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Unilateral Adaptation of the Human Angular Vestibulo-Ocular Reflex

  • Americo A. Migliaccio
  • Michael C. Schubert
Research Article

Abstract

A recent study showed that the angular vestibulo-ocular reflex (VOR) can be better adaptively increased using an incremental retinal image velocity error signal compared with a conventional constant large velocity-gain demand (×2). This finding has important implications for vestibular rehabilitation that seeks to improve the VOR response after injury. However, a large portion of vestibular patients have unilateral vestibular hypofunction, and training that raises their VOR response during rotations to both the ipsilesional and contralesional side is not usually ideal. We sought to determine if the vestibular response to one side could selectively be increased without affecting the contralateral response. We tested nine subjects with normal vestibular function. Using the scleral search coil and head impulse techniques, we measured the active and passive VOR gain (eye velocity / head velocity) before and after unilateral incremental VOR adaptation training, consisting of self-generated (active) head impulses, which lasted ∼15 min. The head impulses consisted of rapid, horizontal head rotations with peak-amplitude 15 o, peak-velocity 150 o/s and peak-acceleration 3,000 o/s2. The VOR gain towards the adapting side increased after training from 0.92 ± 0.18 to 1.11 ± 0.22 (+22.7 ± 20.2 %) during active head impulses and from 0.91 ± 0.15 to 1.01 ± 0.17 (+11.3 ± 7.5 %) during passive head impulses. During active impulses, the VOR gain towards the non-adapting side also increased by ∼8 %, though this increase was ∼70 % less than to the adapting side. A similar increase did not occur during passive impulses. This study shows that unilateral vestibular adaptation is possible in humans with a normal VOR; unilateral incremental VOR adaptation may have a role in vestibular rehabilitation. The increase in passive VOR gain after active head impulse adaptation suggests that the training effect is robust.

Keywords

vestibulo-ocular reflex (VOR) unilateral vestibular adaptation incremental retinal image velocity error vestibular rehabilitation 

Notes

Acknowledgments

This study was supported by a National Health and Medical Research Council (Australia) Biomedical Career Development Award to A.A. Migliaccio.

