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Vol. 83, Issue 5, 1741-1748, 1997
1 Faculty of Education, ABSTRACT Takarada, Yudai, Hiroyuki Iwamoto, Haruo Sugi, Yuichi
Hirano, and Naokata Ishii. Stretch-induced enhancement of
mechanical work production in frog single fibers and human muscle.
J. Appl. Physiol. 83(5):
1741-1748, 1997.
cross bridges; prestretch; work output; eccentric contraction; countermovement
INTRODUCTION WHEN CONTRACTING MUSCLE is stretched (prestretch) and
subsequently allowed to shorten, it exerts larger mechanical work than it does without prestretch. This effect of prestretch has been regarded
as important in various movements of organisms, including movements of
humans. Indeed, movements seen in vivo are often associated with the
forced lengthening (biomechanically termed as eccentric action) before
the shortening (concentric action) of muscles (11). However, studies
with isolated muscle preparations and those on whole body movements
have so far led to separate interpretations for the mechanisms
underlying such an enhancement of mechanical performance.
Both whole muscle preparations and single muscle fibers of the frog
maintain tension higher than that determined by their length-tension
relations when they are stretched and kept at stretched lengths (1, 12,
13). Accordingly, releasing them either isotonically or isokinetically
from the stretched state gives rise to larger velocity or force,
respectively, resulting in an upward shift of the force-velocity
relations (8, 13, 28). In particular, experiments with isotonic
releases followed by stretches of single fibers (13, 29) have shown the
stretch-induced increase in steady-state shortening velocity, which was
determined after a complete elastic recoil of the series elastic
component (SEC). These studies strongly suggest that stretching the
contracting muscle causes an improvement of the ability of the
contractile element (actin-myosin cross bridges) to generate force,
even though the molecular mechanism of such an improvement
is not fully understood.
On the other hand, muscle contractions in situ are subjected to more
complex mechanical environment. Muscles have much longer SEC than do
single fibers. The major portion of SEC is located in the tendon and
may play an important role in the storage of elastic energy and thereby
make the movement energetically more efficient (2, 17).
Because muscle fibers generate larger force (eccentric force) against
the forced lengthening than during isometric and isotonic contractions,
it is plausible that the SEC stores an extra elastic energy through the
course of lengthening and then liberates it during the subsequent
shortening under smaller load (3, 10). However, it should also be noted
that the overstretched SEC may diminish the length change of muscle
fibers and consequently reduce the work done by the muscle fibers
themselves (4, 15). In addition, the level of motor-unit recruitment
can be modified by neural reflex; it can be either facilitated (stretch
reflex) or depressed on stretch through actions of muscle
proprioceptors.
Therefore, in human movement, the mechanical advantage of an eccentric
counteraction (stretching the muscle) before a concentric action may be
the enhancement related to various mechanical events occurring at
various stages of contraction. However, mechanical advantage of
eccentric counteraction has been so far interpreted mainly in terms of
the role played by the SEC (3, 7, 22), although the enhancement of
mechanical performance in the interacting cross bridges has become
evident by studies with single fibers. In this particular context, it
should be noted that the enhancement of the ability of single fibers to
generate force has been shown to depend on the rate of prestretch in a
manner that the enhancement is lowered with the increase in the rate of
prestretch (26). Thus, in the present study, we applied a similar
stretch-release protocol with varied stretch velocity to contractions
of both frog single muscle fibers and human muscles (elbow flexors) to see how the stretch-induced enhancement of mechanical performance within muscle fibers is related to contractions in situ.
