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The Human Muscle Spindle and its Fusimotor Control

  • D. Burke
  • S. C. Gandevia

Summary

It is now 25 years since Hagbarth and Vallbo (1968) described the technique of microneurography, with the first direct recordings of the activity of muscle afferents in human subjects. It is appropriate to take stock of what has been learnt about fusimotor control of human muscle spindles since then in order to define the course of future experiments.

Muscle spindle discharge is used in microneurographic recordings to infer the action of the fusimotor system. This Chapter considers some of the fusimotor and non-fusimotor mechanisms which can influence the behaviour of human muscle spindle afferents. Voluntary contractions under isometric (or lengthening) conditions activate the fusimotor system such that overall spindle discharge increases. Evidence is presented that this can lead to considerable reflex “support” to motoneuronal output. This contribution may diminish during muscle fatigue and be absent during voluntary shortening contractions of sufficient speed.

Further studies will continue to focus on possible flexibility in the activation of fusimotor neurones produced by reflex and voluntary drives. Little data exist on possible abnormalities in fusimotor-induced spindle feedback or in reflexes acting on fusimotor neurones in patients with motor disorders.

Keywords

Muscle Spindle Supportive Excitation Spindle Ending Extrafusal Muscle Spindle Discharge 
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.

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References

  1. Al-Falahe, N.A., Nagoaka, M. and Vallbo, Å.B. (1990). Response profiles of human muscle afferents during active finger movements. Brain 113, 325–346CrossRefGoogle Scholar
  2. Al-Falahe, N.A. and Vallbo, Å.B. (1988). Role of the human fusimotor system in a motor adaptation task. Journal of Physiology 401, 77–95PubMedGoogle Scholar
  3. Aniss, A.M., Diener, H.-C., Hore, J., Burke, D. and Gandevia, S.C. (1990). Reflex influences on muscle spindles in human pretibial muscles during standing. Journal of Neurophysiology 64, 671–679PubMedGoogle Scholar
  4. Binder, M. D. and Stuart, D. G. (1980). Motor unit — muscle receptors interactions: Design features of the neuromuscular control system. In Spinal and Supraspinal Mechanisms of Voluntary Motor Control and Locomotion. Progress in Clinical Neurophysiology, Vol. 8, edited by J.E. Desmedt, pp. 72–98. Karger: BaselGoogle Scholar
  5. Brown, M.C., Goodwin, G.M. and Matthews, P.B.C. (1969). After-effects of fusimotor stimulation on the response of muscle spindle primary afferent endings. Journal of Physiology 205, 677–694PubMedGoogle Scholar
  6. Burke, D. (1981). The activity of human muscle spindle endings in normal motor behavior. International Review of Physiology 25, 91–126PubMedGoogle Scholar
  7. Burke, D. (1983). Critical examination of the case for or against fusimotor involvement in disorders of muscle tone. In: Motor Control Mechanisms in Health and Disease, Advances in Neurology, Vol. 39, edited by J.E. Desmedt, pp. 133–150. Raven Press: New YorkGoogle Scholar
  8. Burke, D., Aniss, A.M. and Gandevia, S.C. (1987). In-parallel and in-series behavior of human muscle spindle endings. Journal of Neurophysiology 58, 417–426PubMedGoogle Scholar
  9. Burke, D. and Gandevia, S.C. (1990). The peripheral motor system. In: The Human Nervous System, edited by G. Paxinos, pp. 125–145. Academic Press: New YorkGoogle Scholar
  10. Burke, D., Hagbarth, K.-E. and Löfstedt, L. (1978a). Muscle spindle responses in man to changes in load during accurate position maintenance. Journal of Physiology 276, 159–164PubMedGoogle Scholar
  11. Burke, D., Hagbarth, K.-E. and Löfstedt, L. (1978b). Muscle spindle activity in man during shortening and lengthening contractions. Journal of Physiology 277, 131–142PubMedGoogle Scholar
