Journal of Neurophysiology, Vol 76, Issue 6 4021-4030, Copyright © 1996 by APS

ARTICLES

Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. II. responses in subjects with unilateral vestibular loss and selective semicircular canal occlusion

S. T. Aw, G. M. Halmagyi, T. Haslwanter, I. S. Curthoys, R. A. Yavor and M. J. Todd
Neurology Department, Royal Prince Alfred Hospital, Sydney, Camperdown, NSW, Australia.

1. We studied the three-dimensional input-output human vestibuloocular reflex (VOR) kinematics after selective loss of semicircular canal (SCC) function either through total unilateral vestibular deafferentation (uVD) or through single posterior SCC occlusion (uPCO), and showed large deficits in magnitude and direction in response to high-acceleration head rotations (head "impulses"). 2. A head impulse is a passive, unpredictable, high-acceleration (3,000-4,000 degrees/s2) head rotation through an amplitude of 10-20 degrees in roll, pitch, or yaw. The subjects were tested while seated in the upright position and focusing on a fixation target. Head and eye rotations were measured with the use of dual search coils, and were expressed as rotation vectors. A three-dimensional vector analysis was performed on the input-output VOR kinematics after uVD, to produce two indexes in the time domain: magnitude and direction. Magnitude is expressed as speed gain (G) and direction as misalignment angle (delta). 3. G. after uVD, was significantly lower than normal in both directions of head rotation during roll, pitch, and yaw impulses, and were much lower during ipsilesional than during contralesional roll and yaw impulses. At 80 ms from the onset of an impulse (i.e., near peak head velocity), G was 0.23 +/- 0.08 (SE) (ipsilesional) and 0.56 +/- 0.08 (contralesional) for roll impulses, 0.61 +/- 0.09 (up) and 0.72 +/- 0.10 (down) for pitch impulses, and 0.36 +/- 0.06 (ipsilesional) and 0.76 +/- 0.09 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). 4. delta, after uVD, was significantly different from normal during ipsilesional roll and yaw impulses and during pitch-up and pitch-down impulses. delta was normal during contralesional roll and yaw impulses. At 80 ms from the onset of the impulse, delta was 30.6 +/- 4.5 (ipsilesional) and 13.4 +/- 5.0 (contralesional) for roll impulses, 23.7 +/- 3.7 (up) and 31.6 +/- 4.4 (down) for pitch impulses, and 68.7 +/- 13.2 (ipsilesional) and 11.0 +/- 3.3 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). 5. VOR gain (gamma), after uVD, were significantly lower than normal for both directions of roll, pitch, and yaw impulses and much lower during ipsilesional than during contralesional roll and yaw impulses. At 80 ms from the onset of the head impulse, the gamma was 0.22 +/- 0.08 (ipsilesional) and 0.54 +/- 0.09 (contralesional) for roll impulses, 0.55 +/- 0.09 (up) and 0.61 +/- 0.09 (down) for pitch impulses, and 0.14 +/- 0.10 (ipsilesional) and 0.74 +/- 0.06 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). Because gamma is equal to [G*cos (delta)], it is significantly different from its corresponding G during ipsilesional roll and yaw, and during all pitch impulses, but not during contralesional roll and yaw impulses. 6. After uPCO, pitch-vertical gamma during pitch-up impulses was reduced to the same extent as after uVD; roll-torsional gamma during ipsilesional roll impulses was significantly lower than normal but significantly higher than after uVD. At 80 ms from the onset of the head impulse, gamma was 0.32 +/- 0.13 (ipsilesional) and 0.55 +/- 0.16 (contralesional) for roll impulses, 0.51 +/- 0.12 (up) and 0.91 +/- 0.14 (down) for pitch impulses, and 0.76 +/- 0.06 (ipsilesional) and 0.73 +/- 0.09 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). 7. The eye rotation axis, after uVD, deviates in the yaw plane, away from the normal interaural axis, toward the nasooccipital axis, during all pitch impulses. After uPCO, the eye rotation axis deviates in same direction as after uVD during pitch-up impulses, but is well aligned with the head rotation axis during pitch-down impulses.

This article has been cited by other articles:

				K. P. Weber, S. T. Aw, M. J. Todd, L. A. McGarvie, I. S. Curthoys, and G. M. Halmagyi Head impulse test in unilateral vestibular loss: Vestibulo-ocular reflex and catch-up saccades Neurology, February 5, 2008; 70(6): 454 - 463. [Abstract] [Full Text] [PDF]

				B. T. Crane, J. Tian, A. Ishiyama, and J. L. Demer Unilateral Deafferentation and Eye Position Misdirect the Initial Vestibulo-ocular Reflex: A Model-Based Study Invest. Ophthalmol. Vis. Sci., December 1, 2007; 48(12): 5512 - 5522. [Abstract] [Full Text] [PDF]

				M. F. Walker and D. S. Zee Cerebellar Disease Alters the Axis of the High-Acceleration Vestibuloocular Reflex J Neurophysiol, November 1, 2005; 94(5): 3417 - 3429. [Abstract] [Full Text] [PDF]

				R. A. Black, G. M. Halmagyi, M. J. Thurtell, M. J. Todd, and I. S. Curthoys The Active Head-Impulse Test in Unilateral Peripheral Vestibulopathy Arch Neurol, February 1, 2005; 62(2): 290 - 293. [Abstract] [Full Text] [PDF]

