Download Series Elasticity Behavior During the Stretch

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439
Lannergren, J., Lindblom, P., & Johansson, B. (1982). Contractile properties of two varieties of
twitch muscle fibres in Xenopus laevis. Acta Physiologica Scandinavica, 114,523-535.
Marsh, R.L. (1994). Jumping ability of anuran amphibians. In J.H. Jones (Ed.),Advances in veterinary science and comparative medicine (pp. 51-11 1 ) . New York: Academic Press.
Marsh, R.L., & John-Alder, H.B. (1994). Jumping performance of hylid frogs measured with highspeed cine film. Journal of Experimental Biology, 188,131-141.
Soest, A.J. van, Roebroeck, M.E., Bobbert, M.E, Huijing, P.A., & Ingen Schenau,G.J. van (1985).A
comparison of one-legged and two-legged countermovementjumps. Medicine and Science
in Sports and Exercise, 17,635-639.
Claire 7: Farley is with the Department of Integrative Biology, University of California, Berkeley,
CA 94720-3140.
Series Elasticity Behavior During the Stretch-Shortening Cycle
Francis Goubel
The target article by Ingen Schenau, Bobbert, and Haan is a pertinent review of the controversies regarding the role played by elastic energy in the stretch-shortening cycle (SSC).
The authors have done an excellent job in bringing together human and animal data where
discrepancy is often due to the difference in level of observation. The part devoted to
efficiency in repetitive SSCs is convincing. My goal here is not to discuss the impressive
overview they have presented even if I don't agree with some of their conclusions.
In this commentary, I would like to expand on some ideas and address a few issues on
series elasticity that should be considered when possible benefits of the SSC are examined.
Slow Twitch or Fast Twitch Fibers?
Ingen Schenau et al. suggest that one of the positive effects of a countermovement is that
it allows muscles time to develop force. They argue that this effect is consistent with the
fact that subjects having a high percentage of slow twitch fibers are able to better benefit
from a countermovement. In my opinion, the influence of fiber type is more complex.
Slow twitch (ST) and fast twitch (FT) fibers can benefit differently from the SSC, depending on the phase of the cycle.
Stretching Phase. The enhancement of performance characterizing SSC exercises
has been attributed to the storage of elastic energy in the muscle-tendon complex during
the stretch. By analyzing countermovementin verticaljumps, Bosco,Tihanyi, Komi, Fekete,
and Apor (1982) demonstrated that those subjects who had more FT fibers in their
vastus lateralis benefited more for the stretching phase performed with small angular
displacements. It was assumed that energy was stored more efficiently in FT fibers due to
a possibility of developing a greater force till the end of the stretch.
The exact amount of energy stored is, however, a function of the stiffness of the
elastic elements, and some results suggest that ST and FT fibers may well have different
elastic characteristics. This was first revealed from the work of Wells (1965), who showed
that the so-called series elastic component (SEC) of a rat muscle containing predominantly ST fibers (soleus) was stiffer than that of a muscle with an important percentage of
FT fibers (tibialis anterior). Unfortunately, the anatomical organization of those muscles
is quite different, and an alternative explanation of the observed differences in terms of
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variation in the ratio between tendon length and total muscle length cannot be excluded
(Close, 1972). In my laboratory we attempted to solve this problem by inducing fiber type
transitions in the rat soleus muscle in response to exercise. We demonstrated that when a
training technique increases the percentage of FT fibers, SEC stiffness decreases (AlmeidaSilveira, Pkrot, Pousson, & Goubel, 1994; Pousson, PCrot, & Goubel, 1991).
The opposite mechanical change (i.e., an increase in SEC stiffness) was also associated with a relative increase in ST fibers (Goubel & Marini, 1987). Such results are in
accordance with those of Petit, Filippi, Emonet-Denand, Hunt, and Laporte (1990), who
found that in the peroneus longus of cat, ST motor units had a greater dynamic stiffness
than FT motor units. On the other hand, data obtained on skinned Ff and ST fibers indicate no difference in elastic characteristics of cross-bridges whatever the myosin heavy
chain isoform (Galler, Hilber, & Pette, 1996). However, differences in complex stiffness
between ST and FT fibers have been demonstrated by sinusoidal analysis (Kawai &
Schachat, 1984). It is also conceivable that elastic structures in series with ST fibers are
stiffer than those in series with FT fibers. This could explain discrepancies between results obtained at different levels of observation (skinned fiber vs. whole muscle). This
would imply, however, an anatomical organization of the passive part of the SEC, which
is unlikely considering the scattered distribution of the fibers.
However that may be, when a muscle has a high proportion of FT fibers, its SEC
seems relatively compliant. This cannot necessarily favor energy storage since a stiffer
SEC should improve the transmission of force (see below).
