Advertisement

The Implications of Force Feedback for the λ Model

  • Richard Nichols
  • Kyla T. Ross
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 629)

Abstract

It is argued here that length and force feedback play important but distinct roles in motor coordination. Length feedback compensates for several nonlinear properties of muscle and therefore simplifies its behavior, but in addition promotes the nonlinear relationship between force and stiffness that is essential to the mechanism for modulating joint stiffness. Excitatory force feedback is also primarily autogenic. Under conditions of level treadmill stepping in cat walking, positive force feedback is restricted in the distal hindlimb to a few and perhaps only one ankle extensor, the gastrocnemius muscle group. Based on the anatomy of this group, positive force feedback provides a stiff linkage that reinforces proportional coordination between ankle and knee joints. In terms of the λ model, excitatory force feedback can reinforce muscular force generation and stiffness, but should have no significant effect on activation threshold. Inhibitory force feedback projects mainly to muscles that span different joints and axes of rotation than the parent muscle. This heterogenic force feedback is thought to promote interjoint coordination and thought to influence stiffness of the joints and limbs. During locomotion, the inhibitory influences appear to be focused on the distal musculature. Since the inhibitory force feedback is heterogenic, it also influences the threshold for activation of relevant musculature. Threshold is therefore not entirely a control variable and independent of feedback. It is proposed that the actuators for movement consist of systems of muscles or motor units that are linked by feedback and that receive control signals from elsewhere in the nervous system.

Keywords

Motor Unit Gastrocnemius Muscle Force Feedback Golgi Tendon Organ Interjoint Coordination 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Suggestions for General Reading