  12. Burke, D., Hagbarth, K.-E. and Skuse, N.F. (1978c). Recruitment order of human spindle endings in isometric voluntary contractions. Journal of Physiology 285, 101–112PubMedGoogle Scholar
  13. Burke, D., Hagbarth, K.-E. and Skuse, N.F. (1979). Voluntary activation of spindle endings in human muscles temporarily paralysed by nerve pressure. Journal of Physiology 287, 329–336PubMedGoogle Scholar
  14. Burke, D., McKeon, B. and Westerman, R.A. (1980). Induced changes in the thresholds for voluntary activation of human spindle endings. Journal of Physiology 302, 171–181PubMedGoogle Scholar
  15. Edin, B.B. and Vallbo, Å.B. (1988). Stretch sensitization of human muscle spindles. Journal of Physiology 400, 101–111PubMedGoogle Scholar
  16. Edin, B.B. and Vallbo, Å.B. (1990). Muscle afferent responses to isometric contraction and relaxation in humans. Journal of Neurophysiology 63, 1307–1313PubMedGoogle Scholar
  17. Gandevia, S.C. and Burke, D. (1985). Effect of training on voluntary activation of human fusimotor neurons. Journal of Neurophysiology 54, 1422–1429PubMedGoogle Scholar
  18. Gandevia, S.C., Burke, D. and McKeon, B. (1984). Coupling between human muscle spindle endings and motor units assessed using spike-triggered averaging. Neuroscience Letters 71, 181–186CrossRefGoogle Scholar
  19. Gandevia, S.C., Macefield, G., Burke, D. and McKenzie, D.K. (1990). Voluntary activation of human motor axons in the absence of muscle afferent feedback: the control of the deafferented hand. Brain 113, 1563–1581PubMedCrossRefGoogle Scholar
  20. Gandevia, S.C., Wilson, L., Cordo, P. and Burke, D. (1993). Fusimotor reflexes in relaxed forearm muscle evoked by afferents from the hand. Proceedings of the International Union of Physiological Sciences 322.27Google Scholar
  21. Gregory, J.E., Morgan, D.L. and Proske, U. (1987). Changes in size of the stretch reflex of cat and man attributed to after effects in muscle spindles. Journal of Neurophysiology 58, 628–640PubMedGoogle Scholar
  22. Gregory, J.E., Mark, R.F., Morgan, D.L., Patak, A., Polus, B. and Proske, U. (1990). Effects of muscle history on the stretch reflex in cat and man. Journal of Physiology 424, 93–107PubMedGoogle Scholar
  23. Hagbarth, K.-E., Kunesch, E.J., Nordin, M., Schmidt, R.F. and Wallin, E.U. (1986). Gamma loop contributing to maximal voluntary contractions in man. Journal of Physiology 380, 575–591PubMedGoogle Scholar
  24. Hagbarth, K.-E. and Vallbo, Å.B (1968). Discharge characteristics of human muscle afferents during muscle stretch and contraction. Experimental Neurology 22, 674–694PubMedCrossRefGoogle Scholar
  25. Hagbarth, K.-E. and Young, R.R. (1979). Participation of the stretch reflex in human physiological tremor. Brain 102, 509–526PubMedCrossRefGoogle Scholar
  26. Logigian, E.L., Wiegner, A.W. and Young, R.R. (1989). Alpha-gamma co-silence in human wrist flexor muscles during slow visually-guided passive wrist flexion. Neuroscience Research Communications 4,117–124Google Scholar
  27. Macefield, G., Gandevia, S.C. and Burke, D. (1990). Perceptual responses to microstimulation of single afferents innervating the joints, muscles and skin of the human hand. Journal of Physiology 429, 113–129PubMedGoogle Scholar
  28. Macefield, G., Hagbarth, K.-E., Gorman, R.B., Gandevia, S.C. and Burke, D. (1991). Decline in spindle support to α motoneurones during sustained voluntary contractions. Journal of Physiology 440, 497–512PubMedGoogle Scholar
  29. Macefield, V.G., Gandevia, S.C., Bigland-Ritchie, B., Gorman, R.B. and Burke, D. (1993). The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback. Journal of Physiology 471, 429–443PubMedGoogle Scholar
  30. Matthews, P.B.C (1972). Mammalian Muscle Receptors and their Central Actions. Edward Arnold: LondonGoogle Scholar
