On the ascent: The soleus operating length is conserved to the ascending limb of the force-length curve across gait mechanics in humans

Journal of Experimental Biology

Volumn 215, Issue 20, 2012, Pages 3539-3551

  Rubenson, Jonas ^a   Pires, Neville J ^a   Loi, Heok O ^a   Pinniger, Gavin J ^a   Shannon, Damian G ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Force length; Gait; Locomotion; Muscle length; Soleus

Indexed keywords

ADULT; ARTICLE; BIOMECHANICS; GAIT; HUMAN; MALE; MECHANICAL STRESS; MECHANICAL TORSION; MUSCLE CONTRACTION; PHYSIOLOGY; RUNNING; SKELETAL MUSCLE; TENDON; TORQUE; WALKING;

ADULT; BIOMECHANICS; GAIT; HUMANS; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; RUNNING; STRESS, MECHANICAL; TENDONS; TORQUE; TORSION, MECHANICAL; WALKING;

EID: 84866853539     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.070466     Document Type: Article

References (58)

1. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36-42.
2. An, K. N., Takahashi, K., Harrigan, T. P. and Chao, E. Y. (1984). Determination of muscle orientations and moment arms. J. Biomech. Eng. 106, 280-282.
3. Arampatzis, A., De Monte, G. and Morey-Klapsing, G. (2007). Effect of contraction form and contraction velocity on the differences between resultant and measured ankle joint moments. J. Biomech. 40, 1622-1628.
4. Arnold, E. M. and Delp, S. L. (2011). Fibre operating lengths of human lower limb muscles during walking. Philos. Trans. R. Soc. B 366, 1530-1539.
5. Arnold, E. M., Ward, S. R., Lieber, R. L. and Delp, S. L. (2010). A model of the lower limb for analysis of human movement. Ann. Biomed. Eng. 38, 269-279.
6. Azizi, E. and Roberts, T. J. (2010). Muscle performance during frog jumping: influence of elasticity on muscle operating lengths. Proc. R. Soc. Lond. B 277, 1523-1530.
7. Behm, D. G., St-Pierre, D. M. and Perez, D. (1996). Muscle inactivation: assessment of interpolated twitch technique. J. Appl. Physiol. 81, 2267-2273.
8. Bellemare, F., Woods, J. J., Johansson, R. and Bigland-Ritchie, B. (1983). Motorunit discharge rates in maximal voluntary contractions of three human muscles. J. Neurophysiol. 50, 1380-1392.
9. Besier, T. F., Sturnieks, D. L., Alderson, J. A. and Lloyd, D. G. (2003). Repeatability of gait data using a functional hip joint centre and a mean helical knee axis. J. Biomech. 36, 1159-1168.
10. Burkholder, T. J. and Lieber, R. L. (2001). Sarcomere length operating range of vertebrate muscles during movement. J. Exp. Biol. 204, 1529-1536.
11. Costa, M. L., Logan, K., Heylings, D., Donell, S. T. and Tucker, K. (2006). The effect of Achilles tendon lengthening on ankle dorsiflexion: a cadaver study. Foot Ankle Int. 27, 414-417.
12. Cronin, N. J., Ishikawa, M., Grey, M. J., af Klint, R., Komi, P. V., Avela, J., Sinkjaer, T. and Voigt, M. (2009). Mechanical and neural stretch responses of the human soleus muscle at different walking speeds. J. Physiol. 587, 3375-3382.
13. Cutts, A. (1989). Sarcomere length changes in muscles of the human thigh during walking. J. Anat. 166, 77-84.
14. Delp, S. L., Anderson, F. C., Arnold, A. S., Loan, P., Habib, A., John, C. T., Guendelman, E. and Thelen, D. G. (2007). OpenSim: open-source software to create and analyze dynamic simulations of movement. IEEE Trans. Biomed. Eng. 54, 1940-1950.
15. De Luca, C. J. (1985). Control properties of motor units. J. Exp. Biol. 115, 125-136.
16. Fukunaga, T., Kawakami, Y., Kubo, K. and Kanehisa, H. (2002). Muscle and tendon interaction during human movements. Exerc. Sport Sci. Rev. 30, 106-110.
