Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents

Journal of Neurophysiology

Volumn 103, Issue 2, 2010, Pages 1066-1079

  Lewis, Richard F ^a,b   Haburcakova, Csilla ^a   Gong, Wangsong ^a   Makary, Chadi ^a   Merfeld, Daniel M ^a  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; ELECTRODE; ELECTROSTIMULATION; EYE MOVEMENT; HEAD; HEAD MOVEMENT; MALE; MOTION; NONHUMAN; PRIORITY JOURNAL; SEMICIRCULAR CANAL; SQUIRREL MONKEY; VESTIBULAR STIMULATION; VESTIBULOOCULAR REFLEX; VISUAL ADAPTATION; VISUAL STIMULATION;

ADAPTATION, PHYSIOLOGICAL; AFFERENT PATHWAYS; ANIMALS; ELECTRIC STIMULATION; HEAD MOVEMENTS; MALE; NEURONAL PLASTICITY; REFLEX, VESTIBULO-OCULAR; SAIMIRI; SEMICIRCULAR CANALS;

EID: 76649127047     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00241.2009     Document Type: Article

References (45)

1. Agrawal Y, Carey JP, Della Santina CC, Schubert MC, Minor LB. Disorders of balance and vestibular function in US adults: data from the National Health and Nutritional Examination Survey, 2001-2004. Arch Intern Med 169: 938-944, 2009.
2. Angelaki DE, Hess BJM, Arai Y, Suzuki J-I. Adaptation of primate vestibuloocular reflex to altered peripheral vestibular inputs. I. Frequency-specific recovery of horizontal VOR after inactivation of the lateral semicircular canals. J Neurophysiol 76: 2941-2953, 1996.
3. Bergquist F, Ludwid M, Dutia MB. Role of commissural inhibitory system in vestibular compensation in the rat. J Physiol 586: 4441-4452, 2008.
4. Blanks RH, Curthoys IS, Bennett ML, Markham CH. Planar relationship of the semicircular canals in rhesus and squirrel monkeys. Brain Res 340: 315-324, 1985.
5. Broussard DM, Bhatia JK, Jones GEG. The dynamics of the vestibuloocular reflex after peripheral vestibular damage. I. Frequency-dependent asymmetry. Exp Brain Res 125: 353-364, 1999.
6. Broussard DM, Bronte-Stewart HM, Lisberger SG. Expression of motor learning in the response of the primate vestibuloocular reflex pathway to electrical stimulation. J Neurophysiol 67: 1493-1508, 1992.
7. Broussard DM, Hong JA. The response of vestibulo-ocular reflex pathways to electrical stimulation after canal plugging. Exp Brain Res 149: 237-248, 2003.
8. Capocchi G, Della Torre G, Grassi S, Pettorossi VE, Zampolini M. NMDA receptor-mediated long term modulation of electrically evoked field potentials in the rat medial vestibular nuclei. Exp Brain Res 90: 546-550, 1992.
9. Courjon JH, Precht W, Sirkin DW. Vestibular nerve and nuclei unit responses and eye movement responses to repetitive galvanic stimulation of the labyrinth in the rat. Exp Brain Res 66: 41-48, 1987.
10. Demer J, Porter F, Goldberg J, Jenkins H, Schmidt K. Adaptation to telescopic spectacles: vestibulo-ocular reflex plasticity. Invest Ophthalmol Vis Sci 30: 159-170, 1989.
11. Dieringer N. "Vestibular compensation": Neural plasticity and its relations to functional recovery after labyrinthine lesions in frogs and other vertebrates. Prog Neurobiol 46: 97-129, 1995.
12. Dimitri PS, Wall C 3rd, Oas JG. Classification of human rotation test results using parametric modeling and multivariate statistics. Acta Otolaryngol 116: 497-506, 1996.
13. Dimitri PS, Wall C 3rd, Rauch SD. Multivariate vestibular testing: thresholds for bilateral Ménière's disease and aminoglycoside ototoxicity. J Vestib Res 11: 391-404, 2001/2002.
14. Fernandez C, Goldberg J. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34: 661-675, 1971.
15. Fetter M, Zee DS. Recovery from unilateral labyrinthectomy in rhesus monkey. J Neurophysiol 59: 370-393, 1988.
16. Furman JM, Becker JT. Vestibular responses in Wernicke's encephalopathy. Ann Neurol 26: 669-674, 1989.
17. Goldberg JM, Fernandez C. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34: 635-660, 1971.
18. Goldberg JM, Smith CE, Fernandez C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of squirrel monkey. J Neurophysiol 51: 1236-1256, 1984.
19. Gong W, Merfeld DM. Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Eng 28: 572-581, 2000.
20. Gong W, Merfeld DM. System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans Biomed Eng 49: 175-181, 2002.
