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History effect and timing of force production introduced in a skeletal muscle model

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Abstract

Skeletal muscle modelling requires a detailed description of muscular force production. We have performed a series of experiments on mouse skeletal muscles to give a basis for an improved description of the muscular force production. Our previous work introduced a force modification in isometric phases, which was based on the work performed by or on the muscle during transient-length-varying contractions. Here, state-space diagrams were used to investigate the timing aspects of the force production. These show a dominant exponential nature of the force development in isometric phases of the contractions, reached after a non-exponential phase, assumed as an activation or deactivation stage and not further analysed here. The time constants of the exponential functions describing isometric force redevelopment after length variations appear to be related to the one for an initial isometric contraction, but depending on the previous history. The timing of force production calculated from the state-space diagrams was in agreement with the generally accepted muscle properties, thereby demonstrating the reliability of the method. A macroscopic muscular model consisting of a contractile element, parallel and series elastic elements was developed. The parameters from the experiment analysis, particularly the force modification after non-isometric contractions and the time constants, were reproduced by the simulations. The relationship between time constants introduced in a mechanistic model and the measured macroscale timings is discussed.

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References

  • Abbott B, Aubert X (1952) The force exerted by active striated muscle during and after change of length. J Physiol 117: 77–86

    Google Scholar 

  • Bagni M, Cecchi G, Colombini B (2005) Crossbridge properties investigated by fast ramp stretching of activated frog muscle fibres. J Physiol 565(1): 261–268

    Article  Google Scholar 

  • Brooks S, Faulkner J (1988) Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol 404: 71–82

    Google Scholar 

  • Bullimore SR, MacIntosh BR, Herzog W (2008) Is a parallel elastic element responsible for the enhancement of steady-state muscle force following active stretch?. J Exp Biol 211: 3001–3008

    Article  Google Scholar 

  • Corr D, Herzog W (2005) Force recovery after activated shortening in whole skeletal muscle: Transient and steady-state aspects of force depression. J Appl Physiol 99(1): 252–260

    Article  Google Scholar 

  • Ebashi S, Endo M (1968) Calcium ion and muscle contraction. Prog Biophys Mol Biol 18: 123–166

    Article  Google Scholar 

  • Edman K (1979) The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol 291: 143–159

    Google Scholar 

  • Fang ZP, Mortimer J (1991) A method to effect physiological recruitment order in electrically activated muscle. IEEE Trans Biomed Eng 38(2): 175–179

    Article  Google Scholar 

  • Gordon A, Huxley A, Julian F (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibers. J Physiol 184: 170–192

    Google Scholar 

  • Günther M, Schmitt S, Wank V (2007) High-frequency oscillations as a consequence of neglected serial damping in Hill-type muscle models. Biol Cybern 97(1): 63–79

    Article  MATH  Google Scholar 

  • Hancock W, Martin D, Huntsman L (2004) Ca2+ and segment length dependence of isometric force kinetics in intact ferret cardiac muscle. Circ Res 73(4): 603–611

    Article  Google Scholar 

  • Hatze H (1977) A myocybernetic control model of skeletal muscle. Biol Cybern 25(2): 103–119

    Article  MATH  Google Scholar 

  • Henneman E, Somjen G, Carpenter D (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28(3): 560–580

    Google Scholar 

  • Herzog W, Leonard T (1997) Depression of cat soleus forces following isokinetic shortening. J Biomech 30(9): 865–872

    Article  Google Scholar 

  • Herzog W, Leonard T (2000) The history dependence of force production in mammalian skeletal muscle following stretch-shortening and shortening-stretch cycles. J Biomech 33: 531–542

    Article  Google Scholar 

  • Herzog W, Leonard T, Wu J (2000) The relationship between force depression following shortening and mechanical work in skeletal muscle. J Biomech 33(5): 659–668

    Article  Google Scholar 

  • Hill A (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond 126: 136–195

    Article  Google Scholar 

  • Jeffrey A (1990) Linear algebra and ordinary differential equations. Blackwell, England

    MATH  Google Scholar 

  • Jordan D, Smith P (1999) Nonlinear ordinary differential equations: an introduction to dynamical systems, 3rd edn. Oxford University Press, New York

    MATH  Google Scholar 

  • Julian F, Morgan D (1979) The effect on tension of non-uniform distribution of length changes applied to frog muscle fibres. J Physiol 293: 379–392

    Google Scholar 

  • Kosterina N, Westerblad H, Lännergren J, Eriksson A (2008) Muscular force production after concentric contraction. J Biomech 44(11): 2422–2429

    Article  Google Scholar 

  • Kosterina N, Westerblad H, Eriksson A (2009) Mechanical work as predictor of force enhancement and force depression. J Biomech 42(11): 1628–1634