17. Gao, F., Grant, T. H., Roth, E. J. and Zhang, L. Q. (2009). Changes in passive mechanical properties of the gastrocnemius muscle at the muscle fascicle and joint levels in stroke survivors. Arch. Phys. Med. Rehabil. 90, 819-826.
18. Gollapudi, S. K. and Lin, D. C. (2009). Experimental determination of sarcomere force-length relationship in type-I human skeletal muscle fibers. J. Biomech. 42, 2011-2016.
19. Gordon, A. M., Huxley, A. F. and Julian, F. J. (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184, 170-192.
20. Hamner, S. R., Seth, A. and Delp, S. L. (2010). Muscle contributions to propulsion and support during running. J. Biomech. 43, 2709-2716.
21. Herbert, R. D., Clarke, J., Kwah, L. K., Diong, J., Martin, J., Clarke, E. C., Bilston, L. E. and Gandevia, S. C. (2011). In vivo passive mechanical behaviour of muscle fascicles and tendons in human gastrocnemius muscle-tendon units. J. Physiol. 589, 5257-5267.
22. Herzog, W., Leonard, T. R., Renaud, J. M., Wallace, J., Chaki, G. and Bornemisza, S. (1992). Force-length properties and functional demands of cat gastrocnemius, soleus and plantaris muscles. J. Biomech. 25, 1329-1335.
23. Hill, A. V. (1953). The mechanics of active muscle. Proc. R. Soc. Lond. B 141, 104-117.
24. Hoang, P. D., Herbert, R. D., Todd, G., Gorman, R. B. and Gandevia, S. C. (2007). Passive mechanical properties of human gastrocnemius muscle tendon units, muscle fascicles and tendons in vivo. J. Exp. Biol. 210, 4159-4168.
25. Hodgson, J. A., Finni, T., Lai, A. M., Edgerton, V. R. and Sinha, S. (2006). Influence of structure on the tissue dynamics of the human soleus muscle observed in MRI studies during isometric contractions. J. Morphol. 267, 584-601.
26. Hof, A. L. and van den Berg, J. (1977). Linearity between the weighted sum of the EMGs of the human triceps surae and the total torque. J. Biomech. 10, 529-539.
27. Julian, F. J. and Morgan, D. L. (1979). Intersarcomere dynamics during fixed-end tetanic contractions of frog muscle fibres. J. Physiol. 293, 365-378.
28. Kawakami, Y., Amemiya, K., Kanehisa, H., Ikegawa, S. and Fukunaga, T. (2000). Fatigue responses of human triceps surae muscles during repetitive maximal isometric contractions. J. Appl. Physiol. 88, 1969-1975.
29. Lichtwark, G. A. and Wilson, A. M. (2005). Effects of series elasticity and activation conditions on muscle power output and efficiency. J. Exp. Biol. 208, 2845-2853.
30. Lichtwark, G. A., Bougoulias, K. and Wilson, A. M. (2007). Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J. Biomech. 40, 157-164.
31. Lieber, R. L. and Ward, S. R. (2011). Skeletal muscle design to meet functional demands. Philos. Trans. R. Soc. B 366, 1466-1476.
32. Lutz, G. J. and Rome, L. C. (1994). Built for jumping: the design of the frog muscular system. Science 263, 370-372.
33. MacIntosh, B. R. and MacNaughton, M. B. (2005). The length dependence of muscle active force: considerations for parallel elastic properties. J. Appl. Physiol. 98, 1666-1673.
34. Maganaris, C. N. (2001). Force-length characteristics of in vivo human skeletal muscle. Acta Physiol. Scand. 172, 279-285.
35. Maganaris, C. N. (2004). Imaging-based estimates of moment arm length in intact human muscle-tendons. Eur. J. Appl. Physiol. 91, 130-139.
36. Manal, K., Cowder, J. D. and Buchanan, T. S. (2010). A hybrid method for computing Achilles tendon moment arm using ultrasound and motion analysis. J. Appl. Biomech. 26, 224-228.
37. Martin, D. C., Medri, M. K., Chow, R. S., Oxorn, V., Leekam, R. N., Agur, A. M. and McKee, N. H. (2001). Comparing human skeletal muscle architectural parameters of cadavers with in vivo ultrasonographic measurements. J. Anat. 199, 429-434.
