Structural and functional features of human muscle–tendon unit

This paper reviews the architectural details and the in vivo behavior of the human muscle–tendon unit with the focus on the triceps surae and quadriceps femoris muscles. Recent advances in experimental techniques allow in vivo measurements of muscle–tendon architecture and function. In particular, the use of ultrasonography for measurement of tendon and muscle has expanded our knowledge in the last decade. Furthermore, the nuclear magnetic resonance imaging is opening up new insights not only for three‐dimensional anatomical information but also for examining musculo‐skeletal motion in vivo. While these two completely non‐invasive methods provide kinematic data, in vivo force measurements still require somewhat invasive procedures and are scarce. Thus, muscle forces are frequently calculated using both simple and complex models. These models can give us suggestions for further experimental work. There is a need to examine the experimental data ranging from single‐fiber experiments to the muscle function in human movement in order to understand the muscle–tendon function in vivo fully. Furthermore, appreciation of the structure–function relationships may help us to understand the entity of muscle–tendon function both from the perspective of mechanical behavior and neural control.

[1]  U. Proske,et al.  Damage to human muscle from eccentric exercise after training with concentric exercise , 1998, The Journal of physiology.

[2]  P. Komi,et al.  Achilles tendon loading during walking: application of a novel optic fiber technique , 1998, European Journal of Applied Physiology and Occupational Physiology.

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

[4]  M. Kjaer,et al.  Tendon properties in relation to muscular activity and physical training , 2003, Scandinavian journal of medicine & science in sports.

[5]  E B Simonsen,et al.  The influence of tendon Youngs modulus, dimensions and instantaneous moment arms on the efficiency of human movement. , 1995, Journal of biomechanics.

[6]  R. Shadwick,et al.  Relationship between body mass and biomechanical properties of limb tendons in adult mammals. , 1994, The American journal of physiology.

[7]  M. Kjaer,et al.  Load‐displacement properties of the human triceps surae aponeurosis and tendon in runners and non‐runners , 2002, Scandinavian journal of medicine & science in sports.

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

[9]  C. Gans,et al.  Functional bases of fiber length and angulation in muscle , 1987, Journal of morphology.

[10]  T. Fukunaga,et al.  In vivo estimation of contraction velocity of human vastus lateralis muscle during "isokinetic" action. , 2000, Journal of applied physiology.

[11]  N. McKee,et al.  Comparing human skeletal muscle architectural parameters of cadavers with in vivo ultrasonographic measurements , 2001, Journal of anatomy.

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

[13]  T. Fukunaga,et al.  Gender differences in the viscoelastic properties of tendon structures , 2003, European Journal of Applied Physiology.

[14]  Taija Finni,et al.  Muscle Mechanics During Human Movement Revealed by In Vivo Measurements of Tendon Force and Muscle Length , 2001 .

[15]  P. Cova,et al.  Effect of unintentionally introduced oxygen on the electron–cyclotron resonance chemical-vapor deposition of SiNX films , 2002 .

[16]  Richard L. Lieber,et al.  Effects of Muscle Contraction on the Load-Strain Properties of Frog Aponeurosis and Tendon , 2000, Cells Tissues Organs.

[17]  A. Hof Muscle mechanics and neuromuscular control. , 2003, Journal of biomechanics.

[18]  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.

[19]  S. Sekiya Muscle architecture and intramuscular distribution of nerves in the human soleus muscle. , 1991, Acta anatomica.

[20]  C. Maganaris Force‐length characteristics of the in vivo human gastrocnemius muscle , 2003, Clinical anatomy.

[21]  M. Horiguchi,et al.  Nerve supply to the accessory soleus muscle. , 1994, Acta Anatomica.

[22]  P A Huijing,et al.  Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. , 1999, Journal of biomechanics.

[23]  T Fukunaga,et al.  Changes in aponeurotic dimensions upon muscle shortening: in vivo observations in man , 2001, Journal of anatomy.

[24]  J. Trotter,et al.  Structural domains of the muscle‐tendon junction. 1. The internal lamina and the connecting domain , 1983, The Anatomical record.

[25]  P. Cerretelli,et al.  In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. , 1996, The Journal of physiology.

[26]  S. Street,et al.  Lateral transmission of tension in frog myofibers: A myofibrillar network and transverse cytoskeletal connections are possible transmitters , 1983, Journal of cellular physiology.

[27]  Masaki Ishikawa,et al.  Effects of different dropping intensities on fascicle and tendinous tissue behavior during stretch-shortening cycle exercise. , 2004, Journal of applied physiology.

