Comparison of the validity of Hill and Huxley muscle–tendon complex models using experimental data obtained from rat m. soleus in situ

ABSTRACT The relationship between mechanical and metabolic behaviour in the widely used Hill muscle–tendon complex (MTC) model is not straightforward, whereas this is an integral part of the Huxley model. In this study, we assessed to what extent Huxley- and Hill-type MTC models yield adequate predictions of mechanical muscle behaviour during stretch–shortening cycles (SSCs). In fully anaesthetized male Wistar rats (N=3), m. soleus was dissected completely free, except for the insertion. Cuff electrodes were placed over the n. ischiadicus. The distal end of the tendon was connected to a servo motor, via a force transducer. The setup allowed for full control over muscle stimulation and length, while force was measured. Quick-release and isovelocity contractions (part 1), and SSCs (part 2) were imposed. Simulations of part 2 were made with both a Hill and a Huxley MTC model, using parameter values determined from part 1. Modifications to the classic two-state Huxley model were made to incorporate series elasticity, activation dynamics, and active and passive force–length relationships. Results were similar for all rats. Fitting of the free parameters to the data of part 1 was near perfect (R2>0.97). During SSCs, predicted peak force and force during relaxation deviated from the experimental data for both models. Overall, both models yielded similarly adequate predictions of the experimental data. We conclude that Huxley and Hill MTC models are equally valid with respect to mechanical behaviour. Summary: Huxley and Hill muscle–tendon-complex models yield similar predictions of rat soleus muscle force, under physiological contraction conditions.

[1]  P A Huijing,et al.  Extramuscular myofascial force transmission within the rat anterior tibial compartment: proximo-distal differences in muscle force. , 2001, Acta physiologica Scandinavica.

[2]  Modeling dynamic contraction of muscle using the cross-bridge theory. , 1997, Mathematical biosciences.

[3]  M. Pandy,et al.  Dynamic optimization of human walking. , 2001, Journal of biomechanical engineering.

[4]  A. Büschges,et al.  Hill-type muscle model parameters determined from experiments on single muscles show large animal-to-animal variation , 2012, Biological Cybernetics.

[5]  G. Zahalak A distribution-moment approximation for kinetic theories of muscular contraction , 1981 .

[6]  T. Roberts The integrated function of muscles and tendons during locomotion. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[7]  P A Huijing,et al.  Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle. , 2001, Journal of biomechanics.

[8]  Matej Daniel,et al.  A comparative study of muscle force estimates using Huxley's and Hill's muscle model , 2014, Computer methods in biomechanics and biomedical engineering.

[9]  R L Lieber,et al.  Sarcomere length operating range of vertebrate muscles during movement. , 2001, The Journal of experimental biology.

[10]  A. Schwab,et al.  The influence of the biarticularity of the gastrocnemius muscle on vertical-jumping achievement. , 1993, Journal of biomechanics.

[11]  G. Lichtwark,et al.  Effects of series elasticity and activation conditions on muscle power output and efficiency , 2005, Journal of Experimental Biology.

[12]  A. J. van den Bogert,et al.  Human muscle modelling from a user's perspective. , 1998, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[13]  C. Krarup Enhancement and diminution of mechanical tension evoked by staircase and by tetanus in rat muscle , 1981, The Journal of physiology.

[14]  Alan M. Wilson,et al.  Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? , 2007, Journal of biomechanics.

[15]  Kenneth S. Campbell,et al.  Interactions between Connected Half-Sarcomeres Produce Emergent Mechanical Behavior in a Mathematical Model of Muscle , 2009, PLoS Comput. Biol..

[16]  Ansgar Büschges,et al.  Determining all parameters necessary to build Hill-type muscle models from experiments on single muscles , 2012, Biological Cybernetics.

[17]  N A Curtin,et al.  Predictions of the time course of force and power output by dogfish white muscle fibres during brief tetani. , 1998, The Journal of experimental biology.

[18]  M L Hull,et al.  Are the maximum shortening velocity and the shape parameter in a Hill-type model of whole muscle related to activation? , 2005, Journal of biomechanics.

[19]  A. M. Krylow,et al.  Dynamic force responses of muscle involving eccentric contraction. , 1997, Journal of biomechanics.

[20]  Marcus G. Pandy,et al.  Tendon elastic strain energy in the human ankle plantar-flexors and its role with increased running speed , 2014, Journal of Experimental Biology.

[21]  M. Pandy,et al.  A phenomenological model for estimating metabolic energy consumption in muscle contraction. , 2004, Journal of biomechanics.

[22]  C. Heckman,et al.  Force from cat soleus muscle during imposed locomotor-like movements: experimental data versus Hill-type model predictions. , 1997, Journal of neurophysiology.

[23]  Guangju Ji,et al.  Stretch-induced Calcium Release in Smooth Muscle , 2002, The Journal of general physiology.

[24]  C. Richards,et al.  A bio-robotic platform for integrating internal and external mechanics during muscle-powered swimming , 2012, Bioinspiration & biomimetics.

