Elsevier

Journal of Biomechanics

Volume 49, Issue 7, 3 May 2016, Pages 1156-1161
Journal of Biomechanics

Force reduction induced by unidirectional transversal muscle loading is independent of local pressure

https://doi.org/10.1016/j.jbiomech.2016.02.053Get rights and content

Abstract

Transversal unidirectional compression applied to muscles via external loading affects muscle contraction dynamics in the longitudinal direction. A recent study reported decreasing longitudinal muscle forces with increasing transversal load applied with a constant contact area (i.e., leading to a simultaneous increase in local pressure). To shed light on these results, we examine whether the decrease in longitudinal force depends on the load, the local pressure, or both. To this end, we perform isometric experiments on rat M. gastrocnemius medialis without and with transversal loading (i) changing the local pressure from 1.1–3.2 N cm−2 (n=9) at a constant transversal load (1.62 N) and (ii) increasing the transversal load (1.15–3.45 N) at a constant local pressure of 2.3 N cm−2 (n=7). While we did not note changes in the decrease in longitudinal muscle force in the first experiment, the second experiment resulted in an almost-linear reduction of longitudinal force between 7.5±0.6% and 14.1±1.7%. We conclude that the observed longitudinal force reduction is not induced by local effects such as malfunction of single muscle compartments, but that similar internal stress conditions and myofilament configurations occur when the local pressure changes given a constant load. The decreased longitudinal force may be explained by increased internal pressure and a deformed myofilament lattice that is likely associated with the decomposition of cross-bridge forces on the one hand and the inhibition of cross-bridges on the other hand.

Introduction

The vast majority of muscle research examining muscle contraction and its influencing factors has been performed on isolated muscle preparations (e.g., research on the force–length (Gordon et al., 1966) and force–velocity relationships (Hill, 1938)). In real life, skeletal muscles are embedded within other muscles, connective tissue, and bones that possibly modify the muscle׳s force production along its line of action. This fact is important because changes in longitudinal muscle force alter joint torques and therefore potentially influence movement and control of the segment chain. External tensile forces can be transmitted via extramuscular connective tissue that has continuity with the muscle belly (Maas et al., 2001, Yucesoy et al., 2003). These external forces can deform the muscle, affecting, for example, sarcomere lengths and hence modifying the force-producing mechanism of the muscle (Yucesoy, 2010). The physiological relevance of these effects is disputed. Several studies have reported that such forces seem to be irrelevant within physiological boundaries at least for several muscles (Maas and Sandercock, 2008, Tijs et al., 2015). In contrast, other studies have reported substantial mechanical interaction between muscles in situ (Bernabei et al., 2015) and in vivo (Carvalhais et al., 2013, Huijing et al., 2011, Yaman et al., 2013). Furthermore, kinesio taping can influence passive muscle shape and architecture (Pamuk and Yucesoy, 2015) and change at least the initial conditions of a contraction. On the other hand, transversal compressive forces that do not necessarily require structural continuity with the muscle belly to be transmitted can lead to a decrease in longitudinal muscle force, and this decrease is of the same order of magnitude as the transversal load (Siebert et al., 2014b).

It seems plausible that muscles are compressed mainly in a transversal direction via interactions with their environment and by the action of neighboring muscles and bones. This loading condition deviates significantly from increased external steady pressure in all directions that has been shown to have almost no influence on longitudinal muscle force; the maximal isometric tension was depressed by ~1% per 100 N cm−2 (Geeves and Ranatunga, 1987). This finding is likely due to the fact that muscles are water-filled structures characterized by the property of volume constancy (Swammerdam, 1737). External transversal compression in largely one direction may occur rather locally, e.g., in the back and abdominal muscles when wearing lifting belts, in limb muscles when wearing ortheses, in the deltoideus when carrying a backpack, in the gluteus when cycling, or in shank muscles when wearing ski boots; on the other hand, external transversal compression may act on rather large fractions of the muscle surface, e.g., when stemming from neighboring muscles and bones during walking or running (e.g. in the quadriceps).

