On lateral transmission of force in active intact muscle

Abstract

The paper by Ramaswamy et al. (2011) in this issue of The Journal of Physiology, reports some interesting experimental data on force measurements from muscles of wild and mdx-dystrophic mice and from young and old rats; in particular, a comparison is made between the longitudinally transmitted force and the laterally transmitted force of intact muscle activated to different force levels. For a given muscle, different levels of active force development were obtained by changing the number of motor units activated by nerve stimulation. Basically, the proximal muscle tendon was fixed and the longitudinal (or axial) force was recorded in the conventional manner at the distal tendon. An unusual feature of the study is that a lateral (or radial) muscle force was also measured by a novel technique; it was measured (longitudinally) from the proximal tendon to a close-fitting plastic ring (the ‘yoke’) placed around the mid-belly of muscle and sutured to the muscle surface (the epimysium). The experimental force measurements made using this apparatus and methodologies (see Fig. 2B and Fig. 3 in the paper) showed that in normal (control) skeletal muscles (from wild mice and young rats), the longitudinal forces generated during different levels of activation are transmitted laterally to the epimysium with little or no decrement, similar to the original findings of Street (1983) from maximally activated, partially isolated, single fibres from frog muscle. In contrast, in muscles of mdx-dystrophic mice and very old rats the lateral transmission of force was impaired. The magnitude of the impairment in the lateral force transmission was similar to the loss of dystrophin expression in those muscles; this is in keeping with the notion that the dystrophin–glycoprotein complex (DGC) provides a structural link from the muscle fibre cytoskeleton to the extracellular matrix and that it is disrupted in the muscles of mdx mice and in very old rats. Clearly, such comparative data would be of value in demonstrating various structural changes that accompany dystrophy and ageing in muscle. However, a number of subsidiary but more general issues, some of which are indeed referred to in the paper, deserve further examination and clarification. Firstly, compared to force responses typically recorded at the distal tendon in standard mechanics experiments, the force responses appear rather distorted and slow when the ‘yoke apparatus’ is attached to the muscle (Fig. 2A in the paper) and it is not exactly clear why, although some fibre damage may have contributed. Secondly, the lateral force recording is made when the distal tendon was unfixed/unattached (Fig. 1 in the paper), so that fibres or fibre lengths between the yoke and distal tendon would have freely shortened and a substantial muscle volume moved towards the yoke on activation. Whether this may have exaggerated the measured lateral force transmission remains unclear. Given that active muscle force shows a characteristic dependence on initial muscle length, it would be useful to make recordings at different initial muscle lengths. Thirdly, the average muscle fibre length to muscle length ratios for these muscles were around 0.5, so that the lateral force recorded (longitudinally from the yoke) may have had a contribution from end-to-end transmission from some fibres that terminate at the muscle belly region. It would be useful to know any change in lateral force transmission when the yoke is attached to different positions along the proximal to distal tendon axis of muscle. To sum up, there have been many previous studies dealing with the issue of lateral force transmission in active muscle (see review by Huijing, 1999, also refs in Ramaswamy et al. 2011). However, the study by Ramaswamy et al. (2011) presents the first experimentally determined lateral force measurements from intact mammalian muscle; moreover, the paper presents interesting novel results related to differences in laterally transmitted forces between control and defective muscles. The novel method used for determining lateral force transmission raises some concerns and future studies are needed to clarify the importance of impaired lateral force transmission in dysfunctional muscles.