Biomechanical behavior of muscle-tendon complex during dynamic human movements.

This paper reviews the research findings regarding the force and length changes of the muscle-tendon complex during dynamic human movements, especially those using ultrasonography and computer simulation. The use of ultrasonography demonstrated that the tendinous structures of the muscle-tendon complex are compliant enough to influence the biomechanical behavior (length change, shortening velocity, and so on) of fascicles substantially. It was discussed that the fascicles are a force generator rather than a work generator; the tendinous structures function not only as an energy re-distributor but also as a power amplifier, and the interaction between fascicles and tendinous structures is essential for generating higher joint power outputs during the late pushoff phase in human vertical jumping. This phenomenon could be explained based on the force-length/velocity relationships of each element (contractile and series elastic elements) in the muscle-tendon complex during movements. Through computer simulation using a Hill-type muscle-tendon complex model, the benefit of making a countermovement was examined in relation to the compliance of the muscle-tendon complex and the length ratio between the contractile and series elastic elements. Also, the integral roles of the series elastic element were simulated in a cyclic human heel-raise exercise. It was suggested that the storage and reutilization of elastic energy by the tendinous structures play an important role in enhancing work output and movement efficiency in many sorts of human movements.

[1]  T. Fukunaga,et al.  Behavior of fascicles and tendinous structures of human gastrocnemius during vertical jumping. , 2001, Journal of applied physiology.

[2]  M F Bobbert,et al.  Dependence of human squat jump performance on the series elastic compliance of the triceps surae: a simulation study. , 2001, The Journal of experimental biology.

[3]  V R Edgerton,et al.  Specific tension of human plantar flexors and dorsiflexors. , 1996, Journal of applied physiology.

[4]  P V Komi,et al.  Physiological and Biomechanical Correlates of Muscle Function: Effects of Muscle Structure and Stretch—Shortening Cycle on Force and Speed , 1984, Exercise and sport sciences reviews.

[5]  G. V. I. Schenau An alternative view of the concept of utilisation of elastic energy in human movement , 1984 .

[6]  M. Noble,et al.  Residual force enhancement after stretch of contracting frog single muscle fibers , 1982, The Journal of general physiology.

[7]  K. Edman,et al.  Double-hyperbolic nature of the force-velocity relation in frog skeletal muscle. , 1988, Advances in experimental medicine and biology.

[8]  J. van den Berg,et al.  Calf muscle moment, work and efficiency in level walking; role of series elasticity. , 1983, Journal of biomechanics.

[9]  G. Loeb,et al.  Feline caudofemoralis muscle Muscle fibre properties, architecture, and motor innervation , 1998, Experimental Brain Research.

[10]  R. Alexander,et al.  Storage of elastic strain energy in muscle and other tissues , 1977, Nature.

[11]  Pierre Boher,et al.  A transmission electron microscopy study of low‐temperature reaction at the Co‐Si interface , 1990 .

[12]  Akinori Nagano,et al.  Contribution of Series Elasticity in Human Cyclic Heel-Raise Exercise , 2003 .

[13]  A. Cutts,et al.  The range of sarcomere lengths in the muscles of the human lower limb. , 1988, Journal of anatomy.

[14]  T. Fukunaga,et al.  Muscle and Tendon Interaction During Human Movements , 2002, Exercise and sport sciences reviews.

[15]  F. W. Flitney,et al.  Cross‐bridge detachment and sarcomere 'give' during stretch of active frog's muscle. , 1978, The Journal of physiology.

[16]  T. Fukunaga,et al.  The length-force characteristcs of human gastrocnemius and soleus muscles in vivo , 2000 .

[17]  Brown Mc,et al.  The effect of stretching a contracting muscle on its subsequent performance during shortening. , 1972 .

[18]  Matthew T. Wheeler,et al.  Skeletal Muscle Structure and Function , 2006 .

[19]  G. Zahalak,et al.  Muscle activation and contraction: constitutive relations based directly on cross-bridge kinetics. , 1990, Journal of biomechanical engineering.

[20]  Graham E. Caldwell,et al.  Tendon Elasticity and Relative Length: Effects on the Hill Two-Component Muscle Model , 1995 .

