Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis

Abstract

An implantable prosthesis that stimulates vestibular nerve branches to restore sensation of head rotation and vision-stabilizing reflexes could benefit individuals disabled by bilateral loss of vestibular sensation. The normal vestibular system encodes head movement by increasing or decreasing firing rate of the vestibular afferents about a baseline firing rate in proportion to head rotation velocity. Our multichannel vestibular prosthesis emulates this encoding scheme by modulating pulse rate and pulse current amplitude above and below a baseline stimulation rate (BSR) and a baseline stimulation current. Unilateral baseline prosthetic stimulation that mimics normal vestibular afferent baseline firing results in vestibulo-ocular reflex (VOR) eye responses with a wider range of eye velocity in response to stimuli modulated above baseline (excitatory) than below baseline (inhibitory). Stimulus modulation about higher than normal baselines resulted in increased range of inhibitory eye velocity, but decreased range of excitatory eye velocity. Simultaneous modulation of rate and current (co-modulation) above all tested baselines elicited a significantly wider range of excitatory eye velocity than rate or current modulation alone. Time constants associated with the recovery of VOR excitability following adaptation to elevated BSRs implicate synaptic vesicle depletion as a possible mechanism for the small range of excitatory eye velocity elicited by rate modulation alone. These findings can be used toward selecting optimal baseline levels for vestibular stimulation that would result in large inhibitory eye responses while maintaining a wide range of excitatory eye velocity via co-modulation.

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References

  1. Bagnall MW, McElvain L, Faulstich M, du Lac SV (2008) Frequency-independent synaptic transmission supports a linear vestibular behavior. Neuron 60:343–352

    PubMed  Article  CAS  Google Scholar 

  2. Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. 2. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182–203

    PubMed  CAS  Google Scholar 

  3. BeMent SL, Ranck JB Jr (1969) A quantitative study of electrical stimulation of central myelinated fibers. Exp Neurol 24:147–170

    PubMed  Article  CAS  Google Scholar 

  4. Black FO, Wade SW, Nashner LM (1996) What is the minimal vestibular function required for compensation? Am J Otol 17:401–409

    PubMed  Article  CAS  Google Scholar 

  5. Black FO, Gianna-Poulin C, Pesznecker SC (2001) Recovery from vestibular ototoxicity. Otol Neurotol 22:662–671

    PubMed  Article  CAS  Google Scholar 

  6. Black FO, Pesznecker S, Stallings V (2004) Permanent gentamicin vestibulotoxicity. Otol Neurotol 25:559–569

    PubMed  Article  Google Scholar 

  7. Cohen B, Suzuki J, Bender MB (1964) Eye movements from semicircular canal nerve stimulation in cat. Ann Otol Rhinol Laryngol 73:153

    PubMed  CAS  Google Scholar 

  8. Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res 5:67–107

    PubMed  Article  CAS  Google Scholar 

  9. Dai C, Fridman GY, Chiang B, Davidovics NS, Melvin T, Cullen KE, Della Santina CC (2011) Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp Brain Res 210:595–606

    PubMed  Article  Google Scholar 

  10. Davidovics NS, Fridman GY, Chiang B, Della Santina CC (2011) Effects of biphasic current pulse frequency, amplitude, duration, and interphase gap on eye movement responses to prosthetic electrical stimulation of the vestibular nerve. IEEE Trans Neural Syst Rehabil Eng 19:84–94

    PubMed  Article  Google Scholar 

  11. Della Santina C, Migliaccio A, Patel A (2005) Electrical stimulation to restore vestibular function development of a 3-d vestibular prosthesis. Conf Proc IEEE Eng Med Biol Soc 7:7380–7385

    PubMed  Google Scholar 

  12. Della Santina CC, Migliaccio AA, Patel AH (2007) A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-D vestibular sensation. IEEE Trans Biomed Eng 54:1016–1030

    PubMed  Article  Google Scholar 

  13. Fridman G, Davidovics N, Dai C, Migliaccio A, Della Santina C (2010a) Vestibulo-ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment. J Assoc Res Otolaryngol 11:367–381