In a recent study, Siebert et al. (2014b) examined the influence of increasing unidirectional transversal muscle loading on longitudinal contraction dynamics using rat M. gastrocnemius medialis (GM). The muscle was loaded by a plunger in a transversal direction. During contraction, the muscle deformed and lifted the load. Compared with the unloaded contraction, increasing the transversal loads from 0.64 to 2.60 N resulted in a reduction of the rate of longitudinal force development (20–36%) as well as in an almost linear decrease of the longitudinal steady-state muscle force (5–13%) and the lifting height of the plunger (1.7–0.6 mm). Due to the chosen experimental design with a constant plunger contact area, increasing transversal loads corresponded to increasing the local transversal pressure from 1.3 to 5.3 N cm−2. These transversal pressures are of the same order of magnitude as those found in the human gluteus muscle during sitting (Linder-Ganz et al., 2007). However, these results prevent one from drawing conclusions as to whether local pressure effects are involved in generating the observed decrease in longitudinal muscle force.

High, local, unidirectional transversal pressures may lead to large local stresses and large deformations of the myofilament structure within adjacent muscle compartments that could hamper their effectiveness at longitudinal force production. In this case, one would expect a dependency of the decrease in longitudinal force on the local pressure associated with a constant external load. On the other hand, if the active muscle structure is stiff enough in the longitudinal direction and local deformations remain rather small, similar internal stresses may result regardless of the local pressure at a constant transversal load. Then, the decrease in longitudinal force would depend more on the transversal load than on the local transversal pressure. Determining these dependencies is important for further development and validation of simple, computationally inexpensive muscle models that can account for effects of two- or three-dimensional loading conditions of muscles (Siebert et al., 2012, Siebert et al., 2014a).

To examine whether longitudinal muscle force depends on load, local pressure, or both, we performed in situ experiments (i) varying the local transversal pressure at constant transversal load and (ii) increasing the transversal load while keeping the local pressure constant.

Section snippets

Experimental setup

The experiments were approved according to Section 8 of the German animal protection law (Tierschutzgesetz, BGBl I 1972, 1277). We performed the experiments on rat (Rattus norvegicus, Wistar) M. gastrocnemius medialis (GM; n=9, mGM=821±100 mg, mean±standard deviation (SD), Table 1). The experimental setup was described in detail previously in the literature, and we refer the interested reader to Siebert et al. (2014b) and Till et al. (2008).

Briefly, the rats were anaesthetized with sodium

Results

Unidirectional transversal muscle loading depressed the force time traces during isometric contractions (Fig. 1). In the experiments varying the local transversal pressure at a constant load, ΔFim was −8.0±1.2%, ΔRFD was −32.7±3.7%, and Δh was 1.1±0.3 mm (Fig. 2). Linear regression analyses revealed that local transversal pressure had a negligible influence on ΔFim, ΔRFD, and Δh (Fig. 2, Table 3) in these experiments. More specifically, the confidence intervals of the slopes of the linear

Discussion

Varying the local unidirectional transversal pressure at a constant load did not influence the longitudinal contraction dynamics (Fig. 1). When increasing the transversal load while keeping the local pressure constant, we observed an almost-linear decrease in the steady-state longitudinal force Fim (Fig. 3A). We can conclude that the observed longitudinal force reduction is induced exclusively by the transversal load and not by the local transversal pressure.

In our experiments, muscle fibers

Conclusion

Unidirectional transversal compression reduces longitudinal force development in skeletal muscles. The magnitude of this depression depends on the transversal load, not the local pressure associated with this load. This fact implies that the active muscle structure is relatively stiff compared with unidirectional transversal loads expected in everyday tasks. Possible mechanisms decreasing the longitudinal muscle force may be the internal pressure, the deformation of the myofilament grid leading

Conflict of interest statement

The authors of the present manuscript state that there were and are no conflicts of interest with relation to this article.

Acknowledgment

This work was supported by the “Deutsche Forschungsgemeinschaft” (DFG Grant SI841/2-3 to TS).

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