Subtle Nonlinear Neuromuscular Properties Are Consistent with Teleological Design Principles

  • Jack M. Winters
  • Robert E. Kearney
  • Michael P. Slawnych
  • Peter A. Huijing
Chapter

Abstract

The other chapters in this section address certain subtle details of neuromuscular properties, such as interaction between properties (e.g., activation and contractile force-length) and effects of fatigue (see Chapters 5 and 6, Huijing), convergence of information on motoneurons (see Chapter 2), and muscle force-length operating range variability (see Chapter 3). In general, such details may be interpreted as adding complexity to neuromusculoskeletal (NMS) models, and there is thus a natural resistance on the part of modellers to include every single observed behavior. Yet this opens the door to a criticism of models as not being sufficiently accurate, and therefore inadequate; this was a recurring theme during several of the discussions at the recent EFC on Biomechanics and Neural Control of Movement. It needs to be addressed.

Keywords

Fatigue Torque Stein Alexan 

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References

  1. Alexander, R.McN. (1988). Elastic Mechanisms in Animal Movement. Cambridge University Press, Cambridge.Google Scholar
  2. Alexander, R.McN. and Ker, R.F. (1990). The architecture of leg muscles. In Multiple Muscle Systems: Biomech. and Movem. Organiz., Winters, J.M. and Woo, S.Y. (eds.), Chapter 36, pp. 568–577, Springer-Verlag, New York.Google Scholar
  3. Beek, P.J., Peper, C.E., and Stegeman, D.F. (1995). Dynamical models of movement coordination, Hum. Mov. Sci., 14:573–608.CrossRefGoogle Scholar
  4. Bernstein, N. (1935, 1967). The Coordination and Regulation of Movements. Pergamon, New York.Google Scholar
  5. Cannon, S.C. and Zahalak, G.I. (1982). The mechanical behavior of active human skeletal muscle in small oscillations. J. Biomech., 15:111.PubMedCrossRefGoogle Scholar
  6. Cavagna, G.A. (1970). Elastic bounce in the body. J. Appl. Physiol., 29:279–282.PubMedGoogle Scholar
  7. Close, R. (1969). Dynamic properties of fast and slow skeletal muscles of the rat after nerve cross-union. J. Physiol., 204:331–346.PubMedGoogle Scholar
  8. Edman, K.A.P., Elzinga, G., and Noble, M.I.M. (1978). Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J. Physiol., 280:139–155.Google Scholar
  9. Faulkner, J.A., Claflin, D.R., and McCully, K.K. (1986). Power output of fast and slow fibers from human skeletal muscles. In Human Muscle Power. Human Kinetics, Champaign.Google Scholar
  10. Feldman, A.G. (1986). Once more on the equilibrium-point hypothesis (λ model) for motor control. J. Motor Behav., 18:17–54.Google Scholar
  11. Feldman, A.G., Adamovich, S.V., Ostry, D.J., and Flanagan, J.R. (1990). The origin of electromyograms—Explanations based on the equilibrium point hypothesis. In Multiple Muscle Systems. Winters, J.M. and Woo, S.L-Y. (eds.), Chapter 12, pp. 195–213, Springer-Verlag, New York.Google Scholar
  12. Fung, Y.C. (1993). Biomechanics: Mechanical Properties of Living Tissues. 2nd ed., Springer-Verlag, New York.Google Scholar
  13. Gauthier, G.M, Martin, B.J., and Stark, L. (1986). Adapted head and eye movement responses to added-head inertia. Aviat. Space Environ. Med., 57:336–342.PubMedGoogle Scholar
  14. Hannaford, B. and Winters, J.M. (1990). Actuator properties and movement control: biological and technological models. In Multiple Muscle Systems. Winters, J.M. and Woo, S.L-Y. (eds.), Ch. 7, pp. 101–120, Springer-Verlag, New York.Google Scholar
  15. Henneman, E., Somjen, G., and Carpenter, D. (1965). Excitability and inhibitability of motoneurons of different sizes. J. Neurobiol., 28:599–620.Google Scholar
  16. Hill, A.V. (1970). First and Last Experiments in Muscle Mechanics. Cambridge University Press, Cambridge.Google Scholar
  17. Hoffer, J.A. and Andreasson, S. (1981). Regulation of soleus muscle stiffness in premammillary cats: intrinsic and reflex components. J. Neurophys., 45:267–285.Google Scholar
  18. Hogan, N. (1990). Mechanical impedance of single- and multi-articular systems. In Multiple Muscle Systems. Winters, J.M. and Woo, S.Y. (eds.), Chapter 9, pp. 149–164, Springer-Verlag, New York.Google Scholar
  19. Houk, J.C. (1979). Regulation of stiffness by skeleto-motor reflexes. Ann. Rev. Physiol., 41:99–114.CrossRefGoogle Scholar
