Skip to main content
SpringerLink
Log in

Human standing and walking: comparison of the effects of stimulation of the vestibular system

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The adoption of bipedalism by hominids including man has complicated the tasks of balance control and the minimisation of body sway. We have investigated the role of the vestibular organs in controlling sway in the roll direction using galvanic vestibular stimulation (GVS). Two stance conditions were studied: during forward lean posterior compartment muscles are activated and during backward lean anterior compartment muscles are activated. GVS-evoked vestibular signals in stance control leg muscles as a group: all the active muscles in the leg on the GVS cathode side are excited together and those in the contralateral leg (anode side) relax. The subject sways towards the anode side. During treadmill walking, vestibular actions are subtly different: the actions are largely restricted to muscles acting at the ankle joint, occur at longer latencies, are not reciprocal in the opposite limb, are modulated throughout the step cycle (largest early in stance) and are reversed in sign in the peroneus longus muscle. The subject deviates towards the anode side. Hand contact with a firm object reduces GVS-evoked responses in leg muscles during treadmill walking. Responses to GVS are observed during over-ground walking but not significantly during bicycling on an ergometer. The observations suggest that these vestibular actions are part of a roll stabilisation mechanism. They may be mediated through different spinal premotor mechanisms during standing and walking and turned off during bicycling, when leg muscles have no balance control function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Ali AS, Rowen KA, Iles JF (2003) Vestibular actions on back and lower limb muscles during postural tasks in man. J Physiol 546:615–624

    Article  PubMed  CAS  Google Scholar 

  • Bauby CE, Kuo AD (2000) Active control of lateral balance in human walking. J Biomech 33:1433–1440

    Article  PubMed  CAS  Google Scholar 

  • Bent LR, Inglis JT, McFadyen BJ (2004) When is vestibular information important during walking? J Neurophysiol 92:1269–1275

    Article  PubMed  Google Scholar 

  • Brandt T, Strupp M, Benson J, Dieterich M (2001) Vestibulopathic gait. Walking and running. Adv Neurol 87:165–172

    PubMed  CAS  Google Scholar 

  • Britton T, Day B, Brown P, Rothwell J, Thompson P, Marsden C (1993) Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Exp Brain Res 94:143–151

    Article  PubMed  CAS  Google Scholar 

  • Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M (1999) Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol 81:129–139

    PubMed  CAS  Google Scholar 

  • Cappellini G, Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor patterns in human walking and running. J Neurophysiol 95:3426–3437

    Article  PubMed  CAS  Google Scholar 

  • Cathers I, Day BL, Fitzpatrick RC (2005) Otolith and canal reflexes in human standing. J Physiol 563:229–234

    Article  PubMed  CAS  Google Scholar 

  • Cohen HS (2000) Vestibular disorders and impaired path integration along a linear trajectory. J Vestib Res 10:7–15

    PubMed  CAS  Google Scholar 

  • Courtine G, Schieppati M (2003) Human walking along a curved path. II. Gait features and EMG patterns. Eur J Neurosci 18:191–205

    Article  PubMed  Google Scholar 

  • Courtine G, Papaxanthis C, Schieppati M (2006) Coordinated modulation of locomotor muscle synergies constructs straight-ahead and curvilinear walking in humans. Exp Brain Res 170:320–335

    Article  PubMed  Google Scholar 

  • Davies H, Edgley S (1994) Inputs to group II-activated midlumbar interneurones from descending motor pathways in the cat. J Physiol 479:463–473

    PubMed  Google Scholar 

  • Day BL, Cole J (2002) Vestibular-evoked postural responses in the absence of somatosensory information. Brain 125:2081–2088

    Article  PubMed  Google Scholar 

  • Day BL, Severac Cauquil A, Bartolomei L, Pastor MA, Lyon IN (1997) Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol 500:661–672

    PubMed  CAS  Google Scholar 

  • Day BL, Guerraz M, Cole J (2002) Sensory interactions for human balance control revealed by galvanic vestibular stimulation. Adv Exp Med Biol 508:129–137

    PubMed  Google Scholar 

  • Deshpande N, Patla AE (2005) Dynamic visual-vestibular integration during goal directed human locomotion. Exp Brain Res 166:237–247

    Article  PubMed  Google Scholar 

  • Dickstein R, Laufer Y (2004) Light touch and center of mass stability during treadmill locomotion. Gait Posture 20:41–47

    Article  PubMed  Google Scholar 

  • Dickstein R, Peterka RJ, Horak FB (2003) Effects of light fingertip touch on postural responses in subjects with diabetic neuropathy. J Neurol Neurosurg Psychiatr 74:620–626

    Article  PubMed  CAS  Google Scholar 

  • Dickstein R, Ufaz S, Dunsky A, Nadeau S, Abulaffio N (2005) Speed-dependent deviations from a straight-ahead path during forward locomotion in healthy individuals. Am J Phys Med Rehabil 84:330–337

    Article  PubMed  Google Scholar 

  • Donelan JM, Shipman DW, Kram R, Kuo AD (2004) Mechanical and metabolic requirements for active lateral stabilization in human walking. J Biomech 37:827–835

    Article  PubMed  Google Scholar 

  • Fitzpatrick RC, Wardman DL, Taylor JL (1999) Effects of galvanic vestibular stimulation during human walking. J Physiol 517:931–939

    Article  PubMed  CAS  Google Scholar 

  • Goldberg JM, Smith CE, Fernandez C (1984) Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol 51:1236–1256

    PubMed  CAS  Google Scholar 

  • Holden M, Ventura J, Lackner JR (1994) Stabilization of posture by precision contact of the index finger. J Vestib Res 4:285–301

    PubMed  CAS  Google Scholar 

  • Iles J, Tanner R (2006) Limb muscle responses to vestibular stimulation during treadmill walking in man. Proc Physiol Soc 1:C5