				G. C. Y. Peng, D. S. Zee, and L. B. Minor Phase-Plane Analysis of Gaze Stabilization to High Acceleration Head Thrusts: A Continuum Across Normal Subjects and Patients With Loss of Vestibular Function J Neurophysiol, April 1, 2004; 91(4): 1763 - 1781. [Abstract] [Full Text] [PDF]

				C R Gordon, V Joffe, G Vainstein, and N Gadoth Vestibulo-ocular arreflexia in families with spinocerebellar ataxia type 3 (Machado-Joseph disease) J. Neurol. Neurosurg. Psychiatry, October 1, 2003; 74(10): 1403 - 1406. [Abstract] [Full Text] [PDF]

				M Strupp, S Glasauer, E Schneider, T Eggert, M Glaser, K Jahn, and T Brandt Anterior canal failure: ocular torsion without perceptual tilt due to preserved otolith function J. Neurol. Neurosurg. Psychiatry, September 1, 2003; 74(9): 1336 - 1338. [Abstract] [Full Text] [PDF]

				T. Pansell, H. D. Schworm, and J. Ygge Torsional and Vertical Eye Movements during Head Tilt Dynamic Characteristics Invest. Ophthalmol. Vis. Sci., July 1, 2003; 44(7): 2986 - 2990. [Abstract] [Full Text] [PDF]

				M. Karlberg, S. T. Aw, R. A. Black, M. J. Todd, H. G. MacDougall, and G. M. Halmagyi Vibration-induced ocular torsion and nystagmus after unilateral vestibular deafferentation Brain, April 1, 2003; 126(4): 956 - 964. [Abstract] [Full Text] [PDF]

				S. T. Aw, M. J. Todd, L. A. McGarvie, A. A. Migliaccio, and G. M. Halmagyi Effects of Unilateral Vestibular Deafferentation on the Linear Vestibulo-Ocular Reflex Evoked by Impulsive Eccentric Roll Rotation J Neurophysiol, February 1, 2003; 89(2): 969 - 978. [Abstract] [Full Text] [PDF]

				C. C. Della Santina, P. D. Cremer, J. P. Carey, and L. B. Minor Comparison of Head Thrust Test With Head Autorotation Test Reveals That the Vestibulo-ocular Reflex Is Enhanced During Voluntary Head Movements Arch Otolaryngol Head Neck Surg, September 1, 2002; 128(9): 1044 - 1054. [Abstract] [Full Text] [PDF]

				M. Karlberg, S. T. Aw, G. M. Halmagyi, and R. A. Black Vibration-Induced Shift of the Subjective Visual Horizontal: A Sign of Unilateral Vestibular Deficit Arch Otolaryngol Head Neck Surg, January 1, 2002; 128(1): 21 - 27. [Abstract] [Full Text] [PDF]

				S. T. Aw, M. Fetter, P. D. Cremer, M. Karlberg, and G. M. Halmagyi Individual semicircular canal function in superior and inferior vestibular neuritis Neurology, September 11, 2001; 57(5): 768 - 774. [Abstract] [Full Text] [PDF]

				T. D. Fife, R. J. Tusa, J. M. Furman, D. S. Zee, E. Frohman, R. W. Baloh, T. Hain, J. Goebel, J. Demer, and L. Eviatar Assessment: Vestibular testing techniques in adults and children: Report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology Neurology, November 28, 2000; 55(10): 1431 - 1441. [Full Text] [PDF]

				D. M. Lasker, T. E. Hullar, and L. B. Minor Horizontal Vestibuloocular Reflex Evoked by High-Acceleration Rotations in the Squirrel Monkey. III. Responses After Labyrinthectomy J Neurophysiol, May 1, 2000; 83(5): 2482 - 2496. [Abstract] [Full Text] [PDF]

				J. S. Stahl, L. Averbuch-Heller, and R. J. Leigh Acquired Nystagmus Arch Ophthalmol, April 1, 2000; 118(4): 544 - 549. [Abstract] [Full Text] [PDF]

				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, October 1, 1999; 82(4): 2000 - 2005. [Abstract] [Full Text] [PDF]

				D. M. Lasker, D. D. Backous, A. Lysakowski, G. L. Davis, and L. B. Minor Horizontal Vestibuloocular Reflex Evoked by High-Acceleration Rotations in the Squirrel Monkey. II. Responses After Canal Plugging J Neurophysiol, September 1, 1999; 82(3): 1271 - 1285. [Abstract] [Full Text] [PDF]

				R. D. Rabbitt, R. Boyle, and S. M. Highstein Influence of Surgical Plugging on Horizontal Semicircular Canal Mechanics and Afferent Response Dynamics J Neurophysiol, August 1, 1999; 82(2): 1033 - 1053. [Abstract] [Full Text] [PDF]

				S. B. Yakushin, T. Raphan, J.-I. Suzuki, Y. Arai, and B. Cohen Dynamics and Kinematics of the Angular Vestibulo-Ocular Reflex in Monkey: Effects of Canal Plugging J Neurophysiol, December 1, 1998; 80(6): 3077 - 3099. [Abstract] [Full Text] [PDF]