Effects of biphasic current pulse frequency, amplitude, duration, and interphase gap on eye movement responses to prosthetic electrical stimulation of the vestibular nerve

IEEE Transactions on Neural Systems and Rehabilitation Engineering

Volumn 19, Issue 1, 2011, Pages 84-94

  Davidovics, Natan S ^a   Fridman, Gene Y ^a   Chiang, Bryce ^a   Santina, Charles C Della ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Electrical stimulation; interphase gap; neural; prosthesis; pulse duration; vestibular; vestibular implant

Indexed keywords

ELECTRICAL STIMULATIONS; INTERPHASE GAP; NEURAL; PROSTHESIS; PULSE DURATION; VESTIBULAR; VESTIBULAR IMPLANT;

ANIMALS; ENCODING (SYMBOLS); FREQUENCY RESPONSE; OPTIMIZATION; PROSTHETICS; PULSE TIME MODULATION; RESTORATION; ROTATION;

EYE MOVEMENTS;

ANIMAL; ARTICLE; CHINCHILLA; ELECTROSTIMULATION THERAPY; EYE MOVEMENT; METHODOLOGY; PATHOPHYSIOLOGY; VESTIBULAR DISORDER; VESTIBULAR NERVE; VESTIBULOOCULAR REFLEX;

ANIMALS; CHINCHILLA; ELECTRIC STIMULATION THERAPY; EYE MOVEMENTS; REFLEX, VESTIBULO-OCULAR; VESTIBULAR DISEASES; VESTIBULAR NERVE;

EID: 79951605454     PISSN: 15344320     EISSN: None     Source Type: Journal    
DOI: 10.1109/TNSRE.2010.2065241     Document Type: Article

References (72)