[28]  V R Edgerton,et al.  Mechanical output of the cat soleus during treadmill locomotion: in vivo vs in situ characteristics. , 1988, Journal of biomechanics.

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

[30]  J L Van Leeuwen,et al.  Modelling mechanically stable muscle architectures. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  P. Komi,et al.  Biomechanical loading of Achilles tendon during normal locomotion. , 1992, Clinics in sports medicine.

[32]  J. Laidlaw,et al.  ANATOMY OF THE HUMAN BODY , 1967, The Ulster Medical Journal.

[33]  V. Edgerton,et al.  Nonuniform strain of human soleus aponeurosis-tendon complex during submaximal voluntary contractions in vivo. , 2003, Journal of applied physiology.

[34]  P. V. Komi,et al.  Optic fibre as a transducer of tendomuscular forces , 2004, European Journal of Applied Physiology and Occupational Physiology.

[35]  Susan J. Harkema,et al.  Clonus after human spinal cord injury cannot be attributed solely to recurrent muscle-tendon stretch , 2003, Experimental Brain Research.

[36]  C. Maganaris,et al.  Force-length characteristics of in vivo human skeletal muscle. , 2001, Acta physiologica Scandinavica.

[37]  P. Komi,et al.  Comparison of force-velocity relationships of vastus lateralis muscle in isokinetic and in stretch-shortening cycle exercises. , 2003, Acta physiologica Scandinavica.

[38]  F. Noyes,et al.  BIOMECHANICS OF LIGAMENTS AND TENDONS , 1978, Exercise and sport sciences reviews.

[39]  P. Huijing,et al.  Length-force characteristics of the aponeurosis in the passive and active muscle condition and in the isolated condition. , 1994, Journal of biomechanics.

[40]  M. Kjaer,et al.  Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. , 2003, Acta physiologica Scandinavica.

[41]  A. Krammer,et al.  Structural insights into the mechanical regulation of molecular recognition sites. , 2001, Trends in biotechnology.

[42]  T Finni,et al.  Behaviour of vastus lateralis muscle-tendon during high intensity SSC exercises in vivo. , 2003, Acta physiologica Scandinavica.

[43]  Constantinos N Maganaris,et al.  Paradoxical muscle movement in human standing , 2004, The Journal of physiology.

[44]  G. Gottlieb,et al.  Dependence of human ankle compliance on joint angle. , 1978, Journal of biomechanics.

[45]  T Fukunaga,et al.  Estimation of active force-length characteristics of human vastus lateralis muscle. , 1997, Acta anatomica.

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

[47]  T. Fukunaga,et al.  Muscle architecture and function in humans. , 1997, Journal of biomechanics.

[48]  A. Levick NETTER’S CONCISE ATLAS OF ORTHOPAEDIC ANATOMY , 2004, Australasian Chiropractic & Osteopathy.

[49]  Paavo V. Komi,et al.  Two Methods for Estimating Tendinous Tissue Elongation during Human Movement , 2002 .

[50]  J P Paul,et al.  Hysteresis measurements in intact human tendon. , 2000, Journal of biomechanics.

[51]  Yasuo Kawakami,et al.  Architecture of contracting human muscles and its functional significance , 2000 .

[52]  M. Kjaer,et al.  Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. , 2004, Journal of applied physiology.

[53]  J. P. Paul,et al.  Tensile properties of the in vivo human gastrocnemius tendon. , 2002, Journal of biomechanics.

[54]  P. Sheard,et al.  Intramuscular force transmission. , 2002, Advances in experimental medicine and biology.

[55]  P. Huijing,et al.  Compartmental fasciotomy and isolating a muscle from neighboring muscles interfere with myofascial force transmission within the rat anterior crural compartment , 2003, Journal of morphology.

[56]  B Bigland-Ritchie,et al.  EMG/FORCE RELATIONS AND FATIGUE OF HUMAN VOLUNTARY CONTRACTIONS , 1981, Exercise and sport sciences reviews.

[57]  N. McKee,et al.  Resolving discrepancies in image research: the importance of direct observation in the illustration of the human soleus muscle. , 1998, The Journal of biocommunication.

[58]  R. Balaban,et al.  Efficiency of human skeletal muscle in vivo: comparison of isometric, concentric, and eccentric muscle action. , 1997, Journal of applied physiology.