[21]  M. Lafortune,et al.  Dominant role of interface over knee angle for cushioning impact loading and regulating initial leg stiffness. , 1996, Journal of biomechanics.

[22]  P. Komi,et al.  Electromechanical delay in skeletal muscle under normal movement conditions. , 1979, Acta physiologica Scandinavica.

[23]  M. Bobbert,et al.  A model of the human triceps surae muscle-tendon complex applied to jumping. , 1986, Journal of biomechanics.

[24]  J. Fridén,et al.  Functional and clinical significance of skeletal muscle architecture , 2000, Muscle & nerve.

[25]  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.

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

[27]  P A Huijing,et al.  Efficiency of rat medial gastrocnemius muscle in contractions with and without an active prestretch. , 1989, The Journal of experimental biology.

[28]  D. Newham,et al.  Skeletal Muscle Structure and Function — Implications for rehabilitation and sports medicine , 1992 .

[29]  T. Fukunaga,et al.  Architectural and functional features of human triceps surae muscles during contraction. , 1998, Journal of applied physiology.

[30]  Alan M. Wilson,et al.  Horses damp the spring in their step , 2001, Nature.

[31]  M. Noble,et al.  Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. , 1978, The Journal of physiology.

[32]  S. Walker,et al.  I segment lengths and thin filament periods in skeletal muscle fibers of the rhesus monkey and the human , 1974, The Anatomical record.

[33]  R. Brand,et al.  Muscle fiber architecture in the human lower limb. , 1990, Journal of biomechanics.

[34]  T. Fukunaga,et al.  In vivo muscle fibre behaviour during counter‐movement exercise in humans reveals a significant role for tendon elasticity , 2002, The Journal of physiology.

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

[36]  P. V. Komi,et al.  Joint moment and mechanical power flow of the lower limb during vertical jump. , 1987 .

[37]  A J van Soest,et al.  The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions. , 1990, The Journal of experimental biology.

[38]  W Herzog,et al.  Modelling concentric contraction of muscle using an improved cross-bridge model. , 1999, Journal of biomechanics.

[39]  S L Woo,et al.  The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. , 1981, Journal of biomechanical engineering.

[40]  G J van Ingen Schenau,et al.  Effects of prestretch at the onset of stimulation on mechanical work output of rat medial gastrocnemius muscle-tendon complex. , 1990, The Journal of experimental biology.

[41]  W. O. Fenn,et al.  Muscular force at different speeds of shortening , 1935, The Journal of physiology.

[42]  Jack M. Winters,et al.  Overview: Influence of Muscle on Cyclic and Propulsive Movements Involving the Lower Limb , 1990 .

[43]  H. M. Toussaint,et al.  Positive work as a function of eccentric load in maximal leg extension movements , 2004, European Journal of Applied Physiology and Occupational Physiology.

[44]  C. Bosco,et al.  Influence of stretch-shortening cycle on mechanical behaviour of triceps surae during hopping. , 1992, Acta physiologica Scandinavica.

[45]  M. Pandy,et al.  Storage and utilization of elastic strain energy during jumping. , 1993, Journal of biomechanics.

[46]  Marcus G. Pandy,et al.  An Analytical Framework for Quantifying Muscular Action During Human Movement , 1990 .

[47]  R. Lieber,et al.  Frog semitendinosis tendon load-strain and stress-strain properties during passive loading. , 1991, The American journal of physiology.

[48]  G. Cavagna,et al.  Positive work done by a previously stretched muscle. , 1968, Journal of applied physiology.

[49]  R. Griffiths,et al.  Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. , 1989, Progress in brain research.

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

[51]  T Abe,et al.  Architectural characteristics of muscle in black and white college football players. , 1999, Medicine and science in sports and exercise.

[52]  E. Bizzi,et al.  Posture control and trajectory formation during arm movement , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  I. Hunter,et al.  Dynamics of human ankle stiffness: variation with mean ankle torque. , 1982, Journal of biomechanics.

[54]  T. Fukunaga,et al.  Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. , 1993, Journal of applied physiology.

[55]  R. Griffiths Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. , 1991, The Journal of physiology.

[56]  T. Fukunaga,et al.  Determination of fascicle length and pennation in a contracting human muscle in vivo. , 1997, Journal of applied physiology.

