Experimental Brain Research

, Volume 184, Issue 3, pp 391–410 | Cite as

Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects

  • John H. J. AllumEmail author
  • Lars B. Oude Nijhuis
  • Mark G. Carpenter
Research Article


One of the signatures of balance deficits observed in vestibular loss subjects is the greater instability in the roll compared to pitch planes. Directional differences in the timing and strengths of vestibular and proprioceptive sensory signals between roll and pitch may lead to a greater miscalculation of roll than pitch motion of the body in space when vestibular input is absent. For this reason, we compared the timing and amplitude of vestibular information, (observable in stimulus-induced head accelerations when subjects are tilted in different directions), with that of proprioceptive information caused by stimulus induced rotations of ankle and hip joints [observable as short latency (SL) stretch responses in leg and trunk muscle EMG activity]. We attempted to link the possible mode of sensory interaction with the deficits in balance control. Six subjects with bilaterally absent vestibular function and 12 age-matched controls were perturbed, while standing, in 8 directions of pitch and roll support surface rotation in random order. Body segment movements were recorded with a motion analysis system, head accelerations with accelerometers, and muscle activity with surface EMG. Information on stimulus pitch motion was available sequentially. Pitch movements of the support surface were best coded in amplitude by ankle rotation velocity, and by head vertical linear acceleration, which started at 13 ms after the onset of ankle rotation. EMG SL reflex responses in soleus with onsets at 46 ms provided a distal proprioceptive correlate to the pitch motion. Roll information on the stimulus was available simultaneously. Hip adduction and lumbo-sacral angular velocity were represented neurally as directionally specific short latency stretch and unloading reflexes in the bilateral gluteus medius muscles and paraspinal muscles with onsets at 28 ms. Roll angular accelerations of the head coded roll amplitude and direction at the same time (31 ms). Significant differences in amplitude coding between vestibular loss subjects and controls were only observed as a weaker coding between stimulus motion and head roll and head lateral linear accelerations. The absence of vestibular inputs in vestibular loss subjects led to characteristic larger trunk in motion in roll in the direction of tilt compared to pitch with respect to controls. This was preceded by less uphill flexion and no downhill extension of the legs in vestibular loss subjects. Downhill arm abduction responses were also greater. These results suggest that in man vestibular inputs provide critical information necessary for the appropriate modulation of roll balance-correcting responses in the form of stabilising knee and arm movements. The simultaneous arrival of roll sensory information in controls may indicate that proprioceptive and vestibular signals can only be interpreted correctly when both are present. Thus, roll proprioceptive information may be interpreted inaccurately in vestibular loss subjects, leading to an incorrect perception of body tilt and insufficient uphill knee flexion, especially as cervico-collic signals appear less reliable in these subjects as an alternative sensory input.


Human balance control Vestibular loss Proprioception Muscle activity Leg flexion responses Stretch reflex 



This work was supported by National Swiss Research Fund grant number 3100A0-104212 to JHJ Allum. Funding for MG Carpenter was provided by the Natural Sciences and Engineering Research Council of Canada.