References

  1. Aw ST, Haslwanter T, Halmagyi GM, Curthoys IS, Yavor RA, Todd MJ (1996) Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects. J Neurophysiol 76:4009–4020PubMedGoogle Scholar
  2. Babalian AL, Vidal PP (2000) Floccular modulation of vestibuloocular pathways and cerebellum-related plasticity: an in vitro whole brain study. J Neurophysiol 84:2514–2528PubMedGoogle Scholar
  3. Belton T, McCrea RA (2004) Context contingent signal processing in the cerebellar flocculus and ventral paraflocculus during gaze saccades. J Neurophysiol 92:797–807PubMedCrossRefGoogle Scholar
  4. Blazquez PM, Hirata Y, Highstein SM (2006) Chronic changes in inputs to dorsal Y neurons accompany VOR motor learning. J Neurophysiol 95:1812–1825PubMedCrossRefGoogle Scholar
  5. Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706PubMedCrossRefGoogle Scholar
  6. Diggle PJ, Liang KY, Zeger SL (1994) Analysis of longitudinal data. Oxford University Press, New YorkGoogle Scholar
  7. Galiana HL, Green AM (1998) Vestibular adaptation: how models can affect data interpretations. Otolaryngol Head Neck Surg 119:231–243PubMedCrossRefGoogle Scholar
  8. Gauthier GM, Robinson DA (1975) Adaptation of human’s vestibulo-ocular reflex to magnifying glasses. Brain Res 92:331–335PubMedCrossRefGoogle Scholar
  9. Gonshor A, Melvill Jones G (1976a) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol 256:361–379Google Scholar
  10. Gonshor A, Melvill Jones G (1976b) Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol 256:381–414Google Scholar
  11. Halmagyi GM, Curthoys IS (1988) A clinical sign of canal paresis. Arch Neurol 45:737–739PubMedCrossRefGoogle Scholar
  12. Halmagyi GM, Curthoys IS, Cremer PD, Henderson CJ, Todd MJ, Staples MJ, D'Cruz DM (1990) The human horizontal vestibulo-ocular reflex in response to high-acceleration stimulation before and after unilateral vestibular neurectomy. Exp Brain Res 81:479–490PubMedCrossRefGoogle Scholar
  13. Haslwanter T (1995) Mathematics of three-dimensional eye rotations. Vis Res 35:1727–1739Google Scholar
  14. Hepp K (1990) On Listing’s law. Commun Math Phys 132:285–295CrossRefGoogle Scholar
  15. Hullar TE, Minor LB (1999) High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes. J Neurophysiol 82:2000–2005PubMedGoogle Scholar
  16. Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuomotor distortions. Exp Brain Res 115:557–561PubMedCrossRefGoogle Scholar
  17. Kilgard MP, Merzenich MM (2002) Order-sensitive plasticity in adult primary auditory cortex. Proc Natl Acad Sci USA 99:3205–3209PubMedCrossRefGoogle Scholar
  18. Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol 41:733–763PubMedGoogle Scholar
  19. Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346–354PubMedGoogle Scholar
  20. Lisberger SG, Pavelko TA, Broussard DM (1994a) Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. J Neurophysiol 72:928–953PubMedGoogle Scholar
  21. Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994b) Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. J Neurophysiol 72:954–973PubMedGoogle Scholar
  22. Lisberger SG (1994) Neural basis for motor learning in the vestibulo-ocular reflex of primates. III Computational and behavioral analysis of the sites of learning. J Neurophysiol 72:974–999PubMedGoogle Scholar
  23. McConville KM, Tomlinson RD, NA EQ (1996) Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli. J Neurophysiol 76:3136–3148PubMedGoogle Scholar
  24. McCrea RA, Yoshida K, Evinger C, Berthoz A (1981) The location, axonal arborization and termination sites of eye-movement-related secondary vestibular neurons demonstrated by intra-axonal HRP injection in the alert cat. In: Fuchs A, Becker W (eds) Progress in oculomotor research. Elsevier/North Holland, Amsterdam, pp 379–386Google Scholar
  25. McCrea RA, Luan H (2003) Signal processing of semicircular canal and otolith signals in the vestibular nuclei during passive and active head movements. Ann N Y Acad Sci 1004:169–182PubMedCrossRefGoogle Scholar
  26. Migliaccio AA, Todd MJ (1999) Real-time rotation vectors. Australas Phys Eng Sci Med 22:73–80PubMedGoogle Scholar
  27. Migliaccio AA, Minor LB, Carey JP (2004) Vergence-mediated modulation of the human horizontal vestibulo-ocular reflex is eliminated by a partial peripheral gentamicin lesion. Exp Brain Res 159:92–98PubMedCrossRefGoogle Scholar
  28. Nagarajan S, Mahncke H, Salz T, Tallal P, Roberts T, Merzenich MM (1999) Cortical auditory signal processing in poor readers. Proc Natl Acad Sci USA 96:6483–6488PubMedCrossRefGoogle Scholar
  29. Nagarajan SS, Blake DT, Wright BA, Byl N, Merzenich MM (1998) Practice-related improvements in somatosensory interval discrimination are temporally specific but generalize across skin location, hemisphere, and modality. J Neurosci 18:1559–1570PubMedGoogle Scholar
  30. Paige GD (1994) Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging. Exp Brain Res 98:355–372PubMedCrossRefGoogle Scholar
  31. Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492PubMedGoogle Scholar
  32. Schubert MC, Della Santina CC, Shelhamer M (2008) Incremental angular vestibulo-ocular reflex adaptation to active head rotation. Exp Brain Res 191:435–446PubMedCrossRefGoogle Scholar
  33. Snyder LH, King WM (1996) Behavior and physiology of the macaque vestibulo-ocular reflex response to sudden off-axis rotation: computing eye translation. Brain Res Bull 40:293–301PubMedCrossRefGoogle Scholar
  34. Straumann D, Zee DS, Solomon D, Lasker AG, Roberts DC (1995) Transient torsion during and after saccades. Vision Res 35:3321–3334PubMedCrossRefGoogle Scholar
  35. Szturm T, Ireland DJ, Lessing-Turner M (1994) Comparison of different exercise programs in the rehabilitation of patients with chronic peripheral vestibular dysfunction. J Vestib Res 4:461–479PubMedGoogle Scholar
  36. Ushio M, Minor LB, Della Santina CC, Lasker DM (2011) Unidirectional rotations produce asymmetric changes in horizontal VOR gain before and after unilateral labyrinthectomy in macaques. Exp Brain Res 210:651–660PubMedCrossRefGoogle Scholar
  37. Viirre E, Sitarz R (2002) Vestibular rehabilitation using visual displays: preliminary study. Laryngoscope 112:500–503PubMedCrossRefGoogle Scholar

Copyright information

© Association for Research in Otolaryngology 2012

Authors and Affiliations

  • Americo A. Migliaccio
    • 1
    • 2
    • 3
  • Michael C. Schubert
    • 3
  1. 1.Balance and Vision LaboratoryNeuroscience Research AustraliaRandwick New South WalesAustralia
  2. 2.University of New South WalesSydneyAustralia
  3. 3.Department of Otolaryngology – Head and Neck SurgeryJohns Hopkins University School of MedicineBaltimoreUSA

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