Elastic recoil can either amplify or attenuate muscle-tendon power, depending on inertial vs. fluid dynamic loading

Journal of Theoretical Biology

Volumn 313, Issue , 2012, Pages 68-78

  Richards, Christopher T ^a   Sawicki, Gregory S ^b  

^a HARVARD UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Gearing; Inertial and viscous loads; Mathematical model; Mechanical advantage; Muscle power amplification

Indexed keywords

ENERGY; FLUID DYNAMICS; MUSCLE; NUMERICAL MODEL; SWIMMING;

ARTICLE; BIOENERGY; BIOMECHANICS; CONTRACTILE ELEMENT; ELASTIC COIL; ENERGY RESOURCE; FLUID DYNAMIC LOADING; INERTIAL LOADING; MATHEMATICAL MODEL; MUSCLE CONTRACTION; MUSCLE MASS; MUSCLE STRENGTH; MUSCLE TENDON POWER; MUSCULOSKELETAL SYSTEM PARAMETERS; PREDICTION; PRIORITY JOURNAL; SERIES ELASTIC ELEMENT; SKELETAL MUSCLE; VELOCITY;

ANIMALS; BIOMECHANICAL PHENOMENA; COMPUTER SIMULATION; ELASTICITY; HYDRODYNAMICS; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; TENDONS; XENOPUS LAEVIS;

ANURA;

EID: 84865556512     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2012.07.033     Document Type: Article

References (40)