  31. Merton, P.A. (1953). Speculations on the servo control of movement. In The Spinal Cord. Ciba Foundation Symposium. Edited by G.E.W. Wolstenholme, J.A. Malcolm and J.A.B. Gray, pp. 247–260. Churchill: LondonGoogle Scholar
  32. Meyer-Lohmann, J., Riebold, W. and Robrecht, D. (1974). Mechanical influence of the extrafusal muscle on the static behaviour of deefferented primary muscle spindle endings in cat. Pflügers Archiv 352, 267–278PubMedCrossRefGoogle Scholar
  33. McKeon, B. and Burke, D. (1981). Component of muscle spindle discharge related to arterial pulse. Journal of Neurophysiology 46, 788–796PubMedGoogle Scholar
  34. McKeon, B. and Burke, D. (1983). Muscle spindle discharge in response to contraction of single motor units. Journal of Neurophysiology 49, 291–302PubMedGoogle Scholar
  35. McKeon, B., Gandevia, S. and Burke, D. (1984). Absence of somatotopic projection of muscle afferents onto motoneurons of same muscle. Journal of Neurophysiology 51, 185–194PubMedGoogle Scholar
  36. Morgan, D.L., Prochazka, A. and Proske, U. (1984). The after-effects of stretch and fusimotor stimulation on the responses of primary endings of cat muscle spindles. Journal of Physiology 356, 465–477PubMedGoogle Scholar
  37. Newsom Davis, J. (1975). The response to stretch of human intercostal muscle spindles studied in vitro. Journal of Physiology 249, 561–579Google Scholar
  38. Poppele, R.E. and Kennedy, W.R. (1974). Comparison between behaviour of human and cat muscle spindles recorded in vitro. Brain Research 75, 316–319PubMedCrossRefGoogle Scholar
  39. Prochazka, A., Stephens, J.A. and Wand, P. (1979). Muscle spindle discharge in normal and obstructed movements. Journal of Physiology 287, 57–66PubMedGoogle Scholar
  40. Ribot, E., Roll, J.-P. and Vedel, J.-P. (1986). Efferent discharges recorded from single skeletomotor and fusimotor fibres in man. Journal of Physiology 375, 251–268PubMedGoogle Scholar
  41. Ribot-Ciscar, E., Tardy-Gervet, M.F., Vedel, J.-P., and Roll, J.-P. (1991). Post-contraction changes in muscle spindle resting discharge and stretch sensitivity. Experimental Brain Research 86, 673–678CrossRefGoogle Scholar
  42. Roll, J.-P. and Vedel, J.-P. (1982). Kinesthetic role of muscle afferents in man studied by tendon vibration and microneurography. Experimental Brain Research 47, 177–190CrossRefGoogle Scholar
  43. Rothwell, J.C., Gandevia, S.C. and Burke, D. (1990). Activation of fusimotor neurones by motor cortical stimulation in human subjects. Journal of Physiology 430, 105–117Google Scholar
  44. Vallbo, Å.B. (1971). Muscle spindle response at the onset of isometric voluntary contractions in man. Time difference between fusimotor and skeletomotor effects. Journal of Physiology 218, 405–431Google Scholar
  45. Vallbo, Å.B. (1973). Muscle spindle afferent discharge from resting and contracting muscles in normal human subjects. In: New Developments in Electromyography and Clinical Neurophysiology. Volume 3. Edited by J.E. Desmedt, pp. 251–262. Karger: BaselGoogle Scholar
  46. Vallbo, Å.B. (1974). Human muscle spindle discharge during isometric voluntary contractions. Amplituderelations between spindle frequency and torque. Acta Physiologica Scandinavica 90, 319–336PubMedCrossRefGoogle Scholar
  47. Vallbo, Å.B. and Al-Falahe, N.A. (1990). Human muscle spindle response in a motor learning task. Journal of Physiology 421, 553–568PubMedGoogle Scholar
  48. Vallbo, Å.B., Hagbarth, K.-E., Torebjörk, H.E. and Wallin, B.G. (1979). Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiological Reviews 59, 919–957PubMedGoogle Scholar
  49. Windhorst, U., Hamm, T.M. and Stuart, D. (1989). On the function of muscle and reflex partitioning. Behavioral Brain Sciences 12, 629–681CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • D. Burke
    • 1
  • S. C. Gandevia
    • 1
  1. 1.Prince of Wales Medical Research Institute and University of New South WalesSydneyAustralia

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