Model of muscle-tendon interaction during frog semitendinosis fixed-end contractions

Abstract

A structural model was developed to explain sarcomere shortening at the expense of tendon lengthening in the frog semitendinosis (ST) muscle-tendon system. The model was based on the data of Lieber et al. [ Am. J. Physiol. 261, C86–C92 (1991)], who determined the relationship between the sarcomere length, tendon load (as a fraction of maximum isometric tension) and tendon, bone-tendon junction (BTJ), and aponeurosis strain. The model was generated assuming a finite time-course of cross-bridge attachment [Huxley, Prog. Biophys. 7, 255–318 (1957)], an ideal sarcomere length-tension relationship [Gordon et al., J. Physiol. 184, 170–192 (1966)] and an ideal force-velocity relationship [Katz, J. Physiol. 96, 45–64 (1939); Edman, J. Physiol. 291, 143–159 (1979)]. Functionally, sarcomeres operated on three distinct regions of the length-tension curve: (1) regions where the muscle force decreased as sarcomeres shortened (the shallow and steep ascending limbs); (2) regions where the muscle force increased as sarcomeres shortened and there was little passive tension (descending limb, where sarcomere length ≤3.0 μm); and (3) regions where the muscle force increased as sarcomeres shortened and there was a significant passive tension (descending limb where sarcomere length >3.0 μm). Using such a physiological model, it was found that the effect of tendon compliance was to ‘skew’ the sarcomere length-tension curve to the right and to increase the operating range of the muscle-tendon unit. Thus, maximum tension in the muscle occurred at an active sarcomere length of 2.0–2.2 μm, whereas in the muscle-tendon system, the maximum tension occurred at a longer resting sarcomere length of about 2.5 μm. The degree to which the tendon affected the muscle system depended on its material properties and dimensions. These data suggest that tendons are not merely rigid links connecting muscles to bones, but impart distinct properties to the muscular system.