Muscle shortening velocity depends on tissue inertia and level of activation during submaximal contractions

In order to perform external work, muscles must do additional internal work to deform their tissue, and in particular, to overcome the inertia due to their internal mass. However, the contribution of the internal mass within a muscle to the mechanical output of that muscle has only rarely been studied. Here, we use a dynamic, multi-element Hill-type muscle model to examine the effects of the inertial mass within muscle on its contractile performance. We find that the maximum strain-rate of muscle is slower for lower activations and larger muscle sizes. As muscle size increases, the ability of the muscle to overcome its inertial load will decrease, as muscle tension is proportional to cross-sectional area and inertial load is proportional to mass. Thus, muscles that are larger in size will have a higher inertial cost to contraction. Similarly, when muscle size and inertial load are held constant, decreasing muscle activation will increase inertial cost to contraction by reducing muscle tension. These results show that inertial loads within muscle contribute to a slowing of muscle contractile velocities (strain-rates), particularly at the submaximal activations that are typical during animal locomotion.

[1]  Syn Schmitt,et al.  Spreading out Muscle Mass within a Hill-Type Model: A Computer Simulation Study , 2012, Comput. Math. Methods Medicine.

[2]  I. Johnston,et al.  Muscle function in locomotion , 1988, Nature.

[3]  R. Close Dynamic properties of fast and slow skeletal muscles of the rat during development , 1964, The Journal of physiology.

[4]  A. A. Biewener,et al.  The effect of fast and slow motor unit activation on whole-muscle mechanical performance: the size principle may not pose a mechanical paradox , 2014, Proceedings of the Royal Society B: Biological Sciences.

[5]  C. Reggiani,et al.  Force‐velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle. , 1991, The Journal of physiology.

[6]  The effects of asymmetric length trajectories on the initial mechanical efficiency of mouse soleus muscles , 2012, Journal of Experimental Biology.

[7]  A. Hill First and Last Experiments in Muscle Mechanics , 1970 .

[8]  F. Zajac Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. , 1989, Critical reviews in biomedical engineering.

[9]  Walter Herzog,et al.  Theoretical Models of Skeletal Muscle: Biological and Mathematical Considerations , 1998 .

[10]  James M Wakeling,et al.  Motor unit recruitment patterns 1: responses to changes in locomotor velocity and incline , 2008, Journal of Experimental Biology.

[11]  J. L. Leeuwen Muscle Function in Locomotion , 1992 .

[12]  S. Baylor,et al.  Sarcoplasmic reticulum calcium release compared in slow‐twitch and fast‐twitch fibres of mouse muscle , 2003, The Journal of physiology.

[13]  R. Marsh,et al.  The effects of length trajectory on the mechanical power output of mouse skeletal muscles. , 1997, The Journal of experimental biology.

[14]  James M. Wakeling,et al.  Modelling muscle forces: from scaled fibres to physiological task-groups , 2011 .

[15]  R. Josephson,et al.  The consequences of fibre heterogeneity on the force-velocity relation of skeletal muscle. , 1988, Acta physiologica Scandinavica.

[16]  R. Marsh,et al.  Thermal dependence of contractile properties of skeletal muscle from the lizard Sceloporus occidentalis with comments on methods for fitting and comparing force-velocity curves. , 1986, The Journal of experimental biology.

[17]  R. McN. Alexander,et al.  Mechanical stresses in fast locomotion of buffalo (Syncews coffer) and elephant (Loxodonta africana) , 2009 .