  1. Biewener, A.A., & Daley, M.A. (2007). Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control. J. Exp. Biol., 210, 2949–2960.PubMedCrossRefGoogle Scholar
  2. Duysens, J., Clarac, F., & Cruse, H. (2000). Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev, 80(1), 83–133.PubMedGoogle Scholar
  3. Feldman, A. G., & Levin, M. F. (1995). The origin and use of positional frames of reference in motor control. Behavioral and Brain Sciences, 18, 723–806.CrossRefGoogle Scholar
  4. Giszter, S. F., Mussa-Ivaldi, F. A., & Bizzi, E. (1993). Convergent force fields organized in the frog's spinal cord. J Neurosci, 13(2), 467–491.PubMedGoogle Scholar
  5. Jami, L. (1992). Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiol. Rev., 72, 623–666.PubMedGoogle Scholar
  6. Nichols, T. R. (1994). A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. Acta Anat (Basel), 151(1), 1–13.CrossRefGoogle Scholar
  7. Pearson, K. G. (1995). Proprioceptive regulation of locomotion. Current Opinion in Neurobiology, 5, 786–791.PubMedCrossRefGoogle Scholar
  8. Prochazka, A. (1996). Proprioceptive feedback and movement regulation. In L. B. Rowell & J. T. Shepherd (Eds.), Handbook of Physiology. Section 12: Excercise: Regulation and Integration of Multiple Systems.New York: Oxford.Google Scholar
  9. Ting, L. H., & Macpherson, J. M. (2005). A limited set of muscle synergies for force control during a postural task. J Neurophysiol, 93(1), 609–613.PubMedCrossRefGoogle Scholar
  10. Tresch, M. C., Saltiel, P., d'Avella, A., & Bizzi, E. (2002). Coordination and localization in spinal motor systems. Brain Res Brain Res Rev, 40(1–3), 66–79.PubMedCrossRefGoogle Scholar
  11. BibliographyGoogle Scholar
  12. Angel, M. J., Guertin, P., Jimenez, T., & McCrea, D. A. (1996). Group I extensor afferents evoke disynaptic EPSPs in cat hindlimb extensor motorneurones during fictive locomotion. J Physiol (Lond), 494(Pt 3), 851–861.Google Scholar
  13. Asatryan, D. G., & Feldman, A. G. (1965). Functional tuning of nervous system with control of movement or maintenance of a steady posture-1 mechanographic analysis of the work of the joint on execution of a postural task. Biophysics., 10, 837–846.Google Scholar
  14. Bonasera, S. J., & Nichols, T. R. (1994). Mechanical actions of heterogenic reflexes linking long toe flexors with ankle and knee extensors of the cat hindlimb. J Neurophysiol, 71(3), 1096–1110.PubMedGoogle Scholar
  15. Campbell, K. S., & Moss, R. L. (2002). History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J, 82(2), 929–943.PubMedCrossRefGoogle Scholar
  16. Carter, R. R., Crago, P. E., & Keith, M. W. (1990). Stiffness regulation by reflex action in the normal human hand. J Neurophysiol, 64(1), 105–118.PubMedGoogle Scholar
  17. Conway, B. A., Hultborn, H., & Kiehn, O. (1987). Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res, 68(3), 643–656.PubMedCrossRefGoogle Scholar
  18. Cope, T. C., & Pinter, M. J. (1995). The Size Principle: still working after all these years. N.I.P.S., 10, 280–286.Google Scholar
  19. Crago, P. E., Houk, J. C., & Rymer, W. Z. (1982). Sampling of total muscle force by tendon organs. J Neurophysiol, 47(6), 1069–1083.PubMedGoogle Scholar
  20. Daley, M. A., Felix, G., & Biewener, A. A. (2007). Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control. J Exp Biol, 210(Pt 3), 383–394.PubMedCrossRefGoogle Scholar
  21. Donelan, J. M., & Pearson, K. G. (2004). Contribution of force feedback to ankle extensor activity in decerebrate walking cats. J Neurophysiol, 92(4), 2093–2104.PubMedCrossRefGoogle Scholar
  22. Duysens, J., Clarac, F., & Cruse, H. (2000). Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev, 80(1), 83–133.PubMedGoogle Scholar
  23. Duysens, J., & Pearson, K. G. (1980). Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res., 187, 321–332.PubMedCrossRefGoogle Scholar
  24. Eccles, J. C., Eccles, R. M., & Lundberg, A. (1957). The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurons. J Physiol, 137, 22–50.PubMedGoogle Scholar
  25. Eccles, J. C., Eccles, R. M., & Lundberg, A. (1957). Synaptic actions on motoneurons caused by impulses in the Golgi tendon organ afferents. J Physiol, 138, 227–252.PubMedGoogle Scholar
  26. Feldman, A. G. (1966). Functional tuning of the nervous system during control of movement or maintenance of a steady posture III mechanographic analysis of the execution by man of the simplest motor tasks. Biophysics, 11, 766–775.Google Scholar
  27. Feldman, A. G. (1980). Superposition of motor programs I rhythmic forearm movements in man. Neuroscience, 5, 81–90.PubMedCrossRefGoogle Scholar
  28. Feldman, A. G. (1980). Superposition of motor programs II rapid forearm flexion in man. Neuroscience, 5, 91–95.PubMedCrossRefGoogle Scholar
  29. Feldman, A. G. (1986). Once more on the equilibrium point hypothesis model for motor control. J. Motor Behavior, 18, 17–54.Google Scholar