Coupling Time. The coupling time (i.e., the time delay between stretching and
shortening) is important to the "efficiency" of the SSC. Stored energy can be dissipated into
heat if the coupling time is not sufficiently short. Furthermore, part of the potential energy
is stored in cross-bridges as long as they remain in the attached state. Then, it can be
hypothesized that a coupling time shorter than the cross-bridge lifetime will lead to a better
utilization of the potential energy (Bosco, 1982). This stresses the influence of the fiber
type, since the rate of cross-bridge cycling is higher in FT fibers than in ST fibers. Consequently, a SSC with a relatively long coupling time will favor muscles where ST fibers
predominate: Those fibers will be able to retain their potential energy since detachment of
the cross-bridges may not occur.
Shortening Phase. During this phase, when the muscle is generating mechanical work, a part of energy may come from the release of potential energy previously stored
in the SEC. It is evident that this recoil of elastic energy depends on the amount stored
during the stretching phase. Then, in terms of fiber type influence, the same holds for
both phases. Furthermore, Bosco et al. (1982) reported that for small angular displacements, the percentage of recoil of potential energy did not depend on fiber type composition. However, this percentage was higher in subjects rich in ST fibers when jumps were
performed with large angular displacements. This result was interpreted in terms of loss
of potential energy in detached cross-bridges from FT fibers. On the other hand, it can be
hypothesized that fast shortening due to activation of FT fibers would improve the recoil
phenomenon thanks to a rapid fall in tension during the shortening phase. Recent results
concerning determination of efficiency for a range of SSCs of the rat gastrocnemius do
not confirm this hypothesis (Ettema, 1996).
Are Muscle Fibers Lengthened During the Stretching Phase?
Ingen Schenau et al. report the well-documented force enhancement during stretch in
tetanized isolated muscles and single muscle fibers. This phenomenon is also present in
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human muscle. For electrically stimulated muscle in humans, it is clear that stretching the
muscle during isometric tetanus produces extra force. In the first dorsal interosseusmuscle,
forces 1.76 times the isometric value are reported for stretching velocities of 1.08 muscletendon complex length per second (Cook & McDonagh, 1993). In the same way, when
elbow flexors are stretched during maximal voluntary contraction, forces 1.6 times the
isometric value can be obtained (Lensel-Corbeil, Goubel, Gerbeaux, & Pertuzon, 1992).
Even so, I agree that it remains to be proved that muscle fibers are lengthened during
SSCs occurring naturally.
In animals, the length changes of the muscle fibers have been recorded by using an
ultrasound transit-time technique. Thus, Griffiths (1991) was able to study the effect of
slow to medium speed stretches on the active medial gastrocnemius of the cat. He demonstrated that for activities corresponding to walking and trotting, lengthening was entirely
taken up in the tendons: Muscle fibers actually shortened throughout the imposed stretch.
Then, the role of muscle spindles during such exercises needs to be reinvestigated.However, as pointed out by Komi (1990), it should be of greater importance to extend this kind
of study to experimental situations that cause higher muscle stiffness than those mimicking walking and trotting.
As far as human movements are concerned, experimental data are scarce (Winters,
1990). To my knowledge, the conclusion that muscle fibers shorten when the muscletendon complex of humans is lengthened was drawn from simulation studies. Such results necessarily depend on rather crude estimates of SEC characteristics. For instance, a
careful examination of Figure 6 in Belli and Bosco (1992) shows that a slight modification of the numerical value for the SEC stiffness could lead to the opposite result (i.e., a
lengthening of the contractile component). Further work is needed to he sure that muscle
fibers are not lengthened during SSC. Then potentiation during the stretching phase will
be clearly rejected.
SEC: Compliant or Stiff?
It is sometimes claimed that a compliant SEC is necessary for maximal utilization of
elastic strain energy. As indicated by Ingen Schenau et al., this idea led Wilson, Wood, and
Elliott (1991) to propose flexibility training in order to improve the capacity to store elastic energy. However, an increase in SEC stiffness was found by Pousson, Van Hoecke, and
Goubel(1990) when studying the effect of eccentric training on human elbow flexors. As
the goal of training is to improve performance, both results contradict themselves.