[59]  In vivo muscle mechanics during locomotion depend on movement amplitude and contraction intensity , 2001, European Journal of Applied Physiology.

[60]  W Herzog,et al.  The history dependence of force production in mammalian skeletal muscle following stretch-shortening and shortening-stretch cycles. , 2000, Journal of biomechanics.

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

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

[63]  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.

[64]  A. Arndt,et al.  Asymmetrical Loading of the Human Triceps Surae: I. Mediolateral Force Differences in the Achilles Tendon , 1999, Foot & ankle international.

[65]  Constantinos N. Maganaris,et al.  Imaging-based estimates of moment arm length in intact human muscle-tendons , 2004, European Journal of Applied Physiology.

[66]  P. V. Komi,et al.  Relationship between Muscle Tension, EMG and Velocity of Contraction under Concentric and Eccentric Work , 1973 .

[67]  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.

[68]  R. F. Ker,et al.  The implications of the adaptable fatigue quality of tendons for their construction, repair and function. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[69]  V Reggie Edgerton,et al.  Mapping of movement in the isometrically contracting human soleus muscle reveals details of its structural and functional complexity. , 2003, Journal of applied physiology.

[70]  C. Gans Fiber architecture and muscle function. , 1982, Exercise and sport sciences reviews.

[71]  R. Lieber,et al.  Relationship between Achilles tendon mechanical properties and gastrocnemius muscle function. , 1993, Journal of biomechanical engineering.

[72]  T. Fukunaga,et al.  Muscle fiber and tendon length changes in the human vastus lateralis during slow pedaling. , 2001, Journal of applied physiology.

[73]  Yasuo Kawakami,et al.  In vivo determination of fascicle curvature in contracting human skeletal muscles. , 2002, Journal of applied physiology.

[74]  A Garfinkel,et al.  Spatial distribution of motor unit fibers in the cat soleus and tibialis anterior muscles: local interactions , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[76]  J. Tidball Force transmission across muscle cell membranes. , 1991, Journal of biomechanics.

[77]  V. Edgerton,et al.  Muscle synergism during isometric plantarflexion in achilles tendon rupture patients and in normal subjects revealed by velocity-encoded cine phase-contrast MRI. , 2006, Clinical biomechanics.

[78]  T Finni,et al.  Concentric force enhancement during human movement. , 2001, Acta physiologica Scandinavica.

[79]  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.

[80]  Paavo V. Komi,et al.  In vivo behavior of vastus lateralis muscle during dynamic performances , 2001 .

[81]  M. Narici,et al.  Human skeletal muscle architecture studied in vivo by non-invasive imaging techniques: functional significance and applications. , 1999, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[82]  E. Fischer THE OXYGEN-CONSUMPTION OF ISOLATED MUSCLES FOR ISOTONIC AND ISOMETRIC TWITCHES , 1931 .

[83]  C. Maganaris,et al.  In vivo measurements of the triceps surae complex architecture in man: implications for muscle function , 1998, The Journal of physiology.

[84]  T Fukunaga,et al.  Nonisometric behavior of fascicles during isometric contractions of a human muscle. , 1998, Journal of applied physiology.

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

[86]  H. Tamaki,et al.  Alternate activity in the synergistic muscles during prolonged low-level contractions. , 1998, Journal of applied physiology.

[87]  B. Koopman,et al.  Three-dimensional finite element modeling of skeletal muscle using a two-domain approach: linked fiber-matrix mesh model. , 2001, Journal of biomechanics.

[89]  J. Viitasalo Electromechanical behaviour of the knee extensor musculature in maximal isometric and concentric contractions and in jumping. , 1984, Electromyography and clinical neurophysiology.

[90]  P. Huijing Muscular Force Transmission Necessitates a Multilevel Integrative Approach to the Analysis of Function of Skeletal Muscle , 2003, Exercise and sport sciences reviews.

[91]  H.J. Grootenboer,et al.  Revised planimetric model of unipennate skeletal muscle: a mechanical approach. , 1998, Clinical biomechanics.

[92]  T. Fukunaga,et al.  Influence of static stretching on viscoelastic properties of human tendon structures in vivo. , 2001, Journal of applied physiology.

[93]  N. McKee,et al.  Sonographic studies of human soleus and gastrocnemius muscle architecture: gender variability , 2000, European Journal of Applied Physiology.

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

[95]  A. Patla,et al.  Myoelectric changes in the triceps surae muscles under sustained contractions , 1987, European Journal of Applied Physiology and Occupational Physiology.