Experimental Brain Research

, Volume 186, Issue 1, pp 123–130 | Cite as

Vertical perturbations of human gait: organisation and adaptation of leg muscle responses

  • V. Bachmann
  • R. Müller
  • H. J. A. van Hedel
  • V. DietzEmail author
Research Article


During the last several years, evidence has arisen that the neuronal control of human locomotion depends on feedback from load receptors. The aim of the present study was to determine the effects and the course of sudden and unexpected changes in body load (vertical perturbations) on leg muscle activity patterns during walking on a treadmill. Twenty-two healthy subjects walking with 25% body weight support (BWS) were repetitively and randomly loaded to 5% or unloaded to 45% BWS during left mid-stance. At the new level of BWS, the subjects performed 3–11 steps before returning to 25% BWS (base level). EMG activity of upper and lower leg muscles was recorded from both sides. The bilateral leg muscle activity pattern changed following perturbations in the lower leg muscles and the net effect of the vertical perturbations showed onset latencies with a range of 90–105 ms. Body loading enhanced while unloading diminished the magnitude of ipsilateral extensor EMG amplitude, compared to walking at base level. Contralateral leg flexor burst activity was shortened following loading and prolonged following unloading perturbation while flexor EMG amplitude was unchanged. A general decrease in EMG amplitudes occurred during the course of the experiment. This is assumed to be due to adaptation. Only the muscles directly activated by the perturbations did not significantly change EMG amplitude. This is assumed to be due to the required compensation of the perturbations by polysynaptic spinal reflexes released following the perturbations. The findings underline the importance of load receptor input for the control of locomotion.


Locomotion Body weight support (BWS) Loading perturbation (LP) Unloading perturbation (UP) Loading response 



We want to thank all the volunteers who participated in this study, Mathias Wellner for assistance with programming and Rachel Jurd for her help with editing the English. The study was supported by the International Institute for Research in Paraplegia (IFP) and by the Betty and David Koetser Foundation for Brain Research.


