3-DIMENSIONAL VECTOR ANALYSIS OF THE HUMAN VESTIBULOOCULAR REFLEX IN RESPONSE TO HIGH-ACCELERATION HEAD ROTATIONS .2. RESPONSES IN SUBJECTSWITH UNILATERAL VESTIBULAR LOSS AND SELECTIVE SEMICIRCULAR CANAL OCCLUSION

1. We studied the three-dimensional input-output human vestibuloocular reflex (VOR) kinematics after selective loss of semicircular canal (S CC) function either through total unilateral vestibular deafferentatio n (uVD) or through single posterior SCC occlusion (uPCO), and showed l arge deficits in magnitude and direction in response to high-accelerat ion head rotations (head ''impulses''). 2. A head impulse is a passive , unpredictable, high-acceleration (3,000-4,000 degrees/s(2)) head rot ation through an amplitude of 10-20 degrees in roll, pitch, or yaw. Th e subjects were tested while seated in the upright position and focusi ng on a fixation target. Head and eye rotations were measured with the use of dual search coils, and were expressed as rotation vectors. A t hree-dimensional vector analysis was performed on the input-output VOR kinematics after uVD, to produce two indexes in the time domain: magn itude and direction. Magnitude is expressed as speed gain (G) and dire ction as misalignment angle (delta). 3. G, after uVD, was significantl y lower than normal in both directions of head rotation during roll, p itch and yaw impulses, and were much lower during ipsilesional than du ring 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 im pulses (mean +/- 95% confidence intervals). 4. delta, after uVD, was s ignificantly different from normal during ipsilesional roll and yaw im pulses and during pitch-up and pitch-down impulses. delta was normal d uring 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 inte rvals). 5. VOR gain (gamma), after uVD, were significantly lower than normal for both directions of roll, pitch, and yaw impulses and much l ower during ipsilesional than during contralesional roll and yaw impul ses. 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 imp ulses, 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) f or yaw impulses (mean +/- 95% confidence intