Adaptation of Vestibular Tone Studied with Electrical Stimulation of Semicircular Canal Afferents

  • Richard F. Lewis
  • Keyvan Nicoucar
  • Wangsong Gong
  • Csilla Haburcakova
  • Daniel M. Merfeld
Research Article

Abstract

Damage to one vestibular labyrinth or nerve causes a central tone imbalance, reflected by prominent spontaneous nystagmus. Central adaptive mechanisms eliminate the nystagmus over several days, and the mechanisms underlying this process have received extensive study. The characteristics of vestibular compensation when the tone imbalance is presented gradually or repeatedly have never been studied. We used high-frequency electrical stimulation of semicircular canal afferents to generate a vestibular tone imbalance and recorded the nystagmus produced when the stimulation was started abruptly or gradually and when it was repeatedly cycled on and off. In the acute-onset protocol, brisk nystagmus occurred when stimulation started, gradually resolved within 1 day, and reversed direction when the stimulation was stopped after 1 week. Repeated stimulation cycles resulted in progressively smaller nystagmus responses. In the slow-onset protocol, minimal nystagmus occurred while the stimulation ramped-up to its maximum rate over 12 h, but a reversal still occurred when the stimulation was stopped after 1 week, and repeated stimulation cycles did not affect this pattern. The absence of nystagmus during the 12 h ramp of stimulation demonstrates that central vestibular tone can rebalance relatively quickly, and the reduction in the stimulation-off nystagmus with repeated cycles of the acute-onset but not the slow-onset stimulation suggests that dual-state adaptation may have occurred with the former paradigm but not the latter.