  20. Houk, J.C. and Rymer, W.Z. (1981). Neural control of muscle length and tension. Handbook of Physiol. The Nervous System II, Chapter 8, pp. 257–323.Google Scholar
  21. Lacquaniti, F.F., Licata, R., and Soetching, J.F. (1982). The mechanical behavior of the human forearm in response to transient perturbations. Biol. Cybern., 44:35–46.PubMedCrossRefGoogle Scholar
  22. Loeb, G.E. (1984). The control and response of mammalian muscle spindles during normally executed motor tasks. Exerc. Sport Rev., 12:157–204.Google Scholar
  23. Mannard, A. and Stein, R.B. (1973). Determination of the frequency response of isometric soleus muscle in the cat using random nerve stimulation. J. Physiol., 229:275–296.PubMedGoogle Scholar
  24. Matthews, P.B.C. (1981). Muscle Spindles: their messages and their fusimotor supply. In Handbook of Physiology. The Nervous System II, Brooks, V.B. (ed.), pp. 189–228, Bethesda, Maryland, American Physiological Society.Google Scholar
  25. McMahon, T.A. (1984). Muscles, Reflexes and Locomotion. Princeton University Press, Princeton.Google Scholar
  26. McMahon, T.A. (1990). Spring-like properties of muscle and reflexes in running. In Multiple Muscle Systems. Winters, J.M. and Woo, S.Y. (eds.), Chapter 5, pp. 69–93, Springer-Verlag, New York.Google Scholar
  27. Rack, P.M.H. and Westbury, D.R. (1969). The effects of length and stimulus rate on tension in isometric cat soleus muscle. J. Physiol., 204:443–460.PubMedGoogle Scholar
  28. Rack, P.M.H. and Westbury, D.R. (1974). The short range stiffness of active mammalian muscle and its effect on mechanical properties. J. Physiol., 240:331–350.PubMedGoogle Scholar
  29. Roux, W. (1895). Gasmmelte Abhandlungen uber Entwicklungs-mechanik der Organismen V. I & II. Engelmann, Leipzing.Google Scholar
  30. Seif-Naraghi, A.H. and Winters, J.M. (1989). Effect of task-specific linearization on musculoskeletal system control strategies. Biomech. Symp., ASME, AMD-98:347–350, San Diego.Google Scholar
  31. Sperry, R.W. (1959). The growth of nerve circuits. Sci. Amer., November, pp. 1–9.Google Scholar
  32. Winters, J.M. (1990). Hill-based muscle models: a systems engineering perspective. In Multiple Muscle System. Winters, J.M. and Woo, S.Y. (eds.), Chapter 5, pp. 69–93, Springer-Verlag, New York.Google Scholar
  33. Winters, J.M. (1995a). How detailed should muscle models be to understand multi-joint movement coordination? Hum. Mov. Sci., 14:401–442.CrossRefGoogle Scholar
  34. Winters, J.M. (1995b). An improved muscle-reflex actuator for use in large-scale neuromusculoskeletal models. Ann. Biomed. Eng., 23:359–374.PubMedCrossRefGoogle Scholar
  35. Winters, J.M. (1995c). Concepts in neuro-muscular modelling, In 3-D Analysis of Human Movement. Allard et al. (eds.), Chapter 12, pp. 257–292, Human Kinetics.Google Scholar
  36. Winters, J.M. and Stark, L. (1985). Analysis of fundamental movement patterns through the use of in-depth antagonistic muscle models. IEEE Trans. Biomed. Eng., BME-32:826–839.CrossRefGoogle Scholar
  37. Winters, J.M. and Stark, L. (1987). Muscle models: what is gained and what is lost by varying model complexity. Biol. Cybern., 55:403–420.PubMedCrossRefGoogle Scholar
  38. Winters, J.M. and Van der Helm, F.C.T. (1994). A field-based musculoskeletal framework for studying human posture and manipulation in 3-D, pp. 410–415, Proc. Symp. on Modeling Control of Biomed. Sys., IFAC, Galveston.Google Scholar
  39. Winters, J.M., Stark, L., and Seif-Naraghi, A.H. (1988). An analysis of the sources of muscle-joint system impedance. J. Biomech., 12:1011–1025.CrossRefGoogle Scholar
  40. Wolff, J. (1884). Das Gesetz der transformation der inneren architektur der knochen bei pathologischen veranderungen der ausseren knochenform. Sitz, Ber. Preuss. Akad. Wiss. 22. Sitzg., phys-math. Kl.Google Scholar
  41. Zahalak, G.I. (1982). The dynamics of active human skeletal muscle in vivo. In Mechanics of Skeletal and Cardiac Muscle. Phillips, C.A. and Petrofsky, J.S. (eds.), Springfield, Charles C Thomas.Google Scholar
  42. Zahalak, G.I. (1990). Modeling muscle mechanics (and energetics). In Multiple Muscle Systems Winters, J.M. and Woo, S.Y. (eds.), Chapter 1, pp. 1–23, Springer-Verlag, New York.Google Scholar
  43. Zajac, F. (1989). Muscle and tendon: properties, models, scaling and application to biomechancis and motor control. CRC Crit. Rev. Biomed. Eng., 17:359–415.Google Scholar