  1. Bastiaanse CM, Duysens J, Dietz V (2000) Modulation of cutaneous reflexes by load receptor input during human walking. Exp Brain Res 135:189–198PubMedCrossRefGoogle Scholar
  2. Berger W, Dietz V, Quintern J (1984) Corrective reactions to stumbling in man: neuronal co-ordination of bilateral leg muscle activity during gait. J Physiol 357:109–125PubMedGoogle Scholar
  3. Berger W, Dietz V, Quintern J (1987) Interlimb coordination of posture in man (Abstract). J Physiol 390:135Google Scholar
  4. Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, OxfordGoogle Scholar
  5. Dietz V (2002a) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462–467PubMedCrossRefGoogle Scholar
  6. Dietz V (2002b) Proprioception and locomotor disorders. Nat Rev Neurosci 3:781–790PubMedCrossRefGoogle Scholar
  7. Dietz V, Duysens J (2000) Significance of load receptor input during locomotion: a review. Gait Posture 11:102–110PubMedCrossRefGoogle Scholar
  8. Dietz V, Harkema SJ (2004) Locomotor activity in spinal cord-injured persons. J Appl Physiol 96:1954–1960PubMedCrossRefGoogle Scholar
  9. Dietz V, Horstmann GA, Berger W (1989a) Interlimb coordination of leg-muscle activation during perturbation of stance in humans. J Neurophysiol 62:680–693PubMedGoogle Scholar
  10. Dietz V, Horstmann GA, Berger W (1989b) Significance of proprioceptive mechanisms in the regulation of stance. Prog Brain Res 80:419–423PubMedGoogle Scholar
  11. Dietz V, Gollhofer A, Kleiber M, Trippel M (1992) Regulation of bipedal stance: dependency on “load” receptors. Exp Brain Res 89:229–231PubMedCrossRefGoogle Scholar
  12. Donelan JM, Pearson KG (2004) Contribution of sensory feedback to ongoing ankle extensor activity during the stance phase of walking. Can J Physiol Pharmacol 82:589–598PubMedCrossRefGoogle Scholar
  13. Duysens J, Pearson KG (1980) Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187:321–332PubMedCrossRefGoogle Scholar
  14. Duysens J, Tax AAM (1994) Interlimb reflexes during gait in cats and human. In: Swinnen SP, Heuer H, Massion J, Casaer P (eds) Interlimb coordination: neural, dynamical, and cognitive constraints. Academic, San Diego, pp 97–126Google Scholar
  15. Faist M, Hoefer C, Hodapp M, Dietz V, Berger W, Duysens J (2006) In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading. Brain Res 1076:87–92PubMedCrossRefGoogle Scholar
  16. Ferris D, Gordon K, Beres-Jones J, Harkema S (2003) Muscle activation during unilateral stepping occurs in the nonstepping limb of humans with clinical complete spinal cord injury. Spinal Cord 42:14–23CrossRefGoogle Scholar
  17. Finch L, Barbeau H, Arsenault B (1991) Influence of body weight support on normal human gait: development of a gait retraining strategy. Phys Ther 71:842–856PubMedGoogle Scholar
  18. Fouad K, Pearson KG (1997) Effects of extensor muscle afferents on the timing of locomotor activity during walking in adult rats. Brain Res 749:320–328PubMedCrossRefGoogle Scholar
  19. Fouad K, Bastiaanse CM, Dietz V (2001) Reflex adaptations during treadmill walking with increased body load. Exp Brain Res 137:133–140PubMedCrossRefGoogle Scholar
  20. Frey M, Colombo G, Vaglio M, Bucher R, Jorg M, Riener R (2006) A novel mechatronic body weight support system. IEEE Trans Neural Syst Rehabil Eng 14:311–321PubMedCrossRefGoogle Scholar
  21. Ghori GM, Luckwill RG (1985) Responses of the lower limb to load carrying in walking man. Eur J Appl Physiol Occup Physiol 54:145–150PubMedCrossRefGoogle Scholar
  22. Gollhofer A, Schmidtbleicher D, Quintern J, Dietz V (1986) Compensatory movements following gait perturbations: changes in cinematic and muscular activation patterns. Int J Sports Med 7:325–329PubMedCrossRefGoogle Scholar
  23. Grey MJ, van Doornik J, Sinkjaer T (2002) Plantar flexor stretch reflex responses to whole body loading/unloading during human walking. Eur J Neurosci 16:2001–2007PubMedCrossRefGoogle Scholar
  24. Grey MJ, Mazzaro N, Nielsen JB, Sinkjaer T (2004) Ankle extensor proprioceptors contribute to the enhancement of the soleus EMG during the stance phase of human walking. Can J Physiol Pharmacol 82:610–616PubMedCrossRefGoogle Scholar
  25. Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR (1997) Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol 77:797–811PubMedGoogle Scholar
