The anatomical arrangement of muscle and tendon enhances limb versatility and locomotor performance

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1570, 2011, Pages 1540-1553

  Wilson, Alan ^a   Lichtwark, Glen ^b  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Biomechanics; Locomotion; Muscle; Tendon

Indexed keywords

BIOMECHANICS; LOCOMOTION; MEASUREMENT METHOD; MUSCLE;

EID: 79955458163     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0361     Document Type: Article

References (70)

1. Epstein, M. & Herzog, W. 1998 Theoretical models of skeletal muscle. Chichester, UK: Wiley.
2. Gordon, A. M., Huxley, A. F. & Julian, F. J. 1966 Variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol.-Lond. 184, 170.
3. Woledge, R. C., Curtin, N. A. & Homsher, E. 1985 Energetic aspects of muscle contraction. Monogr. Physiol. Soc. 41, 1-357.
4. Wells, J. B. 1965 Comparison of mechanical properties between slow and fast mammalian muscles. J. Physiol. 178, 252-269.
5. Powell, P. L., Roy, R. R., Kanim, P., Bello, M. A. & Edgerton, V. R. 1984 Predictability of skeletal-muscle tension from architectural determinations in guinea-pig hindlimbs. J. Appl. Physiol. 57, 1715-1721.
6. Alexander, R. M. 2003 Principles of animal locomotion. Princeton, NJ: Princeton University Press.
7. Biewener, A. A. 2003 Animal locomotion. Oxford, UK: Oxford University Press.
8. Hudson, P. E., Corr, S. A., Payne-Davis, R. C., Clancy, S. N., Lane, E. & Wilson, A. M. In press. Functional anatomy of the cheetah (Acinonyx jubatus) hindlimb. J. Anat. (doi:10.1111/j.1469-7580.2010.01310.x)
9. Williams, S. B., Payne, R. C. & Wilson, A. M. 2007 Functional specialisation of the pelvic limb of the hare (Lepus europeus). J. Anat. 210, 472-490. (doi:10.1111/j.1469-7580.2007.00704.x)
10. Biewener, A. A. & Roberts, T. J. 2000 Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc. Sport Sci. Rev. 28, 99-107.
11. Hill, A. V. 1938 The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B 126, 136. (doi:10.1098/rspb.1938.0050)
12. Hill, A. V. 1950 The series elastic component of muscle. Proc. R. Soc. Lond. B 137, 273-280. (doi:10.1098/rspb.1950.0035)
13. Zajac, F. E. 1989 Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17, 359-411.
14. Huxley, A. F. & Simmons, R. M. 1970 A quick phase in the series-elastic component of striated muscle, demonstrated in isolated fibres from the frog. J. Physiol. 208, 52P-53P.
15. Yamamoto, T. & Herzig, J. W. 1978 Series elastic properties of skinned muscle fibres in contraction and rigor. Pflugers Arch. 373, 21-24. (doi:10.1007/BF00581144)
16. Curtin, N. A., Gardner-Medwin, A. R. & Woledge, R.C. 1998 Predictions of the time course of force and power output by dogfish white muscle fibres during brief tetani. J. Exp. Biol. 201, 103-114.
17. Alexander, R. M. 2002 Tendon elasticity and muscle function. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133, 1001-1011. (doi:10.1016/S1095-6433(02)00143-5)
18. Nigg, B. M. & Herzog, W. 2007 Biomechanics of the musculo-skeletal system, 3rd edn. New York, NY: Wiley.
19. Josephson, R. K. 1985 Mechanical power output from striated-muscle during cyclic contraction. J. Exp. Biol. 114, 493-512.
20. Josephson, R. K. 1993 Contraction dynamics and power output of skeletal muscle. Annu. Rev. Physiol. 55, 527-546. (doi:10.1146/annurev.ph.55.030193.002523)
21. Curtin, N. & Woledge, R. 1996 Power at the expense of efficiency in contraction of white muscle fibres from dogfish Scyliorhinus canicula. J. Exp. Biol. 199, 593-601.
22. Lichtwark, G. A. & Barclay, C. J. 2010 The influence of tendon compliance on muscle power output and efficiency during cyclic contractions. J. Exp. Biol. 213, 707-714. (doi:10.1242/jeb.038026)
23. Josephson, R. K. 1989 Power output from skeletalmuscle during linear and sinusoidal shortening. J. Exp. Biol. 147, 533-537.
24. Biewener, A. A. 1998 Muscle function in vivo: a comparison of muscles used for elastic energy savings versus muscles used to generate mechanical power. Am. Zool. 38, 703-717.
25. Roberts, T. J., Marsh, R. L., Weyand, P. G. & Taylor, C. R. 1997 Muscular force in running turkeys: the economy of minimizing work. Science 275, 1113-1115. (doi:10.1126/science.275.5303.1113)