    PubMed  Article  Google Scholar 

  14. Fridman GY, Blair HT, Blaisdell AP, Judy JW (2010b) A quantitative model for the perceived intensity of cortical electrical stimulation. Exp Brain Res 203:499–515

    PubMed  Article  Google Scholar 

  15. Gong WS, Merfeld DM (2000) Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Eng 28:572–581

    PubMed  Article  CAS  Google Scholar 

  16. Gong WS, Merfeld DM (2002) System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans Biomed Eng 49:175–181

    PubMed  Article  Google Scholar 

  17. Gong WS, Haburcakova C, Merfeld DM (2008) Vestibulo-ocular responses evoked via bilateral electrical stimulation of the lateral semicircular canals. IEEE Trans Biomed Eng 55:2608–2619

    PubMed  Article  Google Scholar 

  18. Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476

    PubMed  Article  CAS  Google Scholar 

  19. Hirvonen TP, Minor LB, Hullar TE, Carey JP (2005) Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla. J Neurophysiol 93:643–655

    PubMed  Article  Google Scholar 

  20. Kesar T, Chou L-W, Binder-Macleod SA (2008) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 18:662–671

    PubMed  Article  Google Scholar 

  21. Lewis RF, Merfeld DM, Gong WS (2001) Cross-axis vestibular adaptation produced by patterned electrical stimulation. Neurology 56:A18

    Google Scholar 

  22. Lewis RF, Gong WS, Ramsey M, Minor L, Boyle R, Merfeld DM (2002) Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res Equilib Orientat 12:87–94

    Google Scholar 

  23. Lewis R, Haburcakova C, Gong W, Makary C, Merfeld D (2010) Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 103:1066–1079

    PubMed  Article  Google Scholar 

  24. Mamoto Y, Yamamoto K, Imai T, Tamura M, Kubo T (2002) Three-dimensional analysis of human locomotion in normal subjects and patients with vestibular deficiency. Acta Otolaryngol 122:495–500

    PubMed  Article  Google Scholar 

  25. Merfeld DM, Gong WS, 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 53:2362–2372

    PubMed  Article  Google Scholar 

  26. Merfeld DM, Haburcakova C, Gong W, Lewis RF (2007) Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans Biomed Eng 54:1005–1015

    PubMed  Article  Google Scholar 

  27. Migliaccio AA, Della Santina CC, Carey JP, Niparko JK, Minor LB (2005) The vestibulo-ocular reflex response to head impulses rarely decreases after cochlear implantation. Otol Neurotol 26:655–660

    PubMed  Article  Google Scholar 

  28. Minor LB (1998) Gentamicin-induced bilateral vestibular hypofunction. Jama-J Am Med Assoc 279:541–544

    Article  CAS  Google Scholar 

  29. Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM (1998) Bilateral loss of vestibular function: clinical findings in 53 patients. J Neurol 245:314–321

    PubMed  Article  CAS  Google Scholar 

  30. Suzuki JI, Cohen B (1964) Head eye body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405

    PubMed  Article  CAS  Google Scholar 

  31. Suzuki J, Cohen B, Bender MB (1964) Compensatory eye movements induced by vertical semicircular canal stimulation. Exp Neurol 9:137–160

    PubMed  Article  CAS  Google Scholar 

  32. Suzuki JI, Goto K, Tokumasu K, Cohen B (1969) Implantation of electrodes near individual vestibular nerve branches in mammals. Ann Otol Rhinol Laryngol 78:815–826

    PubMed  CAS  Google Scholar 

  33. Telgkamp PRI (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447–8457

    PubMed  CAS  Google Scholar 

  34. Zeng F-G (2004) Trends in cochlear implants. Trends Amplif 8:1–34

    PubMed  Article  Google Scholar 

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Correspondence to Charles C. Della Santina.

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Davidovics, N.S., Fridman, G.Y. & Della Santina, C.C. Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis. Exp Brain Res 218, 389–400 (2012). https://doi.org/10.1007/s00221-012-3025-8

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Keywords

  • Vestibular
  • Prosthesis
  • Neural
  • Interface
  • Electrical stimulation
  • VOR