Tension responses of frog skeletal muscle fibres to rapid shortening and lengthening steps.

Bressler, Bernard; Dusik, Laureen A.; Menard, Michael R.

doi:10.1113/jphysiol.1988.sp017022

Cited by 15 publications

(8 citation statements)

References 13 publications

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“…The most important and well known of these, which is shown in Fig. 1 A, is that after electrical stimulation of frog skeletal muscle at 1-50C, stiffness, and presumably crossbridge attachment, precedes force development by 15-20 ms (Bressler and Clinch, 1974;Cecchi et al, 1982Cecchi et al, , 1987Tamura et al, 1982;Schoenberg and Wells, 1984;Ford et al, 1986;Kress et al, 1986;Bagni et al, 1988;Bressler et al, 1988). A second finding also not well understood at present concerns the different relationships between stiffness and force during the rise of a tetanus, during the redevelopment of Force FIGURE 3 Force versus stiffness during the rising phase of twitches generated at different temperatures.…”

Section: Resultsmentioning

confidence: 99%

“…While the resting and activated condition have individually been well explained, the transition between rest and activation has not been so well explained. Stiffness and x-ray diffraction measurements suggest that after electrical stimulation of frog skeletal muscle at 0°C, crossbridge attachment precedes force generation by -15 ms (Bressler and Clinch, 1974;Cecchi et al, 1982;Tamura et al, 1982;Schoenberg and Wells, 1984;Ford et al, 1986;Kress et al, 1986;Bagni et al, 1988;Bressler et al, 1988). Whereas the model of Huxley and Simmons (1971) predicts a lag between stiffness and force, the predicted lag is only on the order of a millisecond.…”

Section: Introductionmentioning

confidence: 99%

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A model of force production that explains the lag between crossbridge attachment and force after electrical stimulation of striated muscle fibers

Bagni¹,

Cecchi²,

Schoenberg³

1988

Biophysical Journal

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Whereas the mechanical behavior of fully activated fibers can be explained by assuming that attached force-producing crossbridges exist in at least two configurations, one exerting more force than the other (Huxley A. F., and R. M. Simmons. 1971. Nature [Lond.]. 233:533-538), and the behavior of relaxed fibers can be explained by assuming a single population of weakly binding rapid-equilibrium crossbridges (Schoenberg, M. 1988. Biophys. J. 54:135-148), it has not been possible to explain the transition between rest and activation in these terms. The difficulty in explaining why, after electrical stimulation of resting intact frog skeletal muscle fibers at 1-5 degrees C, force development lags stiffness development by more than 15 ms has led a number of investigators to postulate additional crossbridge states. However, postulation of an additional crossbridge state will not explain the following three observations: (a) Although the lag between force and stiffness is very different after stimulation, during the redevelopment of force after an extended period of high velocity shortening, and during relaxation of a tetanus, nonetheless, the plots of force versus stiffness in each of these cases are approximately the same. (b) When the lag between stiffness and force during the rising phase of a twitch is changed nearly fourfold by changing temperature, again the plot of force versus stiffness remains essentially unchanged. (c) When a muscle fiber is subjected to a small quick length change, the rate constant for the isometric force recovery is faster when the length change is applied during the rising phase of a tenanus than when it is applied on the plateau. We have been able to explain all the above findings using a model for force production that is similar to the 1971 model of Huxley and Simmons, but which makes the additional assumption that the force-producing transition envisioned by them is a cooperative one, with the back rate constant of the force-producing transition decreasing as more crossbridges attach.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A model of force production that explains the lag between crossbridge attachment and force after electrical stimulation of striated muscle fibers

Bagni¹,

Cecchi²,

Schoenberg³

1988

Biophysical Journal

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“…Actually, for tensions up to 3 To the T1 relation exhibited a small upward concavity, which represents a deviation from the linear behaviour in the direction opposite to that expected for yielding of the cross-bridges or a structure in series. An increase in stiffness going from step release to step stretches has been described by Ford et al (1977) and Bressler, Dusik & Menard (1988).…”

Section: Elasticity Of Tetanized Fibres In the Region Of High Forcesmentioning

confidence: 99%

The contractile response during steady lengthening of stimulated frog muscle fibres.