  30. Feldman, A. G., & Levin, M. F. (1995). The origin and use of positional frames of reference in motor control. Behav Brain Sci, 18, 723–806.CrossRefGoogle Scholar
  31. Feldman, A. G., & Orlovsky, G. N. (1972). The influence of different descending systems on the tonic stretch reflex in the cat. Exp. Neurol., 37, 481–494.PubMedCrossRefGoogle Scholar
  32. Giszter, S. F., Mussa-Ivaldi, F. A., & Bizzi, E. (1993). Convergent force fields organized in the frog's spinal cord. J Neurosci, 13(2), 467–491.PubMedGoogle Scholar
  33. Goslow, G. E., Reinking, R. M., & Stuart, D. G. (1973). The cat stop cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morph, 141, 1–42.Google Scholar
  34. Gossard, J. P., Brownstone, R. M., Barajon, I., & Hultborn, H. (1994). Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp Brain Res, 98(2), 213–228.PubMedCrossRefGoogle Scholar
  35. Granit, R. (1950). Reflex self-regulation of muscle contraction and autogenetic inhibition. J Neurophysiol, 13, 351–372.PubMedGoogle Scholar
  36. Gregor, R. J., Smith, D. W., & Prilutsky, B. I. (2006). Mechanics of slope walking in the cat: quantification of muscle load, length change, and ankle extensor EMG patterns. J Neurophysiol, 95(3), 1397–1409.PubMedCrossRefGoogle Scholar
  37. Gregor, R. J., Smith, J. L., Smith, D. W., Oliver, A., & Prilutsky, B. I. (2001). Hindlimb kinetics and neural control during slope walking in the cat: unexpected findings. J Appl Biomech, 17, 277–286.Google Scholar
  38. Griffiths, R. I. (1991). Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. J Physiol, 436, 219–236.PubMedGoogle Scholar
  39. Guertin, P., Angel, M. J., Perreault, M. C., & McCrea, D. A. (1995). Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J Physiol, 487 (Pt 1), 197–209.PubMedGoogle Scholar
  40. Haftel, V. K., Bichler, E. K., Nicholas, T. R., Pinter, M. J., & Cope, T. C. (2004). Movement reduces the dynamic response of muscle spindle afferents and motoneuron synaptic potentials in raf. J Neurophysiol, 91, 2164–2171.Google Scholar
  41. Hoffer, J. A., & Andreassen, S. (1981). Regulation of soleus muscle stiffness in premammillary cat intrinsic and reflex components. J Neurophysiol, 45, 267–285.PubMedGoogle Scholar
  42. Hoffer, J. A., Caputi, A. A., & Pose, I. E. (1992). Activity of muscle proprioceptors in cat posture and locomotion: relation to EMG, tendon force, and the movement of fibers and aponeurotic segments. In L. Jami & E. Pierrot-Deseilligny & D. Zytnicki (Eds.), Muscle Afferents and Spinal Control of Movement.Oxford: Pergamon.Google Scholar
  43. Houk, J., & Henneman, E. (1967). Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol, 30, 466–481.PubMedGoogle Scholar
  44. Houk, J. C. (1972). The phylogeny of muscular control configrations, Biocybernetics IV (Vol. 2, pp. 125–144). Jena: Fischer.Google Scholar
  45. Houk, J. C., Crago, P. E., & Rymer, W. Z. (1981). Function of the spindle dynamic response in stiffness regulation – a predictive mechanism provided by non-linear feedback. In A. Taylor & A. Prochazka (Eds.), Muscle Receptors and Movement (pp. 299–309). London: Macmillan.Google Scholar
  46. Houk, J. C., Fagg, A. H., & Barto, A. G. (2002). Fractional Power Damping Model of Joint Motion. In M. L. Latash (Ed.), Structure-Function Relations in Voluntary Movements (Vol. 2, pp. 147–178). Champaign: Human Kinetics.Google Scholar
  47. Houk, J. C., Rymer, W. Z., & Crago, P. E. (1981). Dependence of dynamic response of spindle receptors on muscle length and velocity. J Neurophysiol, 46, 143–165.PubMedGoogle Scholar
  48. Houk, J. C., Singer, J. J., & Goldman, M. R. (1970). An evaluation of length and force feedback to soleus muscles of decerebrate cats. J Neurophysiol, 33, 784–811.PubMedGoogle Scholar
  49. Huyghues-Despointes, C. M., Cope, T. C., & Nichols, T. R. (2003). Intrinsic properties and reflex compensation in reinnervated triceps surae muscles of the cat: effect of movement history. J Neurophysiol, 90(3), 1547–1555.PubMedCrossRefGoogle Scholar
  50. Jami, L. (1992). Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiol. Rev., 72, 623–666.PubMedGoogle Scholar
  51. Joyce, G. C., Rack, P. M. H., & Westbury, D. R. (1969). The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J. Physiol., 204, 461–474.PubMedGoogle Scholar
  52. Kirsch, R. F., & Rymer, W. Z. (1987). Neural compensation for muscular fatigue: evidence for significant force regulation in man. J Neurophysiol, 57(6), 1893–1910.PubMedGoogle Scholar
  53. Matthews, P. B. C. (1959). The dependence of tension upon extension in the stretch reflex of the soleus muscle of the decerebrate cat. J Physiol, 147, 521–546.PubMedGoogle Scholar
  54. Matthews, P. B. C. (1972). Mammalian Muscle Receptors and Their Central Actions. Baltimore: Williams and Wilkins.Google Scholar
  55. McCrea, D. A., Shefchyk, S. J., Stephens, M. J., & Pearson, K. G. (1995). Disynaptic group I excitation of synergist ankle extensor motoneurones during fictive locomotion in the cat. J Physiol (Lond), 487(Pt 2), 527–539.Google Scholar