26. Bobbert, M. F., Gerritsen, K. G. M., Litjens, M. C. A. & VanSoest, A. J. 1996 Why is countermovement jump height greater than squat jump height? Med. Sci. Sports Exerc. 28, 1402-1412.
27. Asmussen, E. & Sorensen, N. 1971 Wind-up movement in athletics. Travail Humain. 34, 147-150.
28. Lichtwark, G. A. & Wilson, A. M. 2005 Effects of series elasticity and activation conditions on muscle power output and efficiency. J. Exp. Biol. 208, 2845-2853. (doi:10.1242/jeb.01710)
29. Lichtwark, G. A. & Wilson, A. M. 2006 Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion. J. Exp. Biol. 209, 4379-4388. (doi:10.1242/jeb.02434)
30. Roberts, T. J. 2002 The integrated function of muscles and tendons during locomotion. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133, 1087-1099. (doi:10.1016/S1095-6433(02)00244-1)
31. Lichtwark, G. A. & Wilson, A. M. 2005 A modified Hill muscle model that predicts muscle power output and efficiency during sinusoidal length changes. J. Exp. Biol. 208, 2831-2843. (doi:10.1242/jeb.01709)
32. Alexander, R. M. 1997 Optimum muscle design for oscillatory movements. J. Theor. Biol. 184, 253-259. (doi:10.1006/jtbi.1996.0271)
33. Lichtwark, G. A. & Wilson, A. M. 2005 In vivo mechanical properties of the human Achilles tendon during onelegged hopping. J. Exp. Biol. 208, 4715-4725. (doi:10.1242/jeb.01950)
34. Maganaris, C. N. & Paul, J. P. 2002 Tensile properties of the in vivo human gastrocnemius tendon. J. Biomech. 35, 1639-1646. (doi:10.1016/S0021-9290(02)00240-3)
35. Wren, T. A., Lindsey, D. P., Beaupre, G. S. & Carter, D. R. 2003 Effects of creep and cyclic loading on the mechanical properties and failure of human Achilles tendons. Ann. Biomed. Eng. 31, 710-717. (doi:10.1114/1.1569267)
36. Kawakami, Y., Muraoka, T., Ito, S., Kanehisa, H. & Fukunaga, T. 2002 In vivo muscle fibre behaviour during counter-movement exercise in humans reveals a significant role for tendon elasticity. J. Physiol.-Lond. 540, 635-646. (doi:10.1113/jphysiol.2001.013459)
37. Komi, P. V. 1990 Relevance of in vivo force measurements to human biomechanics. J. Biomech. 23(Suppl. 1), 23-34. (doi:10.1016/0021-9290(90)90038-5)
38. Lichtwark, G. A. & Wilson, A. M. 2007 Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? J. Biomech. 40, 1768-1775. (doi:10.1016/j.jbiomech.2006.07.025)
39. Lichtwark, G. A. & Wilson, A. M. 2008 Optimal muscle fascicle length and tendon stiffness for maximising gastrocnemius efficiency during human walking and running. J. Theor. Biol. 252, 662-673. (doi:10.1016/j.jtbi.2008.01.018)
40. Biewener, A. A. 1989 Scaling body support in mammals: limb posture and muscle mechanics. Science 245, 45-48. (doi:10.1126/science.2740914)
41. Daley, M. & Biewener, A. A. 2011 Leg muscles that mediate stability: mechanics and control of two distal extensor muscles during obstacle negotiation in the guinea fowl. Phil. Trans. R. Soc. B 366, 1580-1591. (doi:10.1098/rstb.2010.0338)
42. Daley, M. A. & Biewener, A. A. 2003 Muscle force- length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors. J. Exp. Biol. 206, 2941-2958. (doi:10.1242/jeb.00503)
43. Ker, R. F. 1981 Dynamic tensile properties of the plantaris tendon of sheep (Ovis-Aries). J. Exp. Biol. 93, 283-302.
44. Lichtwark, G. A., Watson, J. C., Mavrommatis, S. & Wilson, A. M. 2009 Intensity of activation and timing of deactivation modulate elastic energy storage and release in a pennate muscle and account for gait-specific initiation of limb protraction in the horse. J. Exp. Biol. 212, 2454-2463. (doi:10.1242/jeb.027995)
45. Collins, J. A. 2009 Mechanical design of machine elements and machines: a failure prevention perspective, 2nd ed., pp. 584-585. Hoboken, NJ: Wiley.
46. Budynas, R. G. & Nisbett, J. K. 2008 Shigley's mechanical engineering design (SI units). London, UK: McGraw-Hill Higher Education.
47. Wilson, A. M., McGuigan, M. P., Su, A. & van Den Bogert, A. J. 2001 Horses damp the spring in their step. Nature 414, 895-899. (doi:10.1038/414895a)