1. Aerts P. Vertical jumping in Galago senegalensis: the quest for an obligate mechanical power amplifier. Philos. Trans. R. Soc. London, Ser. B: Biol. Sci. 1998, 353:1607-1620.
2. Aerts P., Nauwelaerts S. Environmentally induced mechanical feedback in locomotion: frog performance as a model. J. Theor. Biol. 2009, 261:372-378.
3. Alexander R. Optimum muscle design for oscillatory movements. J. Theor. Biol. 1997, 184:253-259.
4. Astley H.C., Roberts T.J. Evidence for a vertebrate catapult: elastic energy storage in the plantaris tendon during frog jumping. Biol. Lett. 2011.
5. Azizi E., Roberts T.J. Muscle performance during frog jumping: influence of elasticity on muscle operating lenghts. Proc. R. Soc. London, Ser. B. Biol. Sci. 2010, 277:1523-1530.
6. Bennet-Clark H.C., Lucey E.C.A. The jump of the flea: a study of the energetics and a model of the mechanism. J. Exp. Biol. 1967, 47:59-76.
7. Carrier D., Heglund N., Earls K. Variable gearing during locomotion in the human musculoskeletal system. Science 1994, 265:651-653.
8. Carrier D., Gregersen C., Silverton N. Dynamic gearing in running dogs. J. Exp. Biol. 1998, 201:3185-3195.
9. Clemente C.J., Richards C.T. Determining the influence of muscle operating length on muscle performance during frog swimming using a bio-robotic model. Bioinspiration Biomimetics 2012, 7(036018):12.
10. Curtin N.A., Gardner-Medwin A.R., Woledge R.C. Predictions of the time course of force and power output by dogfish white muscle fibers during brief tetani. J. Exp. Biol. 1998, 201:103-114.
11. Edman K. Mechanical deactivation induced by active shortening in isolated muscle fibres of the frog. J. Physiol. 1975, 246:255-275.
12. Emerson S.B. Allometry and Jumping in frogs: helping the twain to meet. Evolution 1978, 32:551-564.
13. Gal J.M., Blake R.W. Biomechanics of frog swimming: I. Estimation of the propulsive force generated by Hymenochirus boettgeri. J. Exp. Biol. 1988, 138:399-411.
14. Galantis A., Woledge R.C. The theoretical limits to the power output of a muscle-tendon complex with inertial and gravitational loads. Proc. R. Soc. London, Ser. B: Biol. Sci. 2003, 270:1493.
15. Gordon A.M., Huxley A.F., Julian F.J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 1966, 184:170-192.
16. Gray P., Mill P. The mechanics of the predatory strike of the praying mantid Heirodula membranacea. J. Exp. Biol. 1983, 107:245.
17. Hedrick T.L., Tobalske B.W., Biewener A.A. How cockatiels (Nymphicus hollandicus) modulate pectoralis power output across flight speeds 10.1242/jeb.00272. J. Exp. Biol. 2003, 206:1363-1378.
18. Hill A.V. The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. London, Ser. B: Biol. Sci. 1938, 126:136-195.
19. Hoerner S.F. Fluid Dynamic Drag 1965, Published by the author, Midland Park, NJ.
20. James R.S., Wilson R.S. Explosive jumping: extreme morphological and physiological specializations of Australian rocket frogs (Litoria nasuta). Physiol. Biochem. Zool. 2008, 81(2):176-185.
21. Johansson L.C., Lauder G.V. Hydrodynamics of surface swimming in leopard frogs (Rana pipiens). J. Exp. Biol. 2004, 207:3945-3958.
22. Josephson R., Stokes D. Work-dependent deactivation of a crustacean muscle. J. Exp. Biol. 1999, 202:2551-2565.
23. Lutz G.J., Rome L.C. Built for jumping: the design of the frog muscular system. Science 1994, 263:370-372.
24. Marsh R., John-Alder H. Jumping performance of hylid frogs measured with high-speed cine film. J. Exp. Biol. 1994, 188:131-141.
25. Nauwelaerts S., Aerts P. Propulsive impulse as a covarying performance measure in the comparison of the kinematics of swimming and jumping in frogs 10.1242/jeb.00690. J. Exp. Biol. 2003, 206:4341-4435.
26. Nauwelaerts S., Stamhuis E.J., Aerts P. Propulsive force calculations in swimming frogs I. A momentum-impulse approach 10.1242/jeb.01509. J. Exp. Biol. 2005, 208:1435-1443.
27. Otten E. A myocybernetic model of the jaw system of the rat. J. Neurosci. Methods 1987, 21:287-302.
28. Peplowski M., Marsh R. Work and power output in the hindlimb muscles of Cuban tree frogs Osteopilus septentrionalis during jumping. J. Exp. Biol. 1997, 200:2861-2870.
29. Peters S.E., Kamel L.T., Bashor D.P. Hopping and swimming in the Leopard Frog, Rana pipiens: I. step cycles and kinematics. J. Morphol. 1996, 230:1-16.
30. Reilly S.M., Jorgensen M.E. The evolution of jumping in frogs: morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans. J. Morphol. 2011, 272:149-188.
31. Richards C.T., Biewener A.A. Modulation of in vivo muscle power output during swimming in the African clawed frog (Xenopus laevis). J. Exp. Biol. 2007, 210:3147-3159.
32. Richards C.T. The kinematic determinants of anuran swimming performance: an inverse and forward dynamics approach. J. Exp. Biol. 2008, 211:3181-3194. 10.1242/jeb.019844.
33. Richards C.T. Kinematics and hydrodynamics analysis of swimming anurans reveals striking inter-specific differences in the mechanism for producing thrust. J. Exp. Biol. 2010, 213:621-634.
34. Richards C.T. Building a robotic link between muscle dynamics and hydrodynamics. J. Exp. Biol. 2011, 214:2381-2389.
35. Richards, C. T. and Clemente, C. J., 2012. A bio-robotic platform for integrating internal and external mechanics during muscle-powered swimming. Bioinspiration Biomimetics, 7, 016010.
36. Roberts T.J., Marsh R.L. Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs 10.1242/jeb.00452. J. Exp. Biol. 2003, 206:2567-2580.
37. Rome L.C., Funke R.P., Alexander R.M., Lutz G., Aldridge H., Scott F., Freadman M. Why animals have different muscle fibre types. Nature 1988, 335:824-827.
38. Sheppard, P., Sawicki, G. S., Roberts, T.J. (2009). Power augmentation in a compliant muscle-tendon system. 33rd Annual Meeting of American Society of Biomechanics, August 26-29, State College, Pennsylvania.
39. Shubin N.H., Jenkins, F.A. An early jurassic jumping frog. Nature 1994, 377:49-52.
40. Zajac F.E. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 1989, 17:359.