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, M. J. Todd

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132 Citations (Scopus)

Abstract

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°/s2) head rotation through an amplitude of 10-20° 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 (δ). 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. δ, after uVD, was significantly different from normal during ipsilesional roll and yaw impulses and during pitch-up and pitch-down impulses, δ was normal during contralesional roll and yaw impulses. At 80 ms from the onset of the impulse, δ 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 (γ), 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 γ 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 γ is equal to [G*cos (δ)], 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 γ during pitch-up impulses was reduced to the same extent as after uVD; roll-torsional γ 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, γ 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. These misalignments can be explained by activation of the direct neural connections between the vertical SCCs and the extraocular muscles. During all pitch impulses after uVD, and during pitch-up impulses after uPCO, there is excitation and reciprocal inhibition of single, instead of pairs of, vertical SCCs, producing vertical as well as contralesional torsional eye rotations. The torsional eye rotations occur because the oppositely directed torsional eye rotations arising from stimulation of pairs of vertical SCCs are no longer canceled. 8. The eye rotation axis, after uVD, deviates in the pitch plane away from the normal rostrocaudal axis toward the nasooccipital axis during ipsilesional yaw impulses. In contrast, the eye rotation axis remains well aligned with the head rotation axis during contralesional yaw impulses. We propose that the anatomic orientation of, and the direction the endolymph flow, in the remaining intact vertical SCCs can explain this misalignment. After uVD, the dominant excitation from the ipsilesional lateral SCC is absent. The relative magnitude of excitation from the intact posterior SCC is larger than that from the anterior SCC on the same side, which results in small horizontal, downward vertical, and large ipsilesional torsional eye rotations.

Original languageEnglish
Pages (from-to)4021-4030
Number of pages10
JournalJournal of Neurophysiology
Volume76
Issue number6
DOIs
Publication statusPublished - Dec 1996

Keywords

  • Adult
  • Afferent Pathways/physiology
  • Aged
  • Confidence Intervals
  • Data Interpretation, Statistical
  • Eye Movements/physiology
  • Fixation, Ocular/physiology
  • Functional Laterality/physiology
  • Head Movements/physiology
  • Humans
  • Middle Aged
  • Reflex, Vestibulo-Ocular/physiology
  • Rotation
  • Semicircular Canals/physiopathology
  • Torque
  • Vestibule, Labyrinth/physiology

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