Keywords

vestibular nystagmus compensation adaptation electrical stimulation 

References

  1. Balter SG, Stokroos RJ, Eterman RM, Paredis SA, Orbons J, Kingma H (2004) Habituation to galvanic vestibular stimulation. Acta Otolaryngol 124:941–945PubMedCrossRefGoogle Scholar
  2. Beraneck M, Idoux E (2012) Reconsidering the role of neuronal intrinsic properties and neuromodulation in vestibular homeostasis. Front Neurol 3:1–13CrossRefGoogle Scholar
  3. Beraneck M, McKee JL, Aleisa M, Cullen KE (2008) Asymmetric recovery in cerebellar-deficient mice following unilateral labyrinthectomy. J Neurophysiol 100:945–958PubMedCrossRefGoogle Scholar
  4. Berquest F, Ludwig M, Dutia MB (2008) Role of the commissural inhibitory system in vestibular compensation in the rat. J Physiol 586:4441–4452CrossRefGoogle Scholar
  5. Cohen H, Cohen B, Raphan T, Waespe W (1992) Habituation and adaptation of the vestibuloocular reflex: a model of differential control by the vestibulocerebellum. Exp Brain Res 90:526–538PubMedCrossRefGoogle Scholar
  6. Courjon JH, Precht W, Sirkin DW (1987) Vestibular nerve and nuclei unit responses and eye movement responses to repetitive galvanic stimulation of the labyrinth in the rat. Exp Brain Res 66:41–48PubMedCrossRefGoogle Scholar
  7. Curthoys IS (1975) The orientation of the semicircular canals in guinea pigs. Acta Otolaryngol 80:197–205PubMedCrossRefGoogle Scholar
  8. Curthoys IS (2000) Vestibular compensation and substitution. Curr Opin Neurol 13:27–30PubMedCrossRefGoogle Scholar
  9. Darlington CL, Smith PF (2000) Molecular mechanisms of recovery from vestibular damage in mammals: recent advances. Prog Neurobiol 62:313–325PubMedCrossRefGoogle Scholar
  10. Day AS, Wang CT, Chen CN, Young YH (2008) Correlating the cochlearvestibular deficits with tumor size of acoustic neuroma. Acta Otolaryngol 128:756–760PubMedCrossRefGoogle Scholar
  11. Dieringer N (1995) ‘Vestibular compensation’: neural plasticity and its relations to functional recovery after labyrinthine lesions in frogs and other vertebrates. Prog Neurobiol 46:97–129PubMedGoogle Scholar
  12. Escudero M, de Waele C, Vibert N, Berthoz A, Vidal PP (1993) Saccadic eye movements and the horizontal vestibulo-ocular and vestibule-collic reflexes in the intact guinea pig. Exp Brain Res 97:254–262PubMedCrossRefGoogle Scholar
  13. Fetter M, Zee DS (1988) Recovery from unilateral labyrinthectomy in rhesus monkey. J Neurophysiol 59:370–393PubMedGoogle Scholar
  14. Gittis AH, du Lac S (2006) Intrinsic and synaptic plasticity in the vestibular system. Curr Opin Neurobiol 16:385–390PubMedCrossRefGoogle Scholar
  15. Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. III. Variations among units in their discharge properties. J Neurophysiol 34:676–684PubMedGoogle Scholar
  16. 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 51:1236–1256PubMedGoogle Scholar
  17. Gong W, Merfeld DM (2000) Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Eng 28:572–581PubMedCrossRefGoogle Scholar
  18. Gong W, Merfeld DM (2002) System design and performance of a unilateral horizontal semicircular prosthesis. IEEE Trans Biomed Eng 49:175–181PubMedCrossRefGoogle Scholar
  19. Hain TC, Fetter M, Zee DS (1987) Head-shaking nystagmus in patients with unilateral peripheral vestibular lesions. Am J Otolaryngol 8:36–47PubMedCrossRefGoogle Scholar
  20. Halmagyi GM, Weber KP, Curthoys IS (2010) Vestibular function after acute vestibular neuritis. Restor Neurol Neurosci 28:37–46PubMedGoogle Scholar
  21. Johnston AR, Seckl JR, Dutia MB (2002) Role of the flocculus in mediating vestibular nucleus neuron plasticity during vestibular compensation in the rat. J Physiol 545:903–911PubMedCrossRefGoogle Scholar
  22. Kandel E, Kupferman I, Iverson S (2000) Learning and memory. In: Kandel E, Schwartz J, Jessel T (eds) Principals of neural science. McGraw-Hill, New York, pp 1227–1246Google Scholar
  23. Lewis RF, Tamargo RJ (2001) Cerebellar lesions impair context-dependent adaptation of reaching movements in primates. Exp Brain Res 138:263–267PubMedCrossRefGoogle Scholar
  24. Lewis RF, Haburcakova C, Gong W, Makary C, Merfeld DM (2010) Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 103:1066–1079PubMedCrossRefGoogle Scholar
  25. Lim R, Callister RJ, Brichta AM (2010) An increase glycinergic quantal amplitude and frequency during early vestibular compensation in the mouse. J Neurophysiol 103:16–24PubMedCrossRefGoogle Scholar
  26. Merfeld DM, Gong W, Morrissey J, Saginaw M, Haburcakova C, Lewis RF (2006) Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng 53:2362–2372PubMedCrossRefGoogle Scholar
  27. Norris SA, Hathaway EN, Taylor JA, Thach WT (2011) Cerebellar inactivation impairs memory of learned prism gaze-reach calibrations. J Neurophysiol 105:2248–2259PubMedCrossRefGoogle Scholar
  28. Pettorossi VE, Dieni CV, Scarduzio M, Grassi S (2011) Long-term potentiation of synaptic response and intrinsic excitability in neurons of the rat medial vestibular nuclei. Neuroscience 187:1–14PubMedCrossRefGoogle Scholar
  29. Quinn KJ (1998) Classical conditioning using using vestibular reflexes. J Vestib Res 8:117–132PubMedCrossRefGoogle Scholar
  30. Ris L, Godaux E (1998a) Spike discharge regularity of vestibular neurons in labyrinthectomized guinea pigs. Neurosci Lett 253:131–134PubMedCrossRefGoogle Scholar
  31. Ris L, Godaux E (1998b) Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 80:2352–2367PubMedGoogle Scholar
  32. Shelhamer M, Robinson DA, Tan HS (1992) Contex-specific adaptation of the gain of the vestibulo-ocular reflex in humans. J Vestib Res 2:89–96PubMedGoogle Scholar
  33. Thach WT (1996) Context-response linkage. Int Rev Neurobiol 41:599–611CrossRefGoogle Scholar
  34. Tykocinski M, Shepard RK, Clark G (1995) Reduction in excitability of the auditory nerve following electrical stimulation at high stimulus rates. Hear Res 88:124–142PubMedCrossRefGoogle Scholar
  35. Vidal P-P, de Waele C, Vibert N, Muhlethaler M (1998) Vestibular compensation revisited. Otolaryngol Head Neck Surg 119:34–42PubMedCrossRefGoogle Scholar
  36. Welch R (1978) Perceptual modification: adapting to altered sensory environments. Academic, New YorkGoogle Scholar

Copyright information

© Association for Research in Otolaryngology 2013

Authors and Affiliations

  • Richard F. Lewis
    • 1
    • 2
    • 3
  • Keyvan Nicoucar
    • 1
    • 2
    • 4
  • Wangsong Gong
    • 1
  • Csilla Haburcakova
    • 1
    • 2
  • Daniel M. Merfeld
    • 1
    • 2
  1. 1.Jenks Vestibular Physiology LaboratoryMassachusetts Eye and Ear InfirmaryBostonUSA
  2. 2.Otology and LaryngologyHarvard Medical SchoolBostonUSA
  3. 3.Department of NeurologyHarvard Medical SchoolBostonUSA
  4. 4.Service of Oto-Rhino-Laryngology, Head and Neck Surgery, University Hospital of Geneva, Faculty of MedicineUniversity of GenevaGenevaSwitzerland

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