In fact, an increase in stiffness has two positive consequences: (a) During stretching, more potential energy can be stored because force is able to rise rapidly, and (b)
during shortening, the contractile component can generate more work since its shortening is not counteracted by a compliant SEC. Other problems remain unresolved. For instance, if the muscle-tendon complex is stretched beyond the elastic limit of its crossbridges, the extra energy stored within the tendon is limited by decreased storage in the
muscle fibers. An increase in fiber stiffness for high levels of force should avoid this
kind of problem. Some results obtained in isolated fibers (Bressler, Dusik, & Menard,
1988; Colomo, Lombardi, & Piazzesi, 1986) and in whole muscles (Goubel & LenselCorbeil, 1988; Stienen & BlangC, 1981) are in accordance with this proposition. On
the other hand, an increase in SEC compliance may have some interest during the early
part of the shortening phase: The consecutive reduction in shortening velocity will
allow the contractile component to develop a higher force thanks to the force-velocity
relationship!
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Finally, the best solution should be an adaptation of the SEC characteristics according to the phase of the SSC. As mentioned by Cavagna, Citterio, and Jacini (1981), it can
be proposed that during an SSC, the SEC tends to meet two opposite requirements: (a) an
increase in stiffness during stretching that will favor a better transmission of force and will
reduce the coupling time, and (b) a decrease in stiffness during shortening that will allow
a better release of potential energy. The "Cavagna effect" (actual increase in compliance
during SEC recoil) was first reported in frog and toad muscles (Cavagna & Citterio, 1974).
As shown by Lensel and Goubel(1987), for the Cavagna effect to occur, a large stretch
must be followed by arelease given from a length that is 15% in excess of the length when
isometric tension is maximal. In view of these restrictions, the usefulness of the Cavagna
effect for human movement is questionable (Hof, Geelen, &Van Den Berg, 1983; LenselCorbeil & Goubel, 1990).
Conclusion
In order to ensure that storage and reutilization of elastic energy can be ruled out as an
explanation for the enhancement of work during SSC, there is a need for more conclusive
experimental data. In the literature, most of the data are contradictory. This is mainly
because results obtained at a given level of observation and using a given protocol d o not
allow systematically broad generalization. Thus, it is not easy to take a clear position in
some of the controversies. However that may be, this target article will be very useful for
all working in the field of muscle mechanics.
References
Almeida-Silveira, M.I., Pkrot, C., Pousson, M., & Goubel, F. (1994). Effects of stretch-shortening
cycle training on mechanical properties and fibre type transition in the rat soleus muscle.
Pflugers Archiv, 427,289-294.
Belli, A., & Bosco, C. (1992). Influence of stretch-shortening cycle on mechanical behaviour of
triceps surae during hopping. Acta Physiologica Scandinavica, 144,401-408.
Bosco, C. (1982). Stretch-shortening cycle in skeletal muscle function with special reference to
elastic energy and potentiation of myoelectrical activity. Studies in Sport, Physical Education
and Health, Volume 15. University of Jyvaskyl2, Finland.
Bosco, C., Tihanyi, J., Komi, P.V., Fekete, G., & Apor, P. (1982). Store and recoil of elastic energy
in slow and fast types of human muscles. Acta Physiologica Scandinavica, 116, 343349.
Bressler, B.H., Dusik, L.A., & Menard, M.R. (1988). Tension responses of frog skeletal muscle
fibres to rapid shortening and lengthening steps. Journal of Physiology, 307,631-641.
Cavagna, G.A., & Citterio, G. (1974). Effect of stretching on the elastic characteristics and the contractile component of frog striated muscle. Journal of Physiology, 239, 1-14.
Cavagna, G.A., Citterio, G., & Jacini, P. (1981). Effects of speed and extent of stretching on the
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Colomo, F., Lombardi, V., & Piazzesi, G. (1986). The relation between force, stiffness and velocity
of lengthening in "tendon-free" segments of frog single muscle fibres. Journal of Physiology,
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Galler, S., Hilber, K., & Pette, D. (1996). Force responses following stepwise length changes of rat
skeletal muscle fibre types. Journal of Physiology, 493,219-227.
Goubel, F., & Marini, J.F. (1987). Fibre type transition and stiffnessmodification of soleus muscle of
trained rats. Pfliigers Archiv, 410,321-325.
Goubel, F., & Lensel-Corbeil, G. (1988). Stiffness changes during ramp stretches in frog sartorius
muscle as studies by shortening or lengthening steps. Journal ofPhysiology, 406,47P.
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stiffness produced by motor units of different types in peroneus longus muscle of the cat.
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Pousson, M., Van Hoecke, J., & Goubel, F. (1990). Changes in elastic characteristics of human
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muscle produced by jumping training. PJugers Archiv, 419, 127-130.
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General Physiology, 78, 161-171.
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Francis Goubel is with the De'partementde GknieBiologique, Universite'deTechnologie CompiLgne,
France.
What I s the Series Elastic Component in Skeletal Muscle?
Walter Herzog
Because of space restrictions, I will focus my comments on issues related to the enhancement of work and will ignore all aspects discussed regarding efficiency. I will start with a