48. Wilson, A. M., Watson, J. C. & Lichtwark, G. A. 2003 Biomechanics: a catapult action for rapid limb protraction. Nature 421, 35-36. (doi:10.1038/421035a)
49. Hof, A. L. 1998 In vivo measurement of the series elasticity release curve of human triceps surae muscle. J. Biomech. 31, 793-800. (doi:10.1016/S0021-9290(98)00062-1)
50. de Zee, M. & Voigt, M. 2001 Moment dependency of the series elastic stiffness in the human plantar flexors measured in vivo. J. Biomech. 34, 1399-1406. (doi:10.1016/S0021-9290(01)00133-6)
51. Chan, A. K., Edgerton, V. R., Goslow, G. E., Kurata, H., Rasmussen, S. A. & Spector, S. A. 1982 Histochemical and physiological-properties of cat motor units after self-reinnervation and cross-reinnervation. J. Physiol.-Lond. 332, 343-361.
52. Arampatzis, A., Karamanidis, K., Morey-Klapsing, G., De Monte, G. & Stafilidis, S. 2007 Mechanical properties of the triceps surae tendon and aponeurosis in relation to intensity of sport activity. J. Biomech. 40, 1946-1952. (doi:10.1016/j.jbiomech.2006.09.005)
53. Rosager, S., Aagaard, P., Dyhre-Poulsen, P., Neergaard, K., Kjaer, M. & Magnusson, S. P. 2002 Load-displacement properties of the human triceps surae aponeurosis and tendon in runners and non-runners. Scand. J. Med. Sci. Sports 12, 90-98. (doi:10.1034/j.1600-0838.2002.120205.x)
54. Scholz, M. N., Bobbert, M. F., van Soest, A. J., Clark, J. R. & van Heerden, J. 2008 Running biomechanics: shorter heels, better economy. J. Exp. Biol. 211, 3266-3271. (doi:10.1242/jeb.018812)
55. Lee, S. S. M. & Piazza, S. J. 2009 Built for speed: musculoskeletal structure and sprinting ability. J. Exp. Biol. 212, 3700-3707. (doi:10.1242/jeb.031096)
56. Biewener, A. A. 2005 Biomechanical consequences of scaling. J. Exp. Biol. 208, 1665-1676. (doi:10.1242/jeb.01520)
57. Blickhan, R. 1989 The spring mass model for running and hopping. J. Biomech. 22, 1217-1227. (doi:10.1016/0021-9290(89)90224-8)
58. Mcmahon, T. A. & Cheng, G. C. 1990 The mechanics of running: how does stiffness couple with speed. J. Biomech. 23, 65-78. (doi:10.1016/0021-9290(90)90042-2)
59. Cavagna, G. A., Heglund, N. C. & Taylor, C. R. 1977 Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. Am. J. Physiol. 233, R243-R261.
60. Witte, T. H., Knill, K. & Wilson, A. A. 2004 Determination of peak vertical ground reaction force from duty factor in the horse (Equus caballus). J. Exp. Biol. 207, 3639-3648. (doi:10.1242/jeb.01182)
61. Weyand, P. G., Sternlight, D. B., Bellizzi, M. J. & Wright, S. 2000 Faster top running speeds are achieved with greater ground forces not more rapid leg movements. J. Appl. Physiol. 89, 1991-1999.
62. Vos, N. J. & Riemersma, D. J. 2006 Determination of coefficient of friction between the equine foot and different ground surfaces: an in vitro study. Equine Comp. Exerc. Physiol. 3, 191-198. (doi:10.1017/S1478061506617234)
63. Galantis, A. & Woledge, R. C. 2003 The theoretical limits to the power output of a muscle-tendon complex with inertial and gravitational loads. Proc. R. Soc. Lond. B 270, 1493-1498. (doi:10.1098/rspb.2003.2403)
64. Roberts, T. J. & Marsh, R. L. 2003 Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs. J. Exp. Biol. 206, 2567-2580. (doi:10.1242/jeb.00452)
65. Bennet-Clark, H. C. 1975 The energetics of the jump of the locust Schistocerca gregaria. J. Exp. Biol. 63, 53-83.
66. Usherwood, J. R. & Wilson, A. M. 2005 No force limit on greyhound sprint speed. Nature 438, 753-754. (doi:10.1038/438753a)
67. Witte, T. H., Hirst, C. V. & Wilson, A. M. 2006 Effect of speed on stride parameters in racehorses at gallop in field conditions. J. Exp. Biol. 209, 4389-4397. (doi:10.1242/jeb.02518)
68. Williams, S. B., Tan, H. L., Usherwood, J. R. & Wilson, A. M. 2009 Pitch then power: limitations to acceleration in quadrupeds. Biol. Lett. 5, 610-613. (doi:10.1098/rsbl.2009.0360)
69. Tan, H. & Wilson, A. M. In press. Grip and limb force limits to turning performance in competition horses. Proc. R. Soc. B. (doi:10.1098/rspb.2010.2395)
70. Van Leeuwen, J. L. & Spoor, C. W. 1993 Modelling the pressure and force equilibrium in unipennate muscles with in-line tendons. Phil. Trans. R. Soc. B. 342, 321-333. (doi:10.1098/rstb.1993.0162)