METHODS
The relations between the velocity of prestretch
and the mechanical energy liberated during the subsequent isovelocity
release were studied in contractions of frog single fibers and human
muscles. During isometric contractions of frog single fibers, a ramp
stretch of varied velocity (amplitude, 0.02 fiber length; velocity,
0.08-1.0 fiber length/s) followed by a release (amplitude, 0.02 fiber length; velocity, 1.0 fiber length/s) was given, and the amount
of work liberated during the release was measured. For human muscles,
elbow flexions were performed with a prestretch of varied
velocity (range, 40°; velocity, 30-180°/s) followed by an
isokinetic shortening (velocity, 90°/s). In both frog single fibers
and human muscles, the work production increased with both the velocity
of stretch and the peak of force attained before the release up to a
certain level; thereafter it declined with the further increases of
these variables. In human muscles, the enhancement of work production
was not associated with a significant increase in integrated
electromyogram. This suggests that changes in intrinsic mechanical
properties of muscle fibers play an important role in the
stretch-induced enhancement of work production.
RESULTS
The work produced by the fiber during the release and the work done on the fiber externally during the stretch were measured from the force-length diagrams (Fig. 2) as positive and negative work, respectively. The values of both positive and negative work were normalized to the positive work produced during the release without prestretch and were plotted against the velocity of stretch for three muscle fibers examined (Fig. 3). The amount of positive work was always larger after stretch than in unstretched control. However, it initially increased with the stretch velocity up to the velocity of ~0.2 Lo/s (optimal velocity of stretch) and then decreased with the further increase in velocity. Thus it exhibited a marked contrast to the negative work, the amount of which increased with the velocity of stretch until it reached a steady level. The presence of an optimal stretch velocity indicated the presence of an optimal force attained before release for the production of positive work, because the force increased with the stretch velocity (Fig. 3, top line). When the positive work was plotted against the force attained before release, relative to the isometric force developed without stretch (Po), it exhibited a more pronounced biphasic dependence with an optimal eccentric force that was 1.6-1.8 times as large as the isometric force (Fig. 4).
) and positive work made by fiber during release (
) were
plotted. Values of work (means ± SE) were normalized with respect
to those of positive work made without stretch (control). Curves were
drawn by eye.
Enhancement of mechanical work in human muscles. When the isovelocity stretch-release protocol similar to that for frog single fibers was applied to contractions of human elbow flexors, responses qualitatively similar to those of frog single fibers were observed. Figure 5 shows representative length and force records. The muscles responded to the stretch with the generation of large eccentric force, and during the subsequent release, they retained a slightly higher level of force (Fig. 5B) than that during the release without stretch (unstretched control, Fig. 5A).
20°) (left), and then ramp stretch (velocity,
90°/s in this record) immediately followed by a release, both by
40°, was given during contraction (right).
As in the case with the frog single fibers, both positive and negative work production was measured from the force-length relations (Fig. 6), normalized to the positive work produced in the unstretched control, and plotted against the velocity of stretch (Fig. 7). Although both the amount of negative work and the degree of the enhancement of positive work were relatively small, their dependencies on the velocity of stretch were substantially similar to those in frog single fibers. The positive work was significantly (P < 0.05) larger than that in the unstretched control at stretch velocities of 60, 90, 120, and 150°/s and was maximal at 90°/s (0.54 Lo/s for biceps brachii).
,
negative work; , positive work) in human elbow flexors. Values of
work (means ± SE, n = 9 subjects)
were normalized to those in unstretched control. Curves were drawn by
eye.
When the positive work was plotted against the eccentric force attained before release, it showed a sharp peak at ~1.25 Po, where Po is the isometric force generated in contractions without stretch (Fig. 8). However, this optimal eccentric force for work production was much smaller than that in the frog single fibers (~1.8 Po).
