History dependent force properties of skeletal muscle: in vitro, in situ and in vivo considerations
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1 History dependent force properties of skeletal muscle: in vitro, in situ and in vivo considerations Introduction W. Herzog, H.D. Lee, J. Wakeling, R. Schachar, and T. Leonard Faculty of Kinesiology, University of Calgary, Calgary, AB, Canada The observation that force production in skeletal muscle is history-dependent has been made on many occasions. For example, Abbott and Aubert (1952) demonstrated convincingly that the steady-state force following muscle shortening is smaller and following stretching is greater than the purely isometric forces at the corresponding muscle length. These phenomena have been termed force depression and force enhancement, respectively. Although history-dependent phenomena have been accepted as important properties in skeletal muscle force production, the mechanisms underlying these properties are not understood. Specifically, force enhancement following muscle stretch has been associated tentatively with the development of sarcomere length nonuniformities that develop on the descending limb of the force-length relationship exclusively. The sarcomere length non-uniformity theory has received virtually unanimous support in the scientific literature despite its obvious shortcomings and the indirect nature of its experimental support. The basic explanation for force enhancement following muscle stretch is illustrated schematically in Figure 1. The idea is that relatively uniform sarcomere lengths exist prior to muscle stretching. However, when a muscle is stretched on the descending limb, sarcomere lengths are assumed to diverge and so cause force enhancement. This idea is based on the notion proposed by Hill (1953) that sarcomere length and force production is unstable on the descending limb of the force-length relationship. Based on the sarcomere length non-uniformity theory, the following testable hypotheses can be put forward: (a) force enhancement can only occur on the descending limb of the force-length relationship (that is in areas where the active isometric force decreases with increasing muscle length) (b) force enhancement cannot exceed the isometric forces measured at the length from which the stretch was initiated (because sarcomere length cannot shorten while the muscle or fibre is stretched substantially) (c) force enhancement cannot exceed the maximal isometric force achieved at the plateau of the force-length relationship (this is only possible if another factor than sarcomere length non-uniformity contributes to the force enhancement). Purpose The purpose of this talk is to provide evidence for rejection of all three proposed hypotheses. Therefore, we will argue that the sarcomere length non-uniformity theory can at best be part of the explanation for force enhancement, but definitely not its sole mechanism. Furthermore, we will propose an alternative theory, based on most recent observations in experiments on in vivo human adductor pollicis, in situ cat soleus and semitendinosus, and in vitro single fibres from frog tibialis anterior. Methods
2 We performed experiments of muscle and fibre stretching on the ascending and descending limbs of the force length relationship using in vivo human adductor pollicis, in situ cat soleus and semitendinosus, and in vitro single fibres from frog. Adductor pollicis experiments were made throughout the anatomical range using artificial electrical nerve stimulation and maximal voluntary contractions. Cat soleus experiments were performed across the entire physiological range of motion, and in addition on the lower parts of the descending limb of the forcelength relationship. Stimulation was performed using electrodes implanted on the tibial nerve. Cat semitendinosus experiments were exclusively performed on the descending limb of the force-length relationship. Frog fibre experiments were performed on mechanically isolated and intact fibres from the tibialis anterior of rana pipiens. Stretching of all preparations was performed for a variety of magnitudes and speeds. Details of these procedures might be obtained from Herzog and Leonard (1997), Lee et al (2001) and Wakeling et al (2001). Results Regarding the first hypothesis, we found in cat soleus that force enhancement could be obtained on the ascending limb of the force-length relationship where sarcomere length non-uniformities are not supposed to occur (Figure 2). Therefore, the first hypothesis was rejected. Regarding the second hypothesis, we observed, in cat semitendinosus and single fibres from frog tibialis anterior that force enhancement exceeded the isometric force at the initial length of the muscle (Figure 3). Therefore, the second hypothesis was rejected. Interestingly, this result has the additional implication that force production on the descending limb must be stable (Zahalak, 1997; Allinger et al 2000), and not unstable, as had been assumed for virtually half a century (Hill, 1953). Regarding the third hypothesis, we found force enhancement that exceeded the isometric plateau force by 5-8% (Figure 4), therefore the third hypothesis was rejected as well. This result has the additional implication that force enhancement is associated with a mechanism that either enhances the active force producing ability of the contractile proteins, or is caused by a passive element of the muscle. We found direct evidence of the latter (a passive component of force enhancement) in experiments on cat soleus and semitendinosus (Figure 5). Discussion and Conclusions From the results presented above from a variety of experimental preparations, we conclude that force enhancement following muscle/fibre stretching cannot be associated exclusively with the sarcomere length nonuniformity theory. It appears that force enhancement has an active and a passive component. The origin of the active component cannot be explained at present. The origin of the passive component might be in the giant structural protein titin. Titin is a molecular spring whose stiffness might be changed by disease (Wu et al 2001) or by enzymatic treatment (Trok and Bennet 2001). If titin could be shown to change its stiffness as a function of contractile state (i.e. active vs. passive; and eccentric contraction vs. isometric/concentric contraction), the proposed theory would be much stronger. However, such evidence is not available at present. We further conclude that force production on the descending limb is mostly stable. This conclusion follows directly from the result that the long-term, steady state force enhancement following muscle stretching is greater than the purely isometric force at the initial muscle length (i.e. the length at which the stretch was initiated). This is in contradiction with the suggestions made by Hill (1953), who voiced the intuitively appealing idea that sarcomere length is unstable on the descending limb because of the negative slope of the isometric force-length
3 relationship. If the dynamic relationship also had a negative slope, Hill=s(1953) argument would definitely be correct. However, Hill (1953), as so many scientists today, assumed that the force-length relationship is a continuous property, which it is not. The force enhancement provides positive stiffness to most experimental preparations and for most contractile conditions, therefore, dynamically contracting muscle exhibits hardening properties on the descending limb of the force-length relationship, thus force production is stable. References 1. Abbott, B.C. & Aubert, X.M. J Physiol 117:77-86, Allinger, T.L., Herzog, W., ter Keurs H.E.D.J., & Epstein, M. ed. Herzog, W., John Wiley and Sons, Chichester, pp , Herzog, W. & Leonard, T.R. J. Biomech. 30(9): , Hill, A.V. Proc Royal Soc London 141: , Lee, H.-D., Dinning, H.J., & Herzog, W. International Society of Biomechanics 2001 (accepted) 6. Trok, B.M. & Barnett, V.A. Biophys. J. 80(1), 275a Wakeling, J., Syme, D. & Herzog, W., Biophys. J. 80(1), 270a Wu, Y., Bell, S.P., LeWinter, M.M., and Granzier, H.L.M. Biophys. J. 80(1), 262a Zahalak, G.I. J Biomech. 30: , Acknowledgments NSERC of Canada Figures Figure 1: Schematic illustration of force enhancement according to the sarcomere length nonuniformity theory
4 Figure 2: Force enhancement on the ascending limb of the force-length relationship in cat soleus Figure 3: Force enhancement following stretch exceeds the corresponding isometric force at a length from which stretching was initiated
5 Figure 4: Force enhancement above the isometric plateau forces for stretches of frog single fibres on the descending limb of the force-length relationship Figure 5: Evidence of passive force enhancement following active (but not passive) muscle stretching in cat soleus
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