  56. McMahon, T. A. (1984). Muscles, Reflexes and Locomotion.Princeton: Princeton University Press.Google Scholar
  57. Merton, P. A. (1953). Speculations on the servo-control of movement. In G. E. W. Wolstenholme (Ed.), The Spinal Cord. London: Churchill.Google Scholar
  58. Nichols, T. R. (1974). Soleus Muscle Stiffness and Its Reflex Control. Harvard, Cambridge.Google Scholar
  59. Nichols, T. R. (1987). The regulation of muscle stiffness: implications for the control of limb stiffness. In P. Marconnet, Komi, P.V. (Ed.), Muscular Function in Exercise and Training (Vol. 26, pp. 36–47). Basel: Karger.Google Scholar
  60. Nichols, T. R. (1994). A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. Acta Anat (Basel), 151(1), 1–13.CrossRefGoogle Scholar
  61. Nichols, T. R. (1999). Receptor mechanisms underlying heterogenic reflexes among the triceps surae muscles of the cat. J Neurophysiol, 81(2), 467–478.PubMedGoogle Scholar
  62. Nichols, T. R., & Cope, T. C. (2004). Cross-bridge mechanisms underlying the history-dependent properties of muscle spindles and stretch reflexes. Can J Physiol. & Pharm, 8, 569–576.Google Scholar
  63. Nichols, T. R., Cope, T. C., & Abelew, T. A. (1999). Rapid spinal mechanisms of motor coordination. Exerc Sport Sci Rev, 27, 255–284.PubMedCrossRefGoogle Scholar
  64. Nichols, T. R., & Houk, J. C. (1976). The improvement in linearity and regulation of stiffness that results from action of the stretch reflex. J Neurophysiol, 39, 119–142.PubMedGoogle Scholar
  65. Pearson, K. G. (1995). Proprioceptive regulation of locomotion. Curr Opin Neurobiol, 5, 786–791.PubMedCrossRefGoogle Scholar
  66. Pearson, K. G., & Collins, D. F. (1993). Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius muscle during locomotor activity. J Neurophysiol, 70, 1009–1017.PubMedGoogle Scholar
  67. Popescu, F. C., & Rymer, W. Z. (2000). End points of planar reaching movements are disrupted by small force pulses: an evaluation of the hypothesis of equifinality. J Neurophysiol, 84(5), 2670–2679.PubMedGoogle Scholar
  68. Popescu, F. C., & Rymeri, W. Z. (2003). Implications of low mechanical impedance in upper limb reaching motion. Motor Control, 7(4), 323–327.PubMedGoogle Scholar
  69. Prochazka, A. (1996). Proprioceptive feedback and movement regulation. In L. B. Rowell & J. T. Shepherd (Eds.), Handbook of Physiology. Section 12: Excercise: Regulation and Integration of Multiple Systems.New York: Oxford.Google Scholar
  70. Prochazka, A., Gillard, D., & Bennett, D. J. (1997). Implications of positive feedback in the control of movement. J Neurophysiol, 77, 3237–3251.PubMedGoogle Scholar
  71. Ross, K. T. (2006) Quantitative Analysis of Feedback During Locomotion. Doctoral Dissertation, Department of Biomedical Engineering, Atlanta: Georgia Institute of Technology.Google Scholar
  72. Ross, K. T., Duysens, J., Smith, V. A., & Nichols, T. R. (2005). Modulation of cutaneous and proprioceptive feedback in the premammillary locomoting cat. Soc Neurosci Abstr, 31.Google Scholar
  73. Ross, K. T., Huyghues-Despointes, C. M., & Nichols, T. R. (2003). Heterogenic feedback among quadriceps and ankle extensors during spontaneous locomotion in premammillary cats. Soc Neurosci Abstr, 29.Google Scholar
  74. Ross, K. T., & Nichols, T. R. (2004). Inhibitory force feedback to and from the plantaris muscle in the locomoting premammillary cat. Soc Neurosci Abstr, 30.Google Scholar
  75. Sinkjaer, T. (1997). Muscle, reflex and central components in the control of the ankle joint in healthy and spastic man. Acta Neurol. scand., 96(Suppl.), 1–28.Google Scholar
  76. Sinkjaer, T., Andersen, J. B., & Larsen, B. (1996). Soleus stretch reflex modulation during gait in humans. J Neurophysiol, 76(2), 1112–1120.PubMedGoogle Scholar
  77. Sokoloff, A. J., Siegel, S. G., & Cope, T. C. (1999). Recruitment order among motoneurons from different motor nuclei. J Neurophysiol, 81(5), 2485–2492.PubMedGoogle Scholar
  78. Stein, R. B., Misiaszek, J. E., & Pearson, K. G. (2000). Functional role of muscle reflexes for force generation in the decerebrate walking cat. J Physiol, 525 Pt 3, 781–791.Google Scholar
  79. Ting, L. H., & Macpherson, J. M. (2005). A limited set of muscle synergies for force control during a postural task. J Neurophysiol, 93(1), 609–613.PubMedCrossRefGoogle Scholar
  80. Tresch, M. C., Saltiel, P., d'Avella, A., & Bizzi, E. (2002). Coordination and localization in spinal motor systems. Brain Res Brain Res Rev, 40(1–3), 66–79.PubMedCrossRefGoogle Scholar
  81. Wilmink, R. J., & Nichols, T. R. (2003). Distribution of heterogenic reflexes among the quadriceps and triceps surae muscles of the cat hind limb. J Neurophysiol, 90(4), 2310–2324.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringGeorgia Institute of TechnologyAtlanta

Personalised recommendations