Effects of prestretch on EMG activity. To see whether any change in the motor-unit recruitment occurs and plays a role in the enhancement of work production after the stretch, we analyzed EMG signals from both elbow flexors (biceps brachii) and extensors (triceps brachii). The iEMGs were obtained during both the stretch and release and were normalized to those during the release in unstretched control. Figure 9, A and B, shows the relationship between the velocity of stretch and the iEMG from biceps brachii and triceps brachii, respectively. In the biceps brachii, the iEMG during both the stretch and release tended to be larger than that during the release in unstretched control (Fig. 9A). However, the difference was not significant (P > 0.05) at stretch velocities of 30, 90, 120, and 150°/s. Notably, the mean iEMG was minimal at the stretch velocities of 90-120°/s, at which the maximal enhancement of work production was seen (Fig. 7). In triceps brachii, the iEMG during the stretch and release was consistently unchanged from that during the release in unstretch control, with an exception of a slight increase (P < 0.05) during the release subsequent to the stretch at 30°/s (Fig. 9B). These results suggest that the change in the motor unit-recruitment pattern is not primarily related to the enhancement of work production observed in the present experimental condition.
) and
stretch (). Values of iEMG (means ± SE;
n = 9 subjects) were normalized to
those in unstretched control.
DISCUSSION
The present study showed that, in both frog single fibers and human elbow flexors, the mechanical work production during the shortening preceded by a stretch is a function of stretch velocity and that an optimal velocity of stretch exists for the enhancement of work production. Because the force attained before release increased consistently with the velocity of stretch, there also existed an optimal eccentric force (Figs. 4 and 8) for the enhancement of work production.
However, one must use caution when comparing the results on human muscles with those on frog single fibers, because the distance of stretch differed considerably between experiments with these two kinds of muscle. In frog single fibers, the distance of stretch was limited to within 2% of Lo, because stretches with longer distance tended to have an injurious effect and often caused irreversible damage in the fibers. Such a short length change is likely within a range of single to a few cross-bridge strokes (16), so that the obtained results would manifest events occurring in single to several cross-bridge cycles. On the other hand, the distance of stretch in human muscles was subjected to severe mechanical constraints imposed on the isokinetic dynamometer. Because of the large mass of the lever system and that of the forearm, the acceleration and deceleration took time (50 ms), so that the stretch had to be much larger in distance (~0.2 Lo) than in frog single fibers. Therefore, the results in human muscles would represent more steady-state events and thus may exhibit some quantitative differences from those on frog single fibers.
Among other differences, we should refer to the difference between the optimal force against stretch for the subsequent work production in human muscles (~1.3 Po) and that in frog single fibers (~1.8 Po). The recent study of Ishii et al. (19) with an in vitro motility assay system, in which velocities of steady-state sliding between isolated myosin filaments and actin filaments were directly measured, has shown that the load exceeding Po caused the sliding movement directed opposite to the polarity of actin filament (corresponding to forced lengthening in muscle). In this system, thick filaments were detached from actin filaments when the force exceeded ~1.4 Po during the steady-state sliding. This finding is apparently consistent with the present results on human muscles and suggests that the markedly large force exerted by frog single fibers represents transient, unsteady force developed by individual cross bridges at the instant when they are forcibly detached.
A part of the negative work absorbed by frog single fibers and human muscles during stretch must be stored by the SEC in the form of elastic energy. Because this elastic energy increases with force on the SEC, it would be maximal at the maximal velocity of stretch attained within the range used in the present experiment. Therefore, the reutilization of elastic energy stored in the SEC cannot fully account for the present, biphasic dependence of the work production on the velocity of stretch.
The work made by the contractile element (CE) after stretch is, however, not as simply evaluated in the isovelocity release experiments. The large force exerted by the CE during the forced lengthening stretches the SEC to a greater extent than in isometric contractions. Although this process gives the SEC larger elastic energy, it reduces the distance of shortening of the CE within a limited range of release. Even if the force generated by the CE during the shortening were enhanced by the previous stretch (see below), the diminished distance of shortening would have an effect of reducing the work produced by the CE, depending on both the degree of force enhancement and the decrease in the distance of shortening. Such a mechanism may provide one possible reason why the total amount of work (work by SEC plus that by CE) was reduced when either stretch velocity or force exceeded a certain level (15).