[57]  G A Cavagna,et al.  Effect of stretching on the elastic characteristics and the contractile component of frog striated muscle , 1974, The Journal of physiology.

[58]  Akinori Nagano,et al.  Effects of the length ratio between the contractile element and the series elastic element on an explosive muscular performance. , 2004, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[59]  J Harlaar,et al.  Evaluation of moment-angle curves in isokinetic knee extension. , 1993, Medicine and science in sports and exercise.

[60]  D. Grieve Prediction of gastrocnemius length from knee and ankle joint posture , 1978 .

[61]  M. Voigt,et al.  Modulation of short latency stretch reflexes during human hopping. , 1998, Acta physiologica Scandinavica.

[62]  Gaudenz Danuser,et al.  Single muscle fiber contraction is dictated by inter-sarcomere dynamics. , 2002, Journal of theoretical biology.

[63]  Akinori Nagano,et al.  Interaction between fascicles and tendinous structures during counter movement jumping investigated in vivo. , 2003, Journal of applied physiology.

[64]  P. Komi,et al.  Prestretch potentiation of human skeletal muscle during ballistic movement. , 1981, Acta physiologica Scandinavica.

[65]  V. Dietz,et al.  Neuronal mechanisms of human locomotion. , 1979, Journal of neurophysiology.

[66]  T. Fukunaga,et al.  Ultrasonography gives directly but noninvasively elastic characteristic of human tendon in vivo , 1995, European Journal of Applied Physiology and Occupational Physiology.

[67]  R. F. Ker,et al.  Mechanical properties of various mammalian tendons , 1986 .

[68]  I W Hunter,et al.  Invariance of ankle dynamic stiffness during fatiguing muscle contractions. , 1983, Journal of biomechanics.

[69]  R. F. Ker Dynamic tensile properties of the plantaris tendon of sheep (Ovis aries). , 1981, The Journal of experimental biology.

[70]  T. Fukunaga,et al.  The length-force characteristics of human gastrocnemius and soleus in vivo , 2000 .

[71]  N C Heglund,et al.  Cross-bridge cycling theories cannot explain high-speed lengthening behavior in frog muscle. , 1990, Biophysical journal.

[72]  Paavo V. Komi,et al.  In vivo human triceps surae and quadriceps femoris muscle function in a squat jump and counter movement jump , 2000, European Journal of Applied Physiology.

[73]  M. Bobbert,et al.  An estimation of power output and work done by the human triceps surae muscle-tendon complex in jumping. , 1986, Journal of biomechanics.

[74]  M. Miyashita,et al.  In vivo achilles tendon loading' during jumping in humans , 2004, European Journal of Applied Physiology and Occupational Physiology.

[75]  T Fukunaga,et al.  Influence of elastic properties of tendon structures on jump performance in humans. , 1999, Journal of applied physiology.

[76]  T. Yanagida,et al.  Compliance of thin filaments in skinned fibers of rabbit skeletal muscle. , 1995, Biophysical journal.

[77]  M. Bobbert,et al.  Mechanics of human triceps surae muscle in walking, running and jumping. , 2002, Acta physiologica Scandinavica.

[78]  F Goubel,et al.  Changes in elastic characteristics of human muscle induced by eccentric exercise. , 1990, Journal of biomechanics.

[79]  R. Shadwick,et al.  Elastic energy storage in tendons: mechanical differences related to function and age. , 1990, Journal of applied physiology.

[80]  W S Levine,et al.  An optimal control model for maximum-height human jumping. , 1990, Journal of biomechanics.

[81]  D. Morgan Separation of active and passive components of short-range stiffness of muscle. , 1977, The American journal of physiology.

[82]  G. Jones,et al.  Observations on the control of stepping and hopping movements in man , 1971, The Journal of physiology.

[83]  G. Cavagna Elastic bounce of the body. , 1970, Journal of applied physiology.

[84]  N A Curtin,et al.  The efficiency of energy conversion by swimming muscles of fish. , 1993, Advances in experimental medicine and biology.

[85]  Martyn R. Shorten,et al.  Muscle Elasticity and Human Performance , 1987 .

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

[87]  M. C. Brown,et al.  The effect of stretching a contracting muscle on its subsequent performance during shortening. , 1972, The Journal of physiology.

