Response to ‘There is no experimental evidence for non-linear myofilament elasticity in skeletal muscle’

Abstract

In his Correspondence article (p. 658), Massimo Reconditi discusses an alternative interpretation of previously presented results (Edman, 2009) concerning the nature of myofilament elasticity in striated muscle. In response to Reconditi (Reconditi, 2010), I should like to make the following remarks.A pertinent finding in the study described by Edman (Edman, 2009) is the sarcomere length dependence of the measured fibre stiffness. The instantaneous stiffness was measured during tetanic stimulation while the active force was kept at a given level by load-clamp control within the range 0.4-0.7 of maximum tetanic force. The results showed that the measured stiffness was invariably lower as the sarcomere length was increased above optimal length, 2.20 μm. This observation provides evidence that the myofilament compliance is indeed lower in the overlap region than in the region outside overlap where there is no interaction with the myosin bridges. The actual compliance of the filaments in the overlap region during tetanic activity cannot be assessed at the present time except that it must be effectively lower than that in the free portions of the filaments. In Edman (Edman, 2009), the assumption is made that the filaments in the overlap region, i.e. the portions involved in cross-bridge formation, are incompliant. On this basis, the results presented in fig. 3 of Edman (Edman, 2009) do suggest that the myofilaments in frog striated muscle have the character of a non-linear spring. To my knowledge, there is no clear-cut evidence that the myofilaments in the overlap zone are compliant in the particular way proposed by Reconditi (Reconditi, 2010), which would lead to a basically different conclusion from that reached in Edman (Edman, 2009). If a fraction of the filament compliance is actually assumed to reside in the overlap zone, this would provide lower values of the calculated myofilament stiffness than shown in fig. 4 of Edman (Edman, 2009), but the increase in myofilament stiffness with force would still hold true as illustrated.As pointed out in Edman (Edman, 2009), the myofilaments of the intact muscle fibre are quite complex structures in that they are surrounded by, and interwoven with, a number of auxiliary filaments that make up the cytoskeleton. These structures may be regarded as an integral part of the myofilament elasticity measured in intact muscle or intact muscle fibres and this will hold true irrespective of the measuring technique used [see Discussion and further references in Edman (Edman, 2009)]. The complexity of the myofilament structure may well be thought to be associated with non-linear elastic properties like those observed in, for example, muscle tendons (Cleworth and Edman, 1972; Edman and Josephson, 2007). Results of previous investigations based on mechanical measurements (Higuchi et al., 1995) and X-ray diffraction studies (Griffiths et al., 2006) provide evidence in favour of this view, thus supporting the conclusion reached in Edman (Edman, 2009). It is worth pointing out in this connection that no concrete evidence has been presented to show that the myofilaments in intact muscle fibres behave as Hookean springs.