarcomere length non-
on the descending limb of the force–length relationship. uniformity theory experimentally, its well-defined math-
The two groups of sarcomeres need to have equal force ematical framework allows for the derivation of testable
to attain equilibrium. At equilibrium, the force produced hypotheses. If the sarcomere length non-uniformity
by the two groups of sarcomeres is greater than the iso- theory is the sole mechanism responsible for the steady-
metric force at the corresponding length, which is state force enhancement after stretch, and if sarcomeres
assumed to have a relatively uniform (average) sarco- behave as proposed by Morgan [18], then the following
mere length distribution. The sarcomere length non-uni- should be true: (1) force enhancement after stretch
formity theory can explain some experimentally should not be observed on the ascending limb of the
observed features of force enhancement after stretch. 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-
5. Instability and non-uniformity of sarcomeres ing stretch should never exceed the isometric force pro-
duced on the plateau of the force–length relationship.
Naturally, the theory of ‘popping’ sarcomeres is based We performed experiments with the cat soleus and with
on the notion of an inherent instability of sarcomere single cells dissected from the frog, in which we tested
lengths that is present on the descending limb of the the above hypotheses.
force–length relationship [17,20]. Instability would be Using single muscle cells dissected from the frog
responsible for the non-uniform length changes in sar- (Rana pipiens) we observed that, on the ascending limb
comeres, which in turn causes sarcomere dispersion and of the force–length relationship, the steady-state force
heterogeneity in sarcomere lengths during contractions. following stretch was greater than the purely isometric
The notion of instability was first introduced by Hill force produced at the final length. The amount of force
D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477 475

enhancement was generally smaller on the ascending the maximal isometric force on the plateau of the force–
compared to the descending limb of the force–length length relationship. An unstable system, or a theory
relationship. The same observation was made in the in based on the sarcomere length non-uniformity idea
situ cat soleus. In these experiments, soleus was stimu- alone, cannot explain this result. If some sarcomeres
lated at 5 and 30 Hz, and we observed a small but con- ‘pop’ during stretch, and others are maintained isometric
sistent force enhancement on the ascending limb of the (or stretch only by a small amount) during the stretch of
force–length relation [8]. Force enhancement on the the whole fiber, force cannot exceed the maximal iso-
ascending limb of the force–length relationship was also metric force produced at the plateau of the force–
reported by De Ruiter et al. [10] in human adductor pol- length relationship.
licis muscle.
Other investigators, using single cells from frog or
whole muscles from the cat, failed to find force enhance- 6. Alternative mechanism of force enhancement
ment on the ascending limb of the force–length relation- after stretch
ship [6,9,20]. They may have used amplitudes of stretch
that were too short to observe a measurable force Since the sarcomere length non-uniformity and the
enhancement. popping sarcomere theory cannot account for the force
In another series of experiments performed with single enhancement above the plateau forces, other mech-
muscle cells from frogs, we were interested in determin- anisms should be considered. An alternative, or
ing if force enhancement could be observed at levels additional, mechanism of force enhancement after
above the isometric force produced on the plateau of the stretch should incorporate all the characteristics
force–length relationship. Our interest was based on pre- observed in the experiments described, and should
viously reported results. Edman et al. [5] (their Fig. 3), assume that the muscular system is stable under contrac-
showed force enhancement of about 1–2% greater than tion.
the isometric force produced at the plateau of the force– One possibility that has been often mentioned in the
length relationship. The authors credited the results to literature but has not received direct experimental sup-
measurement error, and did not persist to evaluate their port is the idea that a passive elastic element is engaged
finding. Results from one experiment from our study are during an active stretch [6,19]. Edman and Tsuchiya [6]
shown in Fig. 3. In this case, force following stretch performed a series of experiments in which single mus-
exceeded the isometric force produced at the initial cle fibers were released to shorten against a small load
length, showing stable properties as explained above. at different times after a stretch, and also after tetanic
Even more important for the present discussion, force contractions. The force transients of the contractions in
after stretch also exceeded the isometric force produced which a stretch was applied exhibited a greater and
at the plateau of the force–length relationship. This result steeper decrease in force than those obtained during an
was statistically confirmed in more than 30 separate isometric contraction. These findings were interpreted as
experiments. In some cases, force was 苲10% higher than resulting from the elongation of a passive elastic struc-

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.
476 D.E. Rassier, W. Herzog / Journal of Electromyography and Kinesiology 12 (2002) 471–477

ture. The authors suggested that some half-sarcomeres With the possibility of measuring force in isolated
would stretch more than others during the elongation, myofibrils [43], one could evaluate the behavior of each
and these overstretched regions of the sarcomere would sarcomere in a myofibril during contraction. With such
be supported by the engagement of an elastic, passive measurements, it should be possible to accompany the
structure. behavior of individual sarcomeres along a myofibril and
Alternatively, the engagement of a passive element investigate, at that level, if the system is unstable or
could be directly responsible for the increase in force. stable. If such measurements were made before and after
Although this possibility has not been directly tested, an active stretch, then the question of non-uniformity of
it has been observed that under some conditions, force sarcomeres in association with the force enhancement
enhancement is accompanied by an increase in the pass- observed after stretch could be clearly answered.
ive force (Fig. 3) [8]. This increase in passive force pro-
duced by stretching an active muscle is not observed
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myosin light chain phosphorylation in rabbit skeletal muscle:
Physical Education from the Federal University
implications for regulation of actin-myosin interaction. Proc Natl of Pelotas (Brazil), his MSc in Exercise Physi-
Acad Sci USA 1990;87:414–8. ology from the Federal University of Rio
[29] Hill AV. The mechanics of active muscle. Proc Royal Soc Lond Grande do Sul (Brazil), and his PhD in Muscle
B 1953;141:104–17. Physiology from the University of Calgary
[30] Allinger TL, Epstein M, Herzog W. Stability of muscle fibers on (Canada). His research examines the mech-
the descending limb of the force-length relation. A theoretical anisms of muscle contraction and force regu-
consideration. J Biomech 1996;29:627–33. lation.
[31] Epstein M, Herzog W. Theoretical models of skeletal muscle:
Biological and mathematical considerations. New York: Wiley, Walter Herzog is Professor of Biomechanics
1998. with Joint Appointments in Kinesiology, Engin-
[32] Deleze JB. The mechanical properties of the semitendinosus mus- eering and Medicine at the University of Cal-
cle at lengths greater than its length in the body. J Physiol gary. He serves as the Associate Dean for
1961;158:154–64. Research in Kinesiology and holds a Canadian
[33] Pollack GH. Muscles and Molecules. Seattle: Ebner, 1990. Research Chair in Cellular and Molecular
[34] ter Keurs HEDJ, Iwazumi T, Pollack GH. The sarcomere length- Biomechanics. He received his Bachelor’s
tension relation in skeletal muscle. J Gen Physiol 1978;72:565– degree from the Federal Technical Institute in
Zurich, Switzerland, his Master’s/PhD degree
92.
from the University of Iowa, USA, and pursued
[35] Schachar R, Herzog W, Leonard TR. Stability and the descending postdoctoral training at the University of Cal-
limb of the force-length relation in mammalian skeletal muscle. gary, Canada. In 1987, he accepted his current
XI Congress of the Canadian Society for Biomechanics; position in Calgary.
2000:148.