38. McGowan, C. P., Kram, R. and Neptune, R. R. (2009). Modulation of leg muscle function in response to altered demand for body support and forward propulsion during walking. J. Biomech. 42, 850-856.
39. Morgan, D. L. (1990). New insights into the behavior of muscle during active lengthening. Biophys. J. 57, 209-221.
40. Narici, M. V. and Maganaris, C. N. (2007). Plasticity of the muscle-tendon complex with disuse and aging. Exerc. Sport Sci. Rev. 35, 126-134.
41. Neptune, R. R. and Sasaki, K. (2005). Ankle plantar flexor force production is an important determinant of the preferred walk-to-run transition speed. J. Exp. Biol. 208, 799-808.
42. Neptune, R. R., Sasaki, K. and Kautz, S. A. (2008). The effect of walking speed on muscle function and mechanical energetics. Gait Posture 28, 135-143.
43. Pinniger, G. J. and Cresswell, A. G. (2007). Residual force enhancement after lengthening is present during submaximal plantar flexion and dorsiflexion actions in humans. J. Appl. Physiol. 102, 18-25.
44. Pinniger, G. J., Steele, J. R., Thorstensson, A. and Cresswell, A. G. (2000). Tension regulation during lengthening and shortening actions of the human soleus muscle. Eur. J. Appl. Physiol. 81, 375-383.
45. Rack, P. M. and Westbury, D. R. (1969). The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J. Physiol. 204, 443-460.
46. Ralston, H. J. (1958). Energy-speed relation and optimal speed during level walking. Int. Z. Angew. Physiol. 17, 277-283.
47. Rassier, D. E. and Herzog, W. (2004). Considerations on the history dependence of muscle contraction. J. Appl. Physiol. 96, 419-427.
48. Rassier, D. E., MacIntosh, B. R. and Herzog, W. (1999). Length dependence of active force production in skeletal muscle. J. Appl. Physiol. 86, 1445-1457.
49. Rome, L. C. and Sosnicki, A. A. (1991). Myofilament overlap in swimming carp. II. Sarcomere length changes during swimming. Am. J. Physiol. 260, C289-C296.
50. Rome, R. (1998). Matching muscle performance to changing demand. In Principles of Animal Design (ed. R. W. Ewald, C. R. Taylor and L. Bolis), pp. 103-113. Cambridge, UK: Cambridge University Press.
51. Rubenson, J., Heliams, D. B., Maloney, S. K., Withers, P. C., Lloyd, D. G. and Fournier, P. A. (2007). Reappraisal of the comparative cost of human locomotion using gait-specific allometric analyses. J. Exp. Biol. 210, 3513-3524.
52. Sasaki, K. and Neptune, R. R. (2006). Muscle mechanical work and elastic energy utilization during walking and running near the preferred gait transition speed. Gait Posture 23, 383-390.
53. Walker, S. M. and Schrodt, G. R. (1974). I segment lengths and thin filament periods in skeletal muscle fibers of the Rhesus monkey and the human. Anat. Rec. 178, 63-81.
54. Ward, S. R., Eng, C. M., Smallwood, L. H. and Lieber, R. L. (2009). Are current measurements of lower extremity muscle architecture accurate? Clin. Orthop. Relat. Res. 467, 1074-1082.
55. Winter, D. A. (1990). Biomechanics and Motor Control of Human Movement. New York, NY: John Wiley and Sons.
56. Winters, T. M., Takahashi, M., Lieber, R. L. and Ward, S. R. (2011). Whole muscle length-tension relationships are accurately modeled as scaled sarcomeres in rabbit hindlimb muscles. J. Biomech. 44, 109-115.
57. Wu, G., Siegler, S., Allard, P., Kirtley, C., Leardini, A., Rosenbaum, D., Whittle, M., DLima, D. D., Cristofolini, L., Witte, H. et al. (2002). ISB recommendation on definitions of joint coordinate system of various joints for the reporting of human joint motion -part I: ankle, hip, and spine. J. Biomech. 35, 543-548.
58. Zajac, F. E. (1989). Muscle and tendon: properties, models, scaling and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17, 359-411.