The other possible mechanism for the present finding is related directly to the contractile properties of the CE. Since Abbot and Aubert (1) demonstrated, for the first time, the stretch-induced improvement of the ability of a frog muscle to generate tension, this phenomenon has been studied extensively with single-fiber preparations. When isometrically contracting single fibers are stretched from lengths at the descending limb of their length-tension relations and then kept at stretched lengths, they generate extremely large tension during the stretch, which is then followed by an exponential decay toward the new steady-state level after the end of stretch. This level of tension is higher than that determined on the length-tension relation (13). The peak tension attained during stretch increases with the velocity of stretch, whereas the level of the after-tension maintenance increases with decreasing velocity of stretch (26), suggesting that the enhancement of tension-generating capability is related to some complicated modification in actin-myosin interaction.
Measurements of stiffness of contracting single fibers (30) have shown that the stiffness after the end of stretch is not larger than without stretch, despite the maintenance of higher tension. This suggests that the enhancement of tension-generating capability is not caused by an increase in the number of interacting actin-myosin cross bridges. On the other hand, an X-ray diffraction study by Sugi et al. (27) has shown the increase in the irregularity of the hexagonal myofilament lattice on stretch, which may bring about an elevation of the electrostatic potential and cause an additive effect on the generation of active tension.
Such an enhancement of tension-generating capability greatly influences the dynamic properties of muscle. When isometrically contracting frog single fibers are stretched and then released isotonically, they exhibit larger shortening velocity than is attained under the same load without stretch, resulting in the upward shift of the force-velocity relations (8, 13, 28).
Notably, the effect of SEC is completely excluded in this type of experiment, since the steady-state shortening velocity is determined after the end of shortening (elastic recoil) of the SEC. Also, isovelocity stretch-release experiments (9) have shown that the force at given shortening velocity increased after the stretch, resulting in the increase in mechanical work produced for the same distance of shortening.
In human muscles, many additional factors still exist that influence muscle contractile properties in situ. Nervous control, including the stretch reflex, is the most likely to be considered, because stretching the muscle may immediately cause an additional recruitment of motor unit and also may cause an inhibitory effect when the force exceeds a certain level. However, in the present study, measurement of electrical activity showed no significant change in iEMG during the shortening after the stretch of 90-150°/s, where the largest enhancement of work production was observed (Figs. 7 and 9). This suggests that the neural modification plays a minor role in the present experimental condition. This result is consistent with the report by Gulch et al. (18) that no appreciable change in iEMG occurred, despite an enhancement of tension, when isometrically contracting elbow flexors were stretched and then held at stretched state. On the other hand, knee extensors have been shown to exhibit much-reduced EMG activities during forced lengthening compared with the EMG activities during isometric contraction (31).
Recent studies of motor control of eccentric contractions have shown that the neural commands controlling eccentric contractions differ considerably from those controlling concentric contractions (14). Among other differences, motoneurons with higher recruitment threshold (motor units for fast-twitch fibers) are predominantly recruited in submaximal eccentric contractions, as opposed to the "size principle" operating in the concentric contractions (23). In addition, the neural commands associated with the eccentric contractions may influence the activity of motoneurons for synergistic muscles (24, 25). Such mechanisms can also enhance the mechanical output during the subsequent concentric contractions. In the present study, however, stretches and subsequent releases were done after the isometric force reached the level of maximal voluntary contraction, so that the eccentric contractions presumably caused no detectable change in the iEMG from the agonist muscle during the following concentric contractions. However, the possibility of increased activity in synergistic muscles needs further examination.