    Article  Google Scholar 

  • Lee H, Herzog W, Leonard T (2001) Effects of cyclic changes in muscle length on force production in in situ cat soleus. J Biomech 34: 979–987

    Article  Google Scholar 

  • Lou F, Curtin N, Woledge R (1998) Contraction with shortening during stimulation or during relaxation: how do the energetic costs compare?. J Muscle Res Cell Motil 19(7): 797–802

    Article  Google Scholar 

  • Luff A (1981) Dynamic properties of the inferior rectus, extensor digitorum longus, diaphragm and soleus muscles of the mouse. J Physiol 313: 161–171

    Google Scholar 

  • Marechal G, Plaghki L (1979) The deficit of the isometric tetanic tension redeveloped after a release of frog muscle at a constant velocity. J Gen Physiol 73(4): 453–467

    Article  Google Scholar 

  • McGowan CP, Neptune RR, Herzog W (2010) A phenomenological model and validation of shortening-induced force depression during muscle contractions. J Biomech 43(3): 449–454

    Article  Google Scholar 

  • Meijer K, Grootenboer H, Koopman H, Van Der Linden B, Huijing P (1998) A Hill type model of rat medial gastrocnemius muscle that accounts for shortening history effects. J Biomech 31(6): 555–563

    Article  Google Scholar 

  • Morgan D (2007) Can all residual force enhancement be explained by sarcomere non-uniformities?. J Physiol 578(2): 613–615

    Article  Google Scholar 

  • Pettersson R, Nordmark A, Eriksson A (2010) Free-time optimization of targeted movements based on temporal FE approximation. In: Proceedings CST2010, Valencia

  • Ranatunga K (1982) Temperature-dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle. J Physiol 329: 465–483

    Google Scholar 

  • Rode C, Siebert T, Blickhan R (2009a) Titin-induced force enhancement and force depression: a ’sticky-spring’ mechanism in muscle contractions?. J Theor Biol 259(2): 350–360

    Article  Google Scholar 

  • Rode C, Siebert T, Herzog W, Blickhan R (2009b) The effects of parallel and series elastic components on estimated active cat soleus muscle force. J Mech Med Biol 9(1): 105–122

    Article  Google Scholar 

  • Savelberg H (2000) Rise and relaxation times of twitches and tetani in submaximally recruited, mixed muscle: a computer model. In: Herzog W (eds) Skeletal muscle mechanics: from mechanisms to function. Wiley, New York, pp 225–240

    Google Scholar 

  • Schachar R, Herzog W, Leonard T (2004) The effects of muscle stretching and shortening on isometric forces on the descending limb of the force-length relationship. J Biomech 37(6): 917–926

    Article  Google Scholar 

  • Siebert T, Rode C, Herzog W, Till O, Blickhan R (2008) Nonlinearities make a difference: comparison of two common Hill-type models with real muscle. Biol Cybern 98: 133–143

    Article  MathSciNet  MATH  Google Scholar 

  • Stein R, Gordon T, Shrive J (1982) Temperature dependence of mammalian muscle contractions and ATPase activities. Biophys J 40(2): 97–107

    Article  Google Scholar 

  • Stephenson D, Williams D (1982) Effects of sarcomere length on the force-pca relation in fast- and slow-twitch skinned muscle fibres from the rat. J Physiol 333: 637–653

    Google Scholar 

  • Sugi H, Tsuchiya T (1988) Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibres. J Physiol 407: 215–229

    Google Scholar 

  • Thompson J, Stewart H (1986) Nonlinear dynamics and chaos, 1st edn. Wiley, England

    MATH  Google Scholar 

  • Till O, Siebert T, Rode C, Blickhan R (2008) Characterization of isovelocity extension of activated muscle: A hill-type model for eccentric contractions and a method for parameter determination. J Theor Biol 255(2): 176–187

    Article  MathSciNet  Google Scholar 

  • van Soest A, Bobbert M (1993) The contribution of muscle properties in the control of explosive movements. Biol Cybern 69(3): 195–204

    Article  Google Scholar 

  • Zajac F, Faden J (1985) Relationship among recruitment order, axonal conduction velocity, and muscle-unit properties of type-identified motor units in cat plantaris muscle. J Neurophysiol 53(5): 1303–1322

    Google Scholar 

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Correspondence to Anders Eriksson.

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Kosterina, N., Westerblad, H. & Eriksson, A. History effect and timing of force production introduced in a skeletal muscle model. Biomech Model Mechanobiol 11, 947–957 (2012). https://doi.org/10.1007/s10237-011-0364-5

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  • DOI: https://doi.org/10.1007/s10237-011-0364-5

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