Residual force enhancement after stretch in striated muscle. A consequence of increased myofilament overlap? - PubMed (original) (raw)

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Residual force enhancement after stretch in striated muscle. A consequence of increased myofilament overlap?

K A P Edman. J Physiol. 2012.

Abstract

When skeletal muscle is stretched above optimal sarcomere length during tetanic activity there is an increase in force that stays above the isometric force level throughout the activity period. This long-lasting increase in contractile force, generally referred to as 'residual force enhancement after stretch' (FE(resid)), has been studied in great detail in various muscle preparations over more than half a century. Substantial evidence has been presented to show that non-uniform sarcomere behaviour plays a major part in the development of FE(resid). However, in a great number of recent studies the role of sarcomere non-uniformity has been challenged and alternative mechanisms have instead been proposed to explain the increase in force such as enhancement of cross-bridge function and/or strengthening of parallel elastic elements along the muscle fibres. This article presents a short review of the salient features of FE(resid) and provides evidence that non-uniform sarcomere behaviour is indeed likely to play a major role in the development of FE(resid). Electron microscopical studies of fibres rapidly fixed after active stretch demonstrate that, dispersed in the preparation, there are assymetrical length changes within the two halves of myofibrillar sarcomeres resulting in greater filament overlap in one half of the sarcomere than in the opposite sarcomere half. Sarcomere halves with increased filament overlap will consequently be in a situation where they are able to produce a greater force than that recorded in the isometric control. Weaker regions in series will be able to keep the enhanced force by recruitment of elastic elements.

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Figures

Figure 1

Figure 1. Force enhancement by stretch during tetanus of a single muscle fibre at two different sarcomere lengths (S.L.)

A, at optimal S.L. and B, on the descending limb of the length–tension relation. Records with active stretch superimposed on ordinary isometric tetanus recorded at the S.L. where the stretch ended. Note that the same force level is finally reached in both records in A, whereas force after stretch remains above the isometric control throughout the activity period in B. Records compiled in Photoshop from scanned analogue oscilloscope recordings from study performed in collaboration with G. Elzinga and M. I. M. Noble.

Figure 2

Figure 2. Relation between slow component of force enhancement during stretch and residual force enhancement after stretch plotted from seven isolated muscle fibres

Inset, tetanus with force enhancement by stretch superimposed on control tetanus to illustrate the approach used for measuring the slow component of force enhancement during stretch (Slow) and the residual force enhancement after stretch (Residual). Values from a given fibre denoted by the same symbols. Line, linear regression based on all data points (P < 0.0001, _n_= 53). Reproduced from Edman & Tsuchiya (1996).

Figure 3

Figure 3. Relation between force enhancement after stretch (_F_E) and strain of damped elastic elements (_S_E) recorded by quick-release technique in whole fibres and marked segments of intact fibres

For details, see Edman & Tsuchiya (1996). Continuous line, linear regression based on all data points: _S_E= 0.200 _F_E+ 8.65. Reproduced from Edman & Tsuchiya (1996).

Figure 4

Figure 4. Muscle fibre rapidly fixed in mercuric chloride at 2.2–2.5 μm after 10% stretch during tetanic stimulation

Note irregularities of Z-line and M-line structures with marked differences in filament overlap between opposite halves of sarcomeres. With kind permission from Springer Science+Business Media: Brown & Hill (1991), J Muscle Res Cell Motil 12, 171–182.

Figure 5

Figure 5. Muscle fibre stretched from an overall sarcomere length of 2.50 μm to 2.65 μm during the plateau of a fused tetanus

Fibre instantaneously frozen at the end of the stretch ramp (for further technical details, see Edman & Lou, 1992). Note irregularities of Z-line and M-line structures with marked differences in filament overlap between opposite halves of sarcomeres. From study in collaboration with F. Lou. Scale bar, 1 μm.

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References

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