The present results for the elbow flexor muscles may not be applied directly to the whole body movements that are composed of coordinated contractions of numerous muscle groups with a variety of structural and contractile properties. For instance, the role played by the SEC may be more important in muscles with longer tendons, such as plantar flexors. Indeed, storage and reutilization of elastic energy by Achilles tendon have been shown to be involved in hopping movements in humans and other mammals (2, 17). The use of the stretch-shortening cycle of the SEC would make this particular type movement more energy efficient, because the length changes of the muscle fibers would be so small that they would not themselves produce large mechanical work. In addition, this elastic energy may be used in more complex movements involving the planter flexion, not only for saving energy but also for adding it to the mechanical work produced by other muscles and consequently gaining higher performance. However, experiments on drop-jump movements of humans (plyometric actions) have shown the presence of an optimal drop distance (and thus the optimal amount of negative work) to perform the highest jump (22), implying that the mechanism shown in the present study can also operate in much more complex movements. In relation to sports, the presence of such an optimal eccentric force would be of particular importance, because this suggests that an eccentric countermovement preceding a concentric action should be taken at an appropriate velocity and deceleration rate to gain the highest performance.
FOOTNOTES
Address for reprint requests: N. Ishii, Dept. of Life Sciences, Graduate School of Arts and Sciences, Univ. of Tokyo, Komaba Tokyo 153, Japan (E-mail: ishii{at}idaten.c.u-tokyo.ac.jp).
Received 30 December 1996; accepted in final form 26 June 1997.
REFERENCES
| 1. | Abbot, B. C., and X. M. Aubert. The force exerted by active striated muscle during and after change of length. J. Physiol. (Lond.) 117: 77-86, 1952. |
| 2. | Alexander, R. M. The mechanics of jumping of a dog. J. Zool. Lond. 173: 549-573, 1974. |
| 3. | Asmussen, E., and F. Bonde-Petersen. Storage of elastic energy in skeletal muscles in man. Acta Physiol. Scand. 91: 385-392, 1974[Medline]. |
| 4. | Avis, F. J., H. Toussaint, P. A. Huijing, and G. A. Van Ingen Schenau. Positive work as a function of eccentric load in maximal leg extension movements. Eur. J. Appl. Physiol. 55: 562-568, 1986. |
| 5. | Basmajian, J. V., and C. J. Deluca. EMG signal amplitude and force. In: Muscle Drive (5th ed.). Baltimore, MD: Williams and Wilkins, 1985, p. 187-200. |
| 6. | Bigland, B., and O. C. J. Lippold. The relation between force, velocity and integrated electrical activity in human muscles. J. Physiol. (Lond.) 123: 214-224, 1954. |
| 7. | Bosco, C., and P. V. Komi. Potentiation of the mechanical behaviour of the human skeletal muscle through prestretching. Acta Physiol. Scand. 106: 467-472, 1979[Medline]. |
| 8. | Cavagna, G. A., and G. Citterio. Effect of stretching on elastic characteristics and the contractile component of frog striated muscle. J. Physiol. (Lond.) 239: 1-14, 1974. |
| 9. |
Cavagna, G. A.,
B. Dusman,
and
R. Margaria.
Positive work done by a previously stretched muscle.
J. Appl. Physiol.
24:
21-32,
1968 |
| 10. | Cnockaert, J. C., E. Pertuzon, F. Goubel, and F. Lestienne. Series elastic component in normal human muscles. In: Biomechanics VI-A, edited by E. Asmussen, and K. Jorgensen. Baltimore, MD: University Park, 1978, vol. 2A, p. 68-72. (Int. Ser. Biomech.) |
| 11. |
De Haan, A.,
G. J. Van Ingen Schenau,
G. J. Ettema,
P. A. Huijing,
and
M. A. N. Lodder.
Efficiency of rat medial gastrocnemius muscle in contractions with and without an active prestretch.
J. Exp. Biol.
141:
327-341,
1989 |
| 12. | Deleze, J. B. The mechanical properties of the semitendinosus muscle at lengths greater than its length in the body. J. Physiol. (Lond.) 158: 154-164, 1961. |
| 13. |
Edman, K. A. P.,
G. Elzinga,
and
M. I. M. Noble.
Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibers.
J. Physiol. (Lond.)
281:
139-155,
1978.
|
| 14. |
Enoka, R. M.