    Google Scholar 

  • Iles JF, Ali A, Pardoe J (2000) Task-related changes of transmission in the pathway of heteronymous spinal recurrent inhibition from soleus to quadriceps motor neurones in man. Brain 123:2264–2272

    Article  PubMed  Google Scholar 

  • Iles JF, Ali AS, Savic G (2004) Vestibular-evoked muscle responses in patients with spinal cord injury. Brain 127:1584–1592

    Article  PubMed  CAS  Google Scholar 

  • Iles JF, Baderin R, Simon A (2005) Short- and medium-latency responses to galvanic vestibular stimulation in human lower limb muscles during tonic and rhythmic motor behaviours. J Physiol 565P:C106

    Google Scholar 

  • Inman V (1947) Functional aspects of the abductor muscles of the hip. J Bone Joint Surg 29:607–619

    Google Scholar 

  • Jahn K, Strupp M, Schneider E, Dieterich M, Brandt T (2000) Differential effects of vestibular stimulation on walking and running. Neuroreport 11:1745–1748

    Article  PubMed  CAS  Google Scholar 

  • Lackner JR, DiZio P (2005) Vestibular, proprioceptive, and haptic contributions to spatial orientation. Annu Rev Psychol 56:115–147

    Article  PubMed  Google Scholar 

  • Langlet C, Leblond H, Rossignol S (2005) The mid-lumbar segments are needed for the expression of locomotion in chronic spinal cats. J Neurophysiol 93:2474–2488

    Article  PubMed  CAS  Google Scholar 

  • Lund S, Broberg C (1983) Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. Acta Physiol Scand 117:307–309

    Article  PubMed  CAS  Google Scholar 

  • Lyon IN, Day BL (2004) Predictive control of body mass trajectory in a two-step sequence. Exp Brain Res 161:193–200

    Article  PubMed  Google Scholar 

  • MacKinnon CD, Winter DA (1993) Control of whole body balance in the frontal plane during human walking. J Biomech 26:633–644

    Article  PubMed  CAS  Google Scholar 

  • Marsden JF, Castellote J, Day BL (2002) Bipedal distribution of human vestibular-evoked postural responses during asymmetrical standing. J Physiol 542:323–331

    Article  PubMed  CAS  Google Scholar 

  • Marsden JF, Blakey G, Day BL (2003) Modulation of human vestibular-evoked postural responses by alterations in load. J Physiol 548:949–953

    Article  PubMed  CAS  Google Scholar 

  • Matsuyama K, Drew T (2000) Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. I. Walking on a level surface. J Neurophysiol 84:2237–2256

    PubMed  CAS  Google Scholar 

  • Misiaszek JE, Stephens MJ, Yang JF, Pearson KG (2000) Early corrective reactions of the leg to perturbations at the torso during walking in humans. Exp Brain Res 131:511–523

    Article  PubMed  CAS  Google Scholar 

  • Moore SP, Rushmer DS, Windus SL, Nashner LM (1988) Human automatic postural responses: responses to horizontal perturbation of stance in multiple directions. Exp Brain Res 73:648–658

    Article  PubMed  CAS  Google Scholar 

  • Orlovsky GN (1972) The effect of different descending systems on flexor and extensor activity during locomotion. Brain Res 40:359–371

    Article  PubMed  CAS  Google Scholar 

  • Pierrynowski MR, Smith SB (1996) Rear foot inversion/eversion during gait relative to the subtalar joint neutral position. Foot Ankle Int 17:406–412

    PubMed  CAS  Google Scholar 

  • Rademaker GGJ (1980) The physiology of standing (translation of Das Stehen, 1931). University of Minnesota Press, Minneapolis

    Google Scholar 

  • Roberts T (1995) Understanding balance: the mechanics of posture and locomotion. Chapman & Hall, London

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics. McGraw Hill, New York

    Google Scholar 

  • Tang P-F, Woollacott M, Chong R (1998) Control of reactive balance adjustments in perturbed human walking: roles of proximal and distal postural muscle activity. Exp Brain Res 119:141–152

    Article  PubMed  CAS  Google Scholar 

  • Tokuno CD, Carpenter MG, Thorstensson A, Cresswell AG (2006) The influence of natural body sway on neuromuscular responses to an unpredictable surface translation. Exp Brain Res 174:19–28

    Article  PubMed  Google Scholar 

  • Ward CV (2002) Interpreting the posture and locomotion of Australopithecus afarensis: where do we stand? Am J Phys Anthropol Suppl 35:185–215

    Article  Google Scholar 

  • Winter DA (1991) The biomechanics and motor control of human gait: normal, elderly and pathological. Waterloo Biomechanics, Waterloo

    Google Scholar 

  • Winter DA (1995) Human balance and posture control during standing and walking. Gait Posture 3:193–214

    Article  Google Scholar 

  • Zollikofer CPE, Ponce de Leon MS, Lieberman DE, Guy F, Pilbeam D, Likius A, Mackaye HT, Vignaud P, Brunet M (2005) Virtual cranial reconstruction of Sahelanthropus tchadensis. Nature 434:755–759

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work has been supported by the International Spinal Research Trust.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK

    John F. Iles, Richard Baderin, Rachel Tanner & Ariel Simon

  2. St Hugh’s College, Oxford, OX2 6LE, UK

    John F. Iles

Authors
  1. John F. Iles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard Baderin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rachel Tanner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ariel Simon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John F. Iles.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iles, J.F., Baderin, R., Tanner, R. et al. Human standing and walking: comparison of the effects of stimulation of the vestibular system. Exp Brain Res 178, 151–166 (2007). https://doi.org/10.1007/s00221-006-0721-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0721-2

Keywords

Search

Navigation