  1. Anderson JH, Soechting JF, Terzuolo CA (1977) Dynamic relations between natural vestibular inputs and activity of forelimb extensor muscles in the decerebrate cat. I. Motor output during sinusoidal linear accelerations. Brain Res 120:1–15PubMedCrossRefGoogle Scholar
  2. Allum JHJ, Pfaltz CR (1985) Visual and vestibular contributions to pitch sway stabilization in the ankle muscles of normals and patients with bilateral peripheral vestibular deficits. Exp Brain Res 58:82–90PubMedCrossRefGoogle Scholar
  3. Allum JHJ, Honegger F, Schicks H (1993) Vestibular and proprioceptive modulation of postural synergies in normal subjects. J Vest Res 3:59–85Google Scholar
  4. Allum JHJ, Honegger F, Acuña H (1995) Differential control of leg and trunk muscle activity by vestibulo-spinal and proprioceptive signals during human balance corrections. Acta Otol Laryngol (Stockh) 115:124–129Google Scholar
  5. Allum JHJ, Honegger F (1998) Interactions between vestibular and proprioceptive signals in triggering and modulating human balance-correcting responses differ across muscles. Exp Brain Res 121:478–494PubMedCrossRefGoogle Scholar
  6. Allum JHJ, Ledin T (1999) Recovery of vestibulo-ocular function in subjects with acute peripheral vestibular loss. J Vest Res 9:135–144Google Scholar
  7. Allum JHJ, Carpenter MG, Bloem BR, Honegger F, Adkin AL (2002) Age-dependent variations in the directional sensitivity of balance corrections. J Physiol (Lond) 542:643–663CrossRefGoogle Scholar
  8. Allum JHJ, Carpenter MG, Honegger F (2003) Directional aspects of balance corrections in man. IEEE Eng Med Biol Mag 22:37–47PubMedCrossRefGoogle Scholar
  9. Bakker M, Allum JHJ, Visser JE, Grüneberg C, Van de Warrenburg BPC, Kremer BH, Bloem BR (2006) Postural responses to multidirectional stance perturbations in cerebellar ataxia. Exp Neurol 202:21–35Google Scholar
  10. Bloem BR, Allum JHJ, Carpenter MG, Honegger F (2000) Is lower leg proprioception essential for triggering human balance corrections? Exp Brain Res 130:375–391PubMedCrossRefGoogle Scholar
  11. Bloem BR, Allum JHJ, Carpenter MG (2002) Triggering of balance corrections and compensatory strategies in a patient with total leg proprioceptive loss. Exp Brain Res 142:91–107PubMedCrossRefGoogle Scholar
  12. Carpenter MG, Allum JHJ, Honegger F (1999) Directional sensitivities of stretch reflexes and balance corrections for normal subjects in the roll and pitch planes. Exp Brain Res 129:93–113PubMedCrossRefGoogle Scholar
  13. Carpenter MG, Allum JHJ, Honegger F (2001) Vestibular influences on human postural control in combination of pitch and roll planes reveal differences in spatio temporal processing. Exp Brain Res 140:95–111PubMedCrossRefGoogle Scholar
  14. Carpenter MG, Allum JHJ, Honegger F, Adkin AL, Bloem BR (2004) Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiat 75:1245–1254PubMedCrossRefGoogle Scholar
  15. Diener HC, Horak FB, Nashner LM (1988) Influence of stimulus parameters on human postural responses. J Neurophysiol 59:1888–1905PubMedGoogle Scholar
  16. Dietz V (1998) Evidence for a load receptor contribution to the control of posture and locomotion. Neurosci Biobehav Rev 22:495–499PubMedCrossRefGoogle Scholar
  17. Forssberg H, Hirschfeld H (1994) Postural adjustments in sitting humans following external perturbations. Exp Brain Res 97:515–527PubMedCrossRefGoogle Scholar
  18. Grillner S, Hongo T (1972) Vestibulo spinal effects on motoneurons and interneurons in the lumbosacral cord. Prog Brain Res 37:243–262PubMedCrossRefGoogle Scholar
  19. Grillner S, Hongo T, Lund S (1971) Convergent effects on α-motoneurons from the vestibulospinal tract and a pathway descending in the medial longitudinal fasciculus. Exp Brain Res 12:457–479PubMedCrossRefGoogle Scholar
  20. Grüneberg C, Allum JHJ, Honegger F, Bloem BR (2004) The influence of artificially increased hip and trunk stiffness on balance control in the pitch and roll planes. Exp Brain Res 157:472–485PubMedCrossRefGoogle Scholar
  21. Grüneberg C, Duysens J, Honegger F, Allum JHJ (2005) Spatio-temporal separation of roll and pitch balance correcting commands in man. J Neurophysiol 94:3143–3158PubMedCrossRefGoogle Scholar
  22. Henry SM, Fung J, Horak FB (1998) EMG responses to maintain stance during multidirectional surface translations. J Neurophysiol 80:1939–1950PubMedGoogle Scholar
  23. Horak FB, Nashner LM, Diener HC (1990) Postural strategies associated with somatosensory and vestibular-loss. Exp Brain Res 82:167–177PubMedCrossRefGoogle Scholar