  26. Hesse S, Werner C, Bardeleben A, Barbeau H (2001) Body weight-supported treadmill training after stroke. Curr Atheroscler Rep 3:287–294PubMedCrossRefGoogle Scholar
  27. Hiebert GW, Whelan PJ, Prochazka A, Pearson KG (1996) Contribution of hind limb flexor muscle afferents to the timing of phase transitions in the cat step cycle. J Neurophysiol 75:1126–1137PubMedGoogle Scholar
  28. Horstmann GA, Dietz V (1988) The contribution of vestibular input to the stabilization of human posture: a new experimental approach. Neurosci Lett 95:179–184PubMedCrossRefGoogle Scholar
  29. Horstmann GA, Dietz V (1990) A basic posture control mechanism: the stabilization of the centre of gravity. Electroencephalogr Clin Neurophysiol 76:165–176PubMedCrossRefGoogle Scholar
  30. Ivanenko YP, Grasso R, Macellari V, Lacquaniti F (2002) Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. J Neurophysiol 87:3070–3089PubMedGoogle Scholar
  31. Lam T, Wolstenholme C, van der Linden M, Pang MY, Yang JF (2003) Stumbling corrective responses during treadmill-elicited stepping in human infants. J Physiol 553:319–331PubMedCrossRefGoogle Scholar
  32. Mazzaro N, Grey MJ, do Nascimento OF, Sinkjaer T (2006) Afferent-mediated modulation of the soleus muscle activity during the stance phase of human walking. Exp Brain Res 173:713–723PubMedCrossRefGoogle Scholar
  33. McCrea DA (2001) Spinal circuitry of sensorimotor control of locomotion. J Physiol 533:41–50PubMedCrossRefGoogle Scholar
  34. Muller R, Dietz V (2006) Neuronal function in chronic spinal cord injury: divergence between locomotor and flexion- and H-reflex activity. Clin Neurophysiol 117:1499–1507PubMedCrossRefGoogle Scholar
  35. Nakazawa K, Kawashima N, Akai M, Yano H (2004) On the reflex coactivation of ankle flexor and extensor muscles induced by a sudden drop of support surface during walking in humans. J Appl Physiol 96:604–611PubMedCrossRefGoogle Scholar
  36. Nashner LM (1980) Balance adjustments of humans perturbed while walking. J Neurophysiol 44:650–664PubMedGoogle Scholar
  37. Pang MY, Yang JF (2001) Interlimb co-ordination in human infant stepping. J Physiol 533:617–625PubMedCrossRefGoogle Scholar
  38. Prochazka A, Gillard D, Bernett D (1997) Indications of positive feedback in the control of movement. J Neurophysiol 77:37–51Google Scholar
  39. Reisman DS, Block HJ, Bastian AJ (2005) Interlimb coordination during locomotion: what can be adapted and stored? J Neurophysiol 94:2403–2415PubMedCrossRefGoogle Scholar
  40. Schillings AM, Van Wezel BM, Duysens J (1996) Mechanically induced stumbling during human treadmill walking. J Neurosci Methods 67:11–17PubMedCrossRefGoogle Scholar
  41. Sinkjaer T (2000) Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol 523:817–827PubMedCrossRefGoogle Scholar
  42. Stephens MJ, Yang JF (1999) Loading during the stance phase of walking in humans increases the extensor EMG amplitude but does not change the duration of the step cycle. Exp Brain Res 124:363–370PubMedCrossRefGoogle Scholar
  43. Tang PF, Woollacott MH, Chong RK (1998) Control of reactive balance adjustments in perturbed human walking: roles of proximal and distal postural muscle activity. Exp Brain Res 119:141–152PubMedCrossRefGoogle Scholar
  44. Ting LH, Kautz SA, Brown DA, Zajac FE (2000) Contralateral movement and extensor force generation alter flexion phase muscle coordination in pedaling. J Neurophysiol 83:3351–3365PubMedGoogle Scholar
  45. Vaughan CL, Davis BL, O’Connor JC (1992) Dynamics of human gait. Human Kinetics, ChampaignGoogle Scholar
  46. Whelan PJ (1996) Control of locomotion in the decerebrate cat. Prog Neurobiol 49:481–515PubMedCrossRefGoogle Scholar
  47. Yang JF, Stephens MJ, Vishram R (1998) Transient disturbances to one limb produce coordinated, bilateral responses during infant stepping. J Neurophysiol 79:2329–2337PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • V. Bachmann
    • 1
    • 2
  • R. Müller
    • 1
    • 2
  • H. J. A. van Hedel
    • 1
  • V. Dietz
    • 1
    Email author
  1. 1.Spinal Cord Injury CenterUniversity Hospital BalgristZurichSwitzerland
  2. 2.Institute of Human Movement Sciences and SportZurichSwitzerland

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