Eccentric contractions require unique activation strategies by the nervous system.
J. Appl. Physiol.
81:
2339-2346,
1996 |
| 15. |
Ettema, G. J. C.,
A. J. Van Soest,
and
P. A. Huijing.
The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions.
J. Exp. Biol.
154:
121-136,
1990.
|
| 16. |
Ford, L. E.,
A. F. Huxley,
and
R. M. Simmons.
Tension responses to sudden length change in stimulated frog muscle fibres near slack length.
J. Physiol. (Lond.)
269:
441-515,
1977 |
| 17. | Fukashiro, S., and P. V. Komi. Joint movement and mechanical power flow of the lower limb during vertical jump. Int. J. Sports Med. 8, Suppl.: 15-21, 1987. |
| 18. | Gulch, R. W., P. Fuchs, A. Geist, M. Eison, and H.-C. Heitokamp. Eccentric and posteccentric contractile behaviour of skeletal muscle: a comparative study in frog single fibres and in humans. Eur. J. Appl. Physiol. 63: 323-329, 1991. |
| 19. | Ishii, N., T. Tsuchiya, and S. Sugi. An in vitro motility assay system retaining the steady-state force-velocity characteristics of muscle fibers under positive and negative loads. Biochim. Biophys. Acta 1319: 155-162, 1997. |
| 20. | Kawakami, Y., K. Nakazawa, T. Fujimoto, D. Nozaki, M. Miyashita, and T. Fukunaga. Specific tension of elbow flexor and extensor muscles based on magnetic resonance imaging. Eur. J. Appl. Physiol. 68: 139-147, 1994. |
| 21. | Komi, P. V. Measurement of the force-velocity relationship in human muscle under concentric and eccentric contractions. In: Medicine and Sport. Biomechanics III. Basel, Switzerland: Karger, 1973, vol. 8, p. 224-229. |
| 22. | Komi, P. V., and C. Bosco. Utilization of stored elastic energy in leg extensor muscles by men and women. Med. Sci. Sports Exercise 10: 261-265, 1978. |
| 23. |
Nardone, A.,
C. Romano,
and
M. Schieppati.
Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles.
J. Physiol. (Lond.)
395:
363-381,
1988 |
| 24. | Nakazawa, K., Y. Kawakami, T. Fukunaga, H. Yano, and M. Miyashita. Differences in activation patterns in elbow flexor muscles during isometric, concentric, and eccentric contractions. Eur. J. Appl. Physiol. 66: 214-220, 1993. |
| 25. | Schieppati, M., F. Valenza, and M. Rezzonico. Motor unit recruitment in human biceps and brachioradialis muscles during lengthening contractions. Eur. J. Neurosci., Suppl. 4: 303, 1991. |
| 26. |
Sugi, H.
Tension changes during and after stretch in frog muscle fibers.
J. Physiol. (Lond.)
225:
237-253,
1972 |
| 27. | Sugi, H., Y. Amemiya, and H. Hashizume. Time-resolved X-ray diffraction from frog skeletal muscle during an isotonic twitch under a small load. Proc. Jpn. Acad. 54B: 559-564, 1978. |
| 28. |
Sugi, H.,
and
T. Tsuchiya.
Enhancement of mechanical performance in frog muscle fibres after quick increases in load.
J. Physiol. (Lond.)
319:
239-252,
1981 |
| 29. |
Sugi, H.,
and
T. Tsuchiya.
Isotonic velocity transients in frog muscle fibres following quick changes in load.
J. Physiol. (Lond.)
319:
219-238,
1981 |
| 30. |
Sugi, H.,
and
T. Tsuchiya.
Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibers.
J. Physiol. (Lond.)
407:
215-229,
1988 |
| 31. | Westing, S. H., and A. Thorstensson. Muscle activation during maximal voluntary eccentric and concentric knee extension. Eur. J. Appl. Physiol. 62: 104-108, 1991. |
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ABSTRACT