1. J. P. Carey and C. C. Della Santina, "Principles of applied vestibular physiology," in Otolaryngology-Head & Neck Surgery, C. W. Cummings, Ed. New York: Elsevier, 2005, pp. 3115-3159.
2. F. O. Black, C. Gianna-Poulin, and S. C. Pesznecker, "Recovery from vestibular ototoxicity," Otology Neurotol., vol. 22, pp. 662-671, 2001. (Pubitemid 32845643)
3. F. O. Black, S. Pesznecker, and V. Stallings, "Permanent gentamicin vestibulotoxicity," Otology Neurotol., vol. 25, pp. 559-569, 2004. (Pubitemid 39079780)
4. Y. Mamoto, K. Yamamoto, T. Imai, M. Tamura, and T. Kubo, "Threedimensional analysis of human locomotion in normal subjects and patients with vestibular deficiency," Acta Oto-Laryngologica, vol. 122, pp. 495-500, 2002. (Pubitemid 34913428)
5. T. Rinne, A. M. Bronstein, P. Rudge, M. A. Gresty, and L. M. Luxon, "Bilateral loss of vestibular function: Clinical findings in 53 patients," J. Neurol., vol. 245, pp. 314-321, 1998. (Pubitemid 28286795)
6. L. B. Minor, "Gentamicin-induced bilateral vestibular hypofunction," JAMA, vol. 279, pp. 541-544, 1998. (Pubitemid 28113434)
7. C. C. Della Santina, V. Potyagaylo, A. A. Migliaccio, L. B. Minor, and J. P. Carey, "Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction," J. Assoc. Res. Otolaryngol., vol. 6, pp. 191-206, 2005.
8. J. R. Ewald, Physiologische Untersuchugen Uber Das Endorgans Des Nervus Octavus. Wiesbaden, Germany: Bergmann, 1892.
9. V. J.Wilson and J. Melvill, Mammalian Vestibular Physiology. New York: Plenum, 1979.
10. B. Cohen, J. Suzuki, and M. B. Bender, "Eye movements from semicircular canal nerve stimulation in cat," Ann. Otology Rhinology Laryngol., vol. 73, p. 153, 1964.
11. J. Suzuki, B. Cohen, and M. B. Bender, "Compensatory eyemovements induced by vertical semicircular canal stimulation," Exp. Neurol., vol. 9, p. 137, 1964.
12. J. I. Suzuki and B. Cohen, "Head eye body + limb movements from semicircular canal nerves," Exp. Neurol., vol. 10, p. 393, 1964.
13. J. I. Suzuki, K. Goto, K. Tokumasu, and B. Cohen, "Implantation of electrodes near individual vestibular nerve branches in mammals," Ann. Otology Rhinology Laryngol., vol. 78, p. 815, 1969.
14. D. M. Merfeld, C. Haburcakova, W. Gong, and R. F. Lewis, "Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis," IEEE Trans. Biomed. Eng., vol. 54, no. 6, pp. 1005-1015, Jun. 2007. (Pubitemid 46815120)
15. D. M. Merfeld, W. S. Gong, J. Morrissey, M. Saginaw, C. Haburcakova, and R. F. Lewis, "Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis," IEEE Trans. Biomed. Eng., vol. 53, no. 11, pp. 2362-2372, Nov. 2006. (Pubitemid 44629876)
16. R. F. Lewis, W. S. Gong, M. Ramsey, L. Minor, R. Boyle, and D. M. Merfeld, "Vestibular adaptation studied with a prosthetic semicircular canal," J. Vestibular Res.-Equilibrium Orientat., vol. 12, pp. 87-94, 2002. (Pubitemid 36819413)
17. W. S. Gong and D. M. Merfeld, "System design and performance of a unilateral horizontal semicircular canal prosthesis," IEEE Trans. Biomed. Eng., vol. 49, no. 2, pp. 175-181, Feb. 2002. (Pubitemid 34112728)
18. W. S. Gong and D. M. Merfeld, "Prototype neural semicircular canal prosthesis using patterned electrical stimulation," Ann. Biomed. Eng., vol. 28, pp. 572-581, 2000.
19. R. F. Lewis, D. M. Merfeld, and W. S. Gong, "Cross-axis vestibular adaptation produced by patterned electrical stimulation," Neurology, vol. 56, p. A18, 2001.
20. W. S. Gong, C. Haburcakova, and D. M. Merfeld, "Vestibulo-ocular responses evoked via bilateral electrical stimulation of the lateral semicircular canals," IEEE Trans. Biomed. Eng., vol. 55, no. 11, pp. 2608-2619, Nov. 2008.
21. G. Y. Fridman, N. Davidovics, C. Dai, and C. C. Della Santina, "Multichannel vestibular prosthesis stabilizes eyes for head rotation about any axis," JARO, vol. 11, no. 3, pp. 367-381, 2009.
22. B. Chiang, G. Y. Fridman, and C. C. Della Santina, Enhancements to the Johns Hopkins multi-channel vestibular prosthesis yield reduced size, extended battery life, current steering and wireless control Assoc. Res. Otolaryngol., Baltimore, MD, 2009.
23. C. C. Della Santina, A. A. Migliaccio, and A. H. Patel, "A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-D vestibular sensation," IEEE Trans. Biomed. Eng., vol. 54, no. 6, pp. 1016-1030, Jun. 2007. (Pubitemid 46815113)
24. C. C. Della Santina, A. Migliaccio, and A. Patel, "Electrical stimulation to restore vestibular function development of a 3-D vestibular prosthesis," in Conf. Proc. IEEE Eng. Med. Biol. Soc., 2005, vol. 7, pp. 7380-5. (Pubitemid 46230689)
25. G. E. Grossman, R. J. Leigh, E. N. Bruce, W. P. Huebner, and D. J. Lanska, "Performance of the human vestibuloocular reflex during locomotion," J. Neurophysiol., vol. 62, pp. 264-272, 1989. (Pubitemid 19180559)