Lombardi

Piazzesi

1990

The Journal of Physiology

288

358

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SUMMARY1. Steady lengthenings at different velocities (0-025-1.2 ,tm/s per half-sarcomere; temperature 2-5-5°C) were imposed on isolated frog muscle fibres at the isometric tetanus plateau by means of a loudspeaker motor. The lengthening at the sarcomere level was measured by means of a striation follower either in fixed-end or in lengthclamp mode. The force response was measured by a capacitance gauge transducer (resonance frequency 50 kHz). Preparations showing gross non-homogeneity during lengthening were excluded.2. A steady tension was in all cases reached after about 20 nm per half-sarcomere of lengthening. Tension during this steady phase rose with speed of elongation up to 0-25-0-4 #sm/s per half-sarcomere, when tension was 1-9-2 times isometric tetanic force (TO). Further increase in speed produced only very little increase in the steady tension.3. During the transitory phase, before steady tension was reached, the tension rose monotonically if speed of lengthening was less than 0-25-0-3 ,um/s per halfsarcomere; at higher speed the tension rose above the steady level, reaching a peak when extension was 10-14 nm per half-sarcomere, and then fell to the steady level. Tension at the peak continued to rise with speed of lengthening above 0 3 ,um/s per half-sarcomere.4. During the tension rise within the transitory phase of force response the segment elongated at a speed 15-20% lower than that imposed on the whole fibre, as a consequence of-tendon compliance.5. During the steady phase, non-homogeneity of lengthening speed began above a speed of lengthening which varied from fibre to fibre. At speeds below this value, segments elongated at the same speed as that imposed on the fibre.6. Tension responses to large step stretches (up to 12 nm per half-sarcomere), applied at the plateau of isometric tetanus, showed that the instantaneous elasticity of contractile machinery is not responsible for the limit in force attained with highspeed lengthening.7. Instantaneous stiffness was determined during the steady state of force response by superposing small steps (< 15 nm per half-sarcomere) on steady lengthening at different velocities. Stiffness was 10-20% larger during lengthening MS 8214 V. LOMBARDI AND G. PIAZZESI than at the plateau of isometric tetanus and remained practically constant, independent of lengthening velocity, in the range of velocities used.8. The results indicate that steady lengthening of a tetanized fibre induces a crossbridge cycle characterized by fast detachment of the cross-bridge extended beyond a critical level. Reattachment of cross-bridges detached in this way is also very rapid. 9. A model of contraction, including separate steps for cross-bridge attachment, force generation and detachment, was found to be compatible with the experimental force-and stiffness-velocity relations. In the model, detachment of extended crossbridges occurs at an early stage of the cycle. The rate constant of this detachment process increases sharply beyond a critical amount of cross-bridge strain; reattac...

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“…The response occurs at reduced metabolic cost (Infante et al 1964; Curtin & Davies, 1973; Linari et al 2003) and is characteristic of eccentric contractions, a condition that is quite common in normal life, such as when the extensor muscles of the legs have to resist the momentum of the body landing at the end of a jump. Step or ramp stretches superposed on isometric contraction produce increases in the stiffness of muscle fibres (Bressler et al 1988; Sugi & Tsuchiya, 1988; Lombardi & Piazzesi, 1990; Mantovani et al 1999; Linari et al 2000 a ). When the stretch is imposed within the range of sarcomere lengths corresponding to the plateau of the force–length relation (2–2.25 μm for frog muscle fibres (Edman, 1966; Gordon et al 1966)) and under the condition that the sarcomere homogeneity along the muscle fibre is preserved, recruitment of elastic structures in parallel to the contractile elements of the sarcomere (Edman et al 1982; Morgan, 1990, 1994; Noble, 1992; Edman & Tsuchiya, 1996; Herzog & Leonard, 2002; Linari et al 2003) can be excluded.…”

Section: Introductionmentioning

confidence: 99%

The mechanism of the resistance to stretch of isometrically contracting single muscle fibres

Fusi

Reconditi

Linari

et al. 2010

The Journal of Physiology

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Rapid attachment to actin of the detached motor domain of myosin dimers with one motor domain already attached has been hypothesized to explain the stretch-induced changes in X-ray interference and stiffness of active muscle. Here, using half-sarcomere mechanics in single frog muscle fibres (2.15 μm sarcomere length and 4• C), we show that: (1) an increase in stiffness of the half-sarcomere under stretch is specific to isometric contraction and does not occur in rigor, indicating that the mechanism of stiffness increase is an increase in the number of attached motors; (2) 2 ms after 100 μs stretches (amplitude 2-8 nm per half-sarcomere) imposed during an isometric tetanus, the stiffness of the array of myosin motors in each half-sarcomere (e m ) increases above the isometric value (e m0 ); (3) e m has a sigmoidal dependence on the distortion of the motor domains ( z) attached in isometric contraction, with a maximum ∼2 e m0 for a distortion of ∼6 nm; e m is influenced by detachment of motors at z > 6 nm; (4) at the end of the 100 μs stretch the relation between e m /e m0 and z lies slightly but not significantly above that at 2 ms. These results support the idea that stretch-induced sliding of the actin filament distorts the actin-attached motor domain of the myosin dimers away from the centre of the sarcomere, providing the steric conditions for rapid attachment of the second motor domain. The rate of new motor attachment must be as high as 7.5 × 10 4 s −1 and explains the rapid and efficient increase of the resistance of active muscle to stretch. Abbreviations hs, half-sarcomere; T 0 , isometric tetanic force; e, half-sarcomere stiffness; e 0 , half-sarcomere stiffness at T 0 ; C f , myofilament compliance; e m , motor array stiffness; e m0 , motor array stiffness at T 0 ; z, distortion of the myosin motor; M3, third order of the myosin-based meridional reflections; I M3 , intensity of M3; R M3 , ratio of the intensities of the higher and lower angle peaks of M3.

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Tension responses of frog skeletal muscle fibres to rapid shortening and lengthening steps.

Cited by 15 publications

References 13 publications

A model of force production that explains the lag between crossbridge attachment and force after electrical stimulation of striated muscle fibers

A model of force production that explains the lag between crossbridge attachment and force after electrical stimulation of striated muscle fibers

The contractile response during steady lengthening of stimulated frog muscle fibres.

The mechanism of the resistance to stretch of isometrically contracting single muscle fibres

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