21. Hess BJM, Lysakowski A, Minor LB, Angelaki DE. Central versus peripheral origin of vestibulo-ocular reflex recovery following semicircular canal plugging in rhesus monkeys. J Neurophysiol 84: 3078-3082, 2000.
22. Jeannerod M, Magnin M, Schmid R, Stefanelli M. Vestibular habituation to angular velocity step in the cat. Biol Cybern 22: 39-48, 1976.
23. Judge SJ, Richmond BJ, Chu FC. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20: 535-538, 1980.
24. Kawaato M, Gomi H. The cerebellum and VOR/OKR learning models. Trends Neurosci 15: 445-453, 1992.
25. Kramer PD, Shelhamer M, Zee DS. Short-term adaptation of the phase of the vestibulo-ocular reflex (VOR) in normal human subjects. Exp Brain Res 106: 318-326, 1995.
26. Lewis RF, Gong W, Ramsey M, Minor L, Boyle R, Merfeld DM. Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res 12: 87-94, 2003/2004.
27. Lewis RF, Haburcakova C, Gong W, Merfeld DM. Effects of semicircular canal activation on perceived head orientation. ARO Abstr 1107, 2006.
28. Li PM, Somdas MA, Eddington DK, Nadol JR Jr. Analysis of intracochlear new bond and fibrous tissue formation in human subjects with cochlear implants. Ann Otol Rhinol Laryngol 116: 731-738, 2007.
29. Lisberger SG, Miles FA, Optican LM. Frequency-selective adaptation: evidence for channels in the vestibulo-ocular reflex? J Neurosci 3: 1234-1244, 1983.
30. Merfeld DM, Gong W, Morrissey J, Saginaw M, Haburcakova C, Lewis RF. Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng 53: 2362-2372, 2006.
31. Merfeld DM, Haburcakova C, Gong W, Lewis RF. Chronic vestibuloocular reflexes evoked by a vestibular prosthesis. IEEE Trans Biomed Eng 54: 1005-1015, 2007.
32. Miles FA, Eighmy BB. Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. J Neurophysiol 43: 1406-1425, 1980.
33. Minor LB, Goldberg JM. Vestibular-nerve inputs to the vestibule-ocular reflex: a functional-ablation study in the squirrel monkey. J Neurosci 11: 1636-1648, 1991.
34. O'Leary MJ, Fayad J, House WF, Linthicum FH Jr. Electrode insertion trauma in cochlear implantation. Ann Otol Rhinol Laryngol 100: 695-699, 1991.
35. Paige GD. Vestibuloocular reflex and its interactions with visual following mechanisms in the squirrel monkey. II. Response characteristics and plasticity following unilateral inactivation of horizontal canal. J Neurophysiol 49: 152-168, 1983.
36. Paige GD. Senescence of human visual-vestibular interactions. 1. Vestibuloocular reflex and adaptive plasticity with aging. J Vestib Res 2: 131-151, 1992.
37. Quinn KJ, Helminski JO, Didier AJ, Baker JF, Peterson BW. Changes in sensitivity of vestibular nucleus neurons induced by cross-axis adaptation of the vestibulo-ocular reflex in the cat. Brain Res 718: 176-180, 1996.
38. Rabbitt RD, Boyle R, Highstein SM. Influence of surgical plugging on horizontal semicircular canal mechanics and afferent response dynamics. J Neurophysiol 82: 1033-1053, 1999.
39. Ris L, de Waele C, Serafin M, Vidal P-P, Godaux E. Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea-pig. J Neurophysiol 74: 2087-2099, 1995.
40. Ris L, Godaux E. Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 80: 2352-2367, 1998.
41. Robblee LS, Rose TL. Electrochemical guidelines for selection of protocols and electrode materials for neural stimulation. In: Neural Prostheses: Fundamental Studies, edited by Agnew WF, McCreery DB. Englewood Cliffs, NJ: Prentice Hall, 1990, p. 25-66.
42. Sadeghi SG, Minor LB, Cullen KE. Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. J Neurophysiol 97: 1503-1514, 2007.
43. Shepard RK, Clark GM. Effect of high electrical stimulus intensities on the auditory nerve suing brain stem response audiometry. Ann Otol Rhinol Laryngol 96, Suppl. 128: 50-52, 1987.
44. Tykocinski M, Shepard RK, Clark G. Reduction in excitability of the auditory nerve following electrical stimulation at high stimulus rates. Hear Res 88: 124-142, 1995.
45. Vidal P-P, De Waele C, Vibert N, Muhlethaler M. Vestibular compensation revisted. Otolaryngol Hean Neck Surg 119: 34-42, 1998.