[88]  P. Rack,et al.  Elastic properties of the cat soleus tendon and their functional importance. , 1984, The Journal of physiology.

[89]  V. M. Zatsiorsky,et al.  Biomechanical characteristics of human ankle-joint muscles , 2004, European Journal of Applied Physiology and Occupational Physiology.

[90]  T. Fukunaga,et al.  In vivo behaviour of human muscle tendon during walking , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[91]  Akinori Nagano,et al.  Comparison of Muscle-Tendon Interaction of Human M. Gastrocnemius Between Ankle- and Drop-Jumping , 2005 .

[92]  T Fukunaga,et al.  In vivo dynamics of human medial gastrocnemius muscle-tendon complex during stretch-shortening cycle exercise. , 2000, Acta physiologica Scandinavica.

[93]  S Fukashiro,et al.  In vivo determination of muscle viscoelasticity in the human leg. , 2001, Acta physiologica Scandinavica.

[94]  Walter Herzog,et al.  Calculated fiber lengths in cat gastrocnemius muscle during walking , 1993 .

[95]  T J Roberts,et al.  Muscular Force in Running Turkeys: The Economy of Minimizing Work , 1997, Science.

[96]  C T Davies,et al.  Electrically evoked isokinetic plantar flexor torque in males. , 1987, Journal of applied physiology.

[97]  P. Komi Stretch-shortening cycle: a powerful model to study normal and fatigued muscle. , 2000, Journal of biomechanics.

[98]  P V Komi,et al.  Joint Moment and Mechanical Power Flow of the Lower Limb During Vertical Jump , 1987, International journal of sports medicine.

[99]  G. Loeb,et al.  Measured and modeled properties of mammalian skeletal muscle: IV. Dynamics of activation and deactivation , 2004, Journal of Muscle Research & Cell Motility.

[100]  W. O. Fenn The relation between the work performed and the energy liberated in muscular contraction , 1924, The Journal of physiology.

[101]  Y Ueno,et al.  X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. , 1994, Biophysical journal.

[102]  H E Huxley,et al.  X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. , 1994, Biophysical journal.

[103]  J. Winters Hill-Based Muscle Models: A Systems Engineering Perspective , 1990 .

[104]  Terry K K Koo,et al.  In vivo determination of subject-specific musculotendon parameters: applications to the prime elbow flexors in normal and hemiparetic subjects. , 2002, Clinical biomechanics.

[105]  G. Loeb,et al.  Measured and modeled properties of mammalian skeletal muscle: III. the effects of stimulus frequency on stretch-induced force enhancement and shortening-induced force depression , 2004, Journal of Muscle Research & Cell Motility.

[106]  G J van Ingen Schenau,et al.  Isokinetic plantar flexion: experimental results and model calculations. , 1990, Journal of biomechanics.

[107]  A. J. van den Bogert,et al.  Intrinsic muscle properties facilitate locomotor control - a computer simulation study. , 1998, Motor control.

[108]  D. Morgan,et al.  The association between flexibility and running economy in sub-elite male distance runners. , 1996, Medicine and science in sports and exercise.

[109]  A. Biewener,et al.  In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. , 1998, The Journal of experimental biology.

[110]  P A Huijing,et al.  Influence of muscle geometry on shortening speed of fibre, aponeurosis and muscle. , 1992, Journal of biomechanics.

[111]  A Cutts Sarcomere length changes in muscles of the human thigh during walking. , 1989, Journal of anatomy.

[112]  David J. Sanderson,et al.  Muscular Coordination in Sporting Skills , 1990 .

[113]  Akinori Nagano,et al.  Effects of Series Elasticity of the Muscle Tendon Complex on an Explosive Activity Performance with a Counter Movement , 2004 .

[114]  A. V. van Soest,et al.  Why is countermovement jump height greater than squat jump height? , 1996, Medicine and science in sports and exercise.

[115]  S. Jaric,et al.  Effects of previous muscle contractions on cyclic movement dynamics , 2006, European Journal of Applied Physiology and Occupational Physiology.

[116]  G Grimby,et al.  Potentiation of concentric plantar flexion torque following eccentric and isometric muscle actions. , 1994, Acta physiologica Scandinavica.

[117]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.