26. B. S. Wilson and M. F. Dorman, "Cochlear implants: A remarkable past and a brilliant future," Hearing Res., vol. 242, pp. 3-21, 2008.
27. B. S. Wilson, C. C. Finley, D. T. Lawson, R. D. Wolford, D. K. Eddington, and W. M. Rabinowitz, "Better speech recognition with cochlear implants," Nature, vol. 352, pp. 236-238, 1991. (Pubitemid 21912323)
28. F. G. Zeng, A. N. Popper, and R. R. Fay, Cochlear Implants: Auditory Prostheses and Electric Hearing. New York: Springer-Verlag, 2004.
29. W. M. Grill and J. T. Mortimer, "The effect of stimulus pulse duration on selectivity of neural stimulation," IEEE Trans. Biomed. Eng., vol. 43, no. 2, pp. 161-166, Feb. 1996. (Pubitemid 26055575)
30. P. H. Gorman and J. T. Mortimer, "The effect of stimulus parameters on the recruitment characteristics of direct nerve-stimulation," IEEE Trans. Biomed. Eng., vol. 30, no. 7, pp. 407-414, Jul. 1983. (Pubitemid 13574005)
31. A. K. Ahuja, M. R. Behrend, M. Kuroda, M. S. Humayun, and J. D. Weiland, "An in vitro model of a retinal prosthesis," IEEE Trans. Biomed. Eng., vol. 55, no. 6, pp. 1744-1753, Jun. 2008. (Pubitemid 351728014)
32. D. R. Merrill, M. Bikson, and J. G. R. Jefferys, "Electrical stimulation of excitable tissue: Design of efficacious and safe protocols," J. Neurosci. Methods, vol. 141, pp. 171-198, 2005. (Pubitemid 40136531)
33. R. A. Baird, G. Desmadryl, C. Fernandez, and J. M. Goldberg, "The vestibular nerve of the chinchilla .2. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals," J. Neurophysiol., vol. 60, pp. 182-203, 1988.
34. C. Fernandez, R. A. Baird, and J. M. Goldberg, "The vestibular nerve of the chinchilla .1. peripheral innervation patterns in the horizontal and superior semicircular canals," J. Neurophysiol., vol. 60, pp. 167-181, 1988.
35. T. E. Hullar and L. B. Minor, "High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes," J. Neurophysiol., vol. 82, pp. 2000-5, 1999. (Pubitemid 29471289)
36. R. F. Lewis, C. Haburcakova, and D. M. Merfeld, "Roll tilt psychophysics in rhesus monkeys during vestibular and visual stimulation," J. Neurophysiol., vol. 100, pp. 140-153, 2008.
37. C. C. Della Santina, A. A. Migliaccio, and A. H. Patel, "Electrical stimulation to restore vestibular function-Development of a 3-D vestibular prosthesis," in Proc. 27th Annu. IEEE Eng. Med. Biol., Shanghai, China, 2005, p. 7380.
38. P. Prado-Guitierrez, L. M. Fewster, J.M. Heasman, C. M. McKay, and R. K. Shepherd, "Effect of interphase gap and pulse duration on electrically evoked potentials is correlated with auditory nerve survival," Hearing Res., vol. 215, pp. 47-55, 2006.
39. A. V. Hill, "Excitation and accomodation in nerve," Proc. R. Soc. B, vol. 119, pp. 305-355, 1936.
40. L. Lapicque, "Recherches quantitatives sur l'excitation électrique des nerfs traitée comme une polarisation," J. Physiologie et de Pathologie Générale, vol. 9, pp. 620-635, 1907.
41. L. Lapicque, "Quantitative investigations of electrical nerve excitation treated as polarization. 1907," Biol. Cybern., vol. 97, pp. 341-9, 2007.
42. C. Vandenhonert and P. H. Stypulkowski, "Physiological-properties of the electrically stimulated auditory-nerve .2. Single fiber recordings," Hearing Res., vol. 14, pp. 225-243, 1984. (Pubitemid 14088243)
43. C. M. McKay and H. J. McDermott, "The perceptual effects of current pulse duration in electrical stimulation of the auditory nerve," J. Acoust. Soc. Am., vol. 106, pp. 998-1009, 1999. (Pubitemid 29379527)
44. E. N. Warman, W. M. Grill, and D. Durand, "Modeling the effects of electric-fields on nerve-fibers-Determination of excitation thresholds," IEEE Trans. Biomed. Eng., vol. 39, no. 12, pp. 1244-1254, Dec. 1992. (Pubitemid 23127282)
45. R. P. Carlyon, A. van Wieringen, J. M. Deeks, C. J. Long, J. Lyzenga, and J.Wouters, "Effect of inter-phase gap on the sensitivity of cochlear implant users to electrical stimulation," Hearing Res., vol. 205, pp. 210-224, 2005. (Pubitemid 40823012)
46. C. M. McKay and K. R. Henshall, "The perceptual effects of interphase gap duration in cochlear implant stimulation," Hearing Res., vol. 181, pp. 94-99, 2003. (Pubitemid 36809064)
47. R. K. Shepherd and E. Javel, "Electrical stimulation of the auditory nerve: II. Effect of stimulus waveshape on single fibre response properties," Hearing Res., vol. 130, pp. 171-188, 1999. (Pubitemid 29172592)
48. C. Vandenhonert and J. T. Mortimer, "Response of the myelinated nerve-fiber to short duration biphasic stimulating currents," Ann. Biomed. Eng., vol. 7, pp. 117-125, 1979. (Pubitemid 10105481)
49. A. vanWieringen, R. P. Carlyon, O. Macherey, and J.Wouters, "Effects of pulse rate on thresholds and loudness of biphasic and alternating monophasic pulse trains in electrical hearing," Hearing Res., vol. 220, pp. 49-60, 2006. (Pubitemid 44348914)