References

  1. Morgan, D.L. (1994). An explanation for residual increased tension in striated muscle after stretch during contraction, 1994. Exp. Physiol., 79:831–838.PubMedGoogle Scholar

References

  1. Bloom, W. and Fawcett, D.W. (1968). T**extbook of histology. Saunders, Philadelphia.Google Scholar
  2. Delp, S.L., Arnold, A.S., and Piazza, S.J. (1997). Clinical applications of musculoskeletal models in orthopaedics and rehabilitation. This volume.Google Scholar
  3. Heron, M.I. and Richmond, F.J.R. (1993). In series fiber architecture in long human muscles. J. Morph., 216:35–45.PubMedCrossRefGoogle Scholar
  4. Huijing, P.A. (1999). Muscle as a collagen fiber reinforced composite material: Force transmission in muscle and whole limbs. J. Biomech., 32:329–345.PubMedCrossRefGoogle Scholar
  5. Huijing, P.A. and Winters, J.M. (1998). Toward a new paradigm of locomotor apparatus and neuromuscular control. In Models in human movement sciences. Bosch, P., Boschker, M.S.J., van Lenthe, H., Post, A.A., Pijpers, J.R., Roeleveld, K., Steenbergen, J., and Tanck, E. (eds.). Free University Press, Amsterdam, pp. 45–50.Google Scholar
  6. Huijing, P.A., Baan, G.C., and Rebel, G. (1998). Nonmyotendinous force transmission in the extensor digitorum longus muscle of the rat. J. Exp. Biol., 201:683–691.Google Scholar
  7. Purslow, P. and Duance, V.C. (1990). Structure and function of intramuscular connective tissue. In Connective tissue matrix, Hukins, D.L. (ed.), Part 2. pp. 127–166, CRC Press, Boca Raton.Google Scholar
  8. Riewald, S.A. and Delp, S.L. (1997). The action of the rectus femoris muscle following distal tendon transfer: does it generate a knee flexion moment? Dev. Med. Child Neurol., 39:99–105.PubMedCrossRefGoogle Scholar
  9. Rowe, R.D.W. (1981). Morphology of perimysial and endomysial connective tissue in skeletal muscle. Tissue Cell, 13:681–690.PubMedCrossRefGoogle Scholar
  10. Strassmann, T., van der Wal, J.C., Halata, Z., and Drukker, J. (1990). Functional topography and ultra-structucture of periarticular mechanoreceptors in the lateral elbow region of the rat. Acta Anat., 138:1–14.CrossRefGoogle Scholar
  11. Street, S.F. (1983). Lateral transmission of tension in frog myofibers: a myofibrilar network and transverse cytoskeletal connections are possible transmitters. J. Cell. Physiol., 114:346–364.PubMedCrossRefGoogle Scholar
  12. Tidball, J.G. (1983). The geometry of actin filament-membrane associations can modify adhesive strength of the myotendinous jumction. Cell. Motil., 3:439–447.PubMedCrossRefGoogle Scholar
  13. Trotter, J.A. (1993). Functional morphology of force transmission in skeletal muscle. Acta Anat., 146:205–222.PubMedCrossRefGoogle Scholar
  14. Trotter, J.A. and Purslow, P.P. (1992). Functional morphology of the endomysium in series fibred muscles. J. Morph., 212:109–122.PubMedCrossRefGoogle Scholar
  15. Trotter, J.A., Richmond, F.J.R., and Purslow, P.P. (1995). Functional morphology and motor control of series-fibered muscles. Exerc. Sport Sci. Rev., 23:167–213.PubMedCrossRefGoogle Scholar
  16. van der Wal, J.C. (1988). The organization of the substrate of proprioception in the elbow region of the rat. Doctoral Dissertation, University of Limburg, Maastricht, The Netherlands.Google Scholar

Copyright information

© Springer-Verlag New York, Inc. 2000

Authors and Affiliations

  • Jack M. Winters
  • Robert E. Kearney
  • Michael P. Slawnych
  • Peter A. Huijing

There are no affiliations available

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