[25]  J Cholewicki,et al.  Relationship between muscle force and stiffness in the whole mammalian muscle: a simulation study. , 1995, Journal of biomechanical engineering.

[26]  G. Lichtwark,et al.  The influence of tendon compliance on muscle power output and efficiency during cyclic contractions , 2010, Journal of Experimental Biology.

[27]  Pierre-Brice Wieber,et al.  Multiscale modeling of skeletal muscle properties and experimental validations in isometric conditions , 2011, Biological Cybernetics.

[28]  B. Allard,et al.  Stretch-induced activation of Ca(2+)-activated K(+) channels in mouse skeletal muscle fibers. , 2000, American journal of physiology. Cell physiology.

[29]  Andrew A Biewener,et al.  Validation of Hill-type muscle models in relation to neuromuscular recruitment and force-velocity properties: predicting patterns of in vivo muscle force. , 2014, Integrative and comparative biology.

[30]  F. Julian Activation in a skeletal muscle contraction model with a modification for insect fibrillar muscle. , 1969, Biophysical journal.

[31]  Andrew A Biewener,et al.  Accuracy of gastrocnemius muscles forces in walking and running goats predicted by one-element and two-element Hill-type models. , 2013, Journal of biomechanics.

[32]  A. V. van Soest,et al.  Equilibrium point control cannot be refuted by experimental reconstruction of equilibrium point trajectories. , 2007, Journal of neurophysiology.

[33]  Walter Herzog,et al.  Considerations on the history dependence of muscle contraction. , 2004, Journal of applied physiology.

[34]  Appaji Panchangam,et al.  Non-uniform distribution of strain during stretch of relaxed skeletal muscle fibers from rat soleus muscle , 2011, Journal of Muscle Research and Cell Motility.

[35]  Emanuel Azizi,et al.  Muscle performance during frog jumping: influence of elasticity on muscle operating lengths , 2010, Proceedings of the Royal Society B: Biological Sciences.

[36]  E. J. Cheng,et al.  Measured and modeled properties of mammalian skeletal muscle. II. The effectsof stimulus frequency on force-length and force-velocity relationships , 1999, Journal of Muscle Research & Cell Motility.

[37]  Huub Maas,et al.  Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat. , 2008, Journal of applied physiology.

[38]  A. Huxley Muscle structure and theories of contraction. , 1957, Progress in biophysics and biophysical chemistry.

[39]  A. Tözeren Constitutive equations of skeletal muscle based on cross-bridge mechanism. , 1985, Biophysical journal.

[40]  A. V. van Soest,et al.  Which factors determine the optimal pedaling rate in sprint cycling? , 2000, Medicine and science in sports and exercise.

[41]  T. L. Hill,et al.  A cross-bridge model of muscle contraction. , 1978, Progress in biophysics and molecular biology.

[42]  M. Delp,et al.  Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. , 1996, Journal of applied physiology.

[43]  M. Pousson,et al.  Stiffness changes and fibre type transitions in rat soleus muscle produced by jumping training , 1991, Pflügers Archiv.

[44]  A. Huxley,et al.  Proposed Mechanism of Force Generation in Striated Muscle , 1971, Nature.

[45]  Hubertus F.J.M. Koopman,et al.  Fully Isometric Length-Force Curves of Rat Muscle Differ from those during and after Concentric Contractions , 1997 .

[46]  N. Curtin,et al.  Predicting force generation by lamprey muscle during applied sinusoidal movement using a simple dynamic model. , 1998, The Journal of experimental biology.

[47]  G I Zahalak,et al.  A re-examination of calcium activation in the Huxley cross-bridge model. , 1997, Journal of biomechanical engineering.

[48]  Ayman Habib,et al.  OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement , 2007, IEEE Transactions on Biomedical Engineering.

[49]  L. Stark,et al.  Muscle models: What is gained and what is lost by varying model complexity , 1987, Biological Cybernetics.

[50]  Awj Sander Gielen,et al.  A Finite Element Approach for Skeletal Muscle using a Distributed Moment Model of Contraction , 2000, Computer methods in biomechanics and biomedical engineering.

[51]  William O. Williams,et al.  Huxley’s Model of Muscle Contraction with Compliance , 2011 .

[52]  V. Comincioli,et al.  A four-state cross bridge model for muscle contraction. Mathematical study and validation , 1984, Journal of mathematical biology.

[53]  P. Haugen Calcium transients in skeletal muscle fibres under isometric conditions and during and after a quick stretch , 1991, Journal of Muscle Research & Cell Motility.

[54]  R. M. Alexander,et al.  Tendon elasticity and muscle function. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[55]  G. Lichtwark,et al.  A modified Hill muscle model that predicts muscle power output and efficiency during sinusoidal length changes , 2005, Journal of Experimental Biology.

[56]  Jachen Denoth,et al.  A multisegmental cross-bridge kinetics model of the myofibril. , 2009, Journal of theoretical biology.

[57]  M. Bobbert Why is the force-velocity relationship in leg press tasks quasi-linear rather than hyperbolic? , 2012, Journal of applied physiology.

[58]  O. Schmitt The heat of shortening and the dynamic constants of muscle , 2017 .