50. A. van Wieringen, O. Macherey, R. P. Carlyon, J. M. Deeks, and J. Wouters, "Alternative pulse shapes in electrical hearing," Hearing Res., vol. 242, pp. 154-63, 2008.
51. A. van Wieringen, R. P. Carlyon, and J. Wouters, "Spatial excitation patterns of different pulse shapes and electrode configurations in cochlear implantees," presented at the Conf. Implantable Auditory Prostheses, Asilomar, CA, 2005.
52. S. Tang, T. A. N. Melvin, and C. C. Della Santina, "Effects of semicircular canal electrode implantation on hearing in chinchillas," Acta Oto-Laryngologica, vol. 129, pp. 481-486, 2009.
53. A. A. Migliaccio, H. G. MacDougall, L. B. Minor, and C. C. D. Santina, "Inexpensive system for real-time 3-dimensional video-oculography using a fluorescent marker array," J. Neurosci. Methods, vol. 143, pp. 141-150, 2005. (Pubitemid 40462258)
54. T. E. Hullar, C. C. Della Santina, T. Hirvonen, D. M. Lasker, J. P. Carey, and L. B. Minor, "Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations," J. Neurophysiol., vol. 93, pp. 2777-2786, 2005. (Pubitemid 40570856)
55. N. Davidovics, G. Y. Fridman, and C. C. Della Santina, Linearity of stimulus-response mapping during semicircular canal stimulation using a vestibular prosthesis Assoc. Res. Otolaryngol., Baltimore, MD, 2009.
56. T. P. Hirvonen, L. B. Minor, T. E. Hullar, and J. P. Carey, "Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla," J. Neurophysiol., vol. 93, pp. 643-655, 2005.
57. A. A. Migliaccio, L. Minor, and C. C. D. Santina, "The 3-Dimensional angular vestibulo-ocular reflex evoked by high-acceleration rotations in normal chinchilla is conjugate, nonlinear and isotropic," in Association for Research in Otolaryngology, Denver, CO, 2007.
58. T. E. Hullar and C. D. Williams, "Geometry of the semicircular canals of the chinchilla (Chinchilla laniger)," Hearing Res., vol. 213, pp. 17-24, 2006. (Pubitemid 43356624)
59. R. Hayden, "A model to guide electrode design for a multichannel vestibular prosthesis," in Biomedical Engineering. Baltimore, MD: Johns Hopkins Univ. Press, 2007, p. 139.
60. G. E. Grossman, R. J. Leigh, L. A. Abel, D. J. Lanska, and S. E. Thurston, "Frequency and velocity of rotational head perturbations during locomotion," Exp. Brain Res., vol. 70, pp. 470-476, 1988.
61. C. Dai, G. Y. Fridman, and C. C. Della Santina, "Effects of vestibular electrode implantation and prosthetic stimulation on hearing in rhesus monkeys," in Association for Research in Otolaryngology, Orange, CA, 2010.
62. G. M. Halmagyi, S. T. Aw, P.D. Cremer,M. J. Todd, and I. S. Curthoys, "The human vertical vestibuloocular reflex in response to high-acceleration stimulation after unilateral vestibular neurectomy," Ann. NY Acad. Sci., vol. 656, pp. 732-738, 1992.
63. S. G. Sadeghi, L. B. Minor, and K. E. Cullen, "Response of vestibularnerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy," J. Neurophysiol., vol. 97, pp. 1503-1514, 2007. (Pubitemid 46239524)
64. J. M. Goldberg, C. E. Smith, and C. Fernandez, "Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel-monkey," J. Neurophysiol., vol. 51, pp. 1236-1256, 1984. (Pubitemid 14076770)
65. C. C. Della Santina, A. A. Migliaccio, H. J. Park, I. C. W. Anderson, P. Jiradejvong, L. B. Minor, and J. P. Carey, "3-D vestibuloocular reflex, afferent responses and crista histology in chinchillas after unilateral intratympanic gentamicin," in Assoc. Res. Otolaryngol. Annu. Mtg., New Orleans, LA, 2005.
66. W. M. Grill and J. T. Mortimer, "Neural and connective tissue response to long-term implantation of multiple contact nerve cuff electrodes," J. Biomed. Materials Res., vol. 50, pp. 215-226, 2000. (Pubitemid 30126967)
67. W. K. Gstoettner, O. Adunka, P. Franz, J. Hamzavi, H. Plenk, M. Susani, W. Baumgartner, and J. Kiefer, "Perimodiolar electrodes in cochlear implant surgery," Acta Oto-Laryngologica, vol. 121, pp. 216-219, 2001. (Pubitemid 32328570)
68. J. C. Middlebrooks and R. L. Snyder, "Auditory prosthesis with a penetrating nerve array," J. Assoc. Res. Otolaryngol., vol. 8, pp. 258-279, 2007. (Pubitemid 46659320)
69. B. H. Bonham and L. M. Litvak, "Current focusing and steering: Modeling, physiology, and psychophysics," Hearing Res., vol. 242, pp. 141-153, 2008.
70. M. Scherer, A. A. Migliaccio, and M. C. Schubert, "Effect of vestibular rehabilitation on passive dynamic visual acuity," J. Vestibular Res.- Equilibrium Orientation, vol. 18, pp. 147-157, 2008.
71. M. C. Schubert, C. C. Della Santina, and M. Shelhamer, "Incremental angular vestibulo-ocular reflex adaptation to active head rotation," Exp. Brain Res., vol. 191, pp. 435-446, 2008.
72. J. M. Goldberg, "Afferent diversity and the organization of central vestibular pathways," Exp. Brain Res., vol. 130, pp. 277-297, 2000. (Pubitemid 30088269)