Experimental Brain Research

, Volume 223, Issue 2, pp 189–197 | Cite as

Dynamic transformation of vestibular signals for orientation

Research Article

Abstract

The same pattern of vestibular afferent feedback may signify a loss of balance or a change in body orientation, depending upon the initial head posture. To resolve this ambiguity and generate an appropriate motor response, the CNS must transform vestibular information from a head-centred reference frame into relevant motor coordinates. But what if the reference frame is continuously moving? Here, we ask if this neural transformation process is continuously updated during a voluntary change in head posture. Galvanic vestibular stimulation (GVS) was used to induce a sensation of head roll motion in blindfolded subjects marching on the spot. When head orientation was fixed, this caused unconscious turning behaviour that was maximal during neck flexion, minimal with the head level and reversed direction with neck extension. Subjects were then asked to produce a continuous voluntary change in head pitch, while GVS was applied. As the neck moved from full flexion into extension, turn velocity was continuously modulated and even reversed direction, reflecting the pattern observed during the head-fixed condition. Hence, an identical vestibular input resulted in motor output which was dynamically modulated by changes in head pitch. However, response magnitude was significantly reduced, suggesting possible suppression of vestibular input during voluntary head movement. Nevertheless, these results show that the CNS continuously reinterprets vestibular exafference to account for ongoing voluntary changes in head posture. This may explain why the head can be moved freely without losing the sense of balance and orientation.

Keywords

Vestibular Locomotion Galvanic vestibular stimulation Voluntary movement Orientation 

Notes

Acknowledgments

Thanks to Lucy Taylor, Adam Floyd, Robert Godfrey and Sebastian Smythe for help with subject recruitment and to Steve Allen for technical assistance. CJO is supported by the BBSRC.

References

  1. Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150PubMedCrossRefGoogle Scholar
  2. Barnett-Cowan M, Harris LR (2009) Perceived timing of vestibular stimulation relative to touch, light and sound. Exp Brain Res 198:221–231PubMedCrossRefGoogle Scholar
  3. Barnett-Cowan M, Harris LR (2011) Temporal processing of active and passive head movement. Exp Brain Res 214:27–35PubMedCrossRefGoogle Scholar
  4. Boyle R, Belton T, McCrea RA (1996) Responses of identified vestibulospinal neurons to voluntary eye and head movements in the squirrel monkey. Ann NY Acad Sci 781:244–263PubMedCrossRefGoogle Scholar
  5. Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706PubMedCrossRefGoogle Scholar
  6. Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933PubMedCrossRefGoogle Scholar
  7. Cullen KE, Brooks JX, Sadeghi SG (2009) How actions alter sensory processing: reafference in the vestibular system. Ann NY Acad Sci 1164:29–36PubMedCrossRefGoogle Scholar
  8. Day BL, Fitzpatrick RC (2005) Virtual head rotation reveals a process of route reconstruction from human vestibular signals. J Physiol 567:591–597PubMedCrossRefGoogle Scholar
  9. Fitzpatrick RC, Day BL (2004) Probing the human vestibular system with galvanic stimulation. J Appl Physiol 96:2301–2316PubMedCrossRefGoogle Scholar
  10. Fitzpatrick RC, Butler JE, Day BL (2006) Resolving head rotation for human bipedalism. Curr Biol 16:1509–1514PubMedCrossRefGoogle Scholar
  11. 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 117:307–309PubMedCrossRefGoogle Scholar
  12. McCrea RA, Gdowski GT, Boyle R, Belton T (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82:416–428PubMedGoogle Scholar
  13. Menz HB, Lord SR, Fitzpatrick RC (2003a) Acceleration patterns of the head and pelvis when walking are associated with risk of falling in community-dwelling older people. J Gerontol A Biol Sci Med Sci 58:M446–M452PubMedCrossRefGoogle Scholar
  14. Menz HB, Lord SR, Fitzpatrick RC (2003b) Acceleration patterns of the head and pelvis when walking on level and irregular surfaces. Gait Posture 18:35–46PubMedCrossRefGoogle Scholar
  15. Pozzo T, Berthoz A, Lefort L (1990) Head stabilization during various locomotor tasks in humans. I. Normal subjects. Exp Brain Res 82:97–106PubMedCrossRefGoogle Scholar
  16. Pozzo T, Levik Y, Berthoz A (1995) Head and trunk movements in the frontal plane during complex dynamic equilibrium tasks in humans. Exp Brain Res 106:327–338PubMedCrossRefGoogle Scholar
  17. Reynolds RF (2011) Vertical torque responses to vestibular stimulation in standing humans. J Physiol 589:3943–3953PubMedGoogle Scholar
  18. Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142PubMedGoogle Scholar
  19. Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111PubMedCrossRefGoogle Scholar
  20. Severac CA, Faldon M, Popov K, Day BL, Bronstein AM (2003) Short-latency eye movements evoked by near-threshold galvanic vestibular stimulation. Exp Brain Res 148:414–418Google Scholar
  21. St George RJ, Fitzpatrick RC (2011) The sense of self-motion, orientation and balance explored by vestibular stimulation. J Physiol 589:807–813PubMedCrossRefGoogle Scholar
  22. Yakusheva TA, Shaikh AG, Green AM, Blazquez PM, Dickman JD, Angelaki DE (2007) Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron 54:973–985PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.School of Sport and Exercise Sciences, College of Life and Environmental SciencesUniversity of BirminghamEdgbastonUK

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