  24. Inglis JT, Macpherson JM (1995) Bilateral labyrinthectomy in the cat: effects on the postural response to translation. J Neurophysiol 73:1181–1191PubMedGoogle Scholar
  25. Katz R, Pierrot-Deseilligny E (1999) Recurrent inhibition in humans. Prog Neurobiol 57:325–355PubMedCrossRefGoogle Scholar
  26. Keshner EA, Allum JHJ, Pfaltz CR (1987) Postural coactivation and adaptation in the sway stabilizing responses of normals and patients with bilateral vestibular deficit. Exp Brain Res 69:77–92PubMedCrossRefGoogle Scholar
  27. Krutki P, Jankowska E, Edgley SA (2003) Are crossed actions of reticulospinal and vestibulospinal neurons on feline motoneurons mediated by the same or separate commissural neurons? J Neurosci 23:8041–8050PubMedGoogle Scholar
  28. Lacour M, Xerri C, Hugen M (1979) Compensation of postural reactions to fall in the vestibular neurectomized monkey. Role of remaining labyrinthic afferences. Exp Brain Res 37:563–580PubMedCrossRefGoogle Scholar
  29. Lindsay KW, Roberts TD, Rosenberg JR (1976) Asymmetric tonic labyrinth reflexes in the decerebrate cat. J Physiol 261:583–601PubMedGoogle Scholar
  30. MacPherson JM (1988) Strategies that simplify the control of quadrupedal stance and forces at the ground. J Neurophysiol 60:204–217PubMedGoogle Scholar
  31. MacPherson JM, Everaert DG, Stapley PJ, Ting LH (2007) Bilateral vestibular loss in cats leads to active destabilization of balance during pitch and roll rotations of the support-surface. J Neurophysiol 97:4357–4367PubMedCrossRefGoogle Scholar
  32. Mergner T, Huber W, Becker W (1997) Vestibular-neck interaction and transformation of sensory coordinates. J Ves Res 7:347–367CrossRefGoogle Scholar
  33. Nashner LM, Black FO, Wall C III (1982) Adaptation to altered support and visual conditions during stance in patients with vestibular deficits. J Neurosc 5:536–544Google Scholar
  34. Perry SD, McIlroy WE, Maki BE (2000) The role of plantar cutaneous mechanoreceptors in the control of compensatory stepping reactions evoked by unpredictable, multi-directional perturbation. Brain Res 877:401–406PubMedCrossRefGoogle Scholar
  35. Peterka RJ, Loughlin PJ (2004) Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 91:410–423PubMedCrossRefGoogle Scholar
  36. Peterson BW, Fukushima K, Hirgi N, Schor RH, Wilson VJ (1980) Responses of vestibulospinal and recticulospinal neurons to sinusoidal vestibular stimulation. J Neurophysiol 43:1236–1250PubMedGoogle Scholar
  37. Pompeiano O (1984) Excitatory and inhibitory influences on the spinal cord during vestibular and neck reflexes. Acta Otolaryngol (Stockh) Suppl 406:5–9Google Scholar
  38. Roberts TMD (1995) Understanding balance. The mechanics of posture and locomotion. Chapman and Hall, London, UKGoogle Scholar
  39. Runge CF, Shepert CL, Horak FB, Zajac FE (1998) Role of vestibular information in initiation of rapid postural responses. Exp Brain Res 122:403–412PubMedCrossRefGoogle Scholar
  40. Stapley PJ, Ting LH, Kuifu C, Everaert DG, MacPherson JM (2006) Bilateral vestibular loss leads to active destabilization of balance during voluntary head turns in the standing cat. J Neurophysiol 95:3783–3797PubMedCrossRefGoogle Scholar
  41. Ting LH, MacPherson JM (2004) Ratio of shear to ground-reaction force may underlie the directional tuning of the automatic postural response to rotation and translation. J Neurophysiol 92:808–823PubMedCrossRefGoogle Scholar
  42. Wilson VJ, Yoshida M (1969) Comparison of effects of stimulation of Dieters’ nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons. J Neurophysiol 32:743–758PubMedGoogle Scholar
  43. Wilson VJ, Melvill Jones G (1979) Mammation vestibular physiology. Plenum, New York, pp 239–245Google Scholar
  44. Wilson VJ, Schor RH, Suzuki I, Parks BR (1986) Spatial organisation of neck and vestibular reflexes acting on the forelimbs of the decerebrate cat. J Neurophysiol 55:514–526PubMedGoogle Scholar
  45. Wilson VJ, Schor RH (1999) The neural substrate of the vestibulo colic reflex. What needs to be learned. Exp Brain Res 129:483–493PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • John H. J. Allum
    • 1
    • 4
    Email author
  • Lars B. Oude Nijhuis
    • 1
    • 2
  • Mark G. Carpenter
    • 1
    • 3
  1. 1.Department of ORLUniversity HospitalBaselSwitzerland
  2. 2.Department of NeurologyRadboud University Medical CentreNijmegenThe Netherlands
  3. 3.School of Human KineticsUniversity of British ColumbiaVancouverCanada
  4. 4.University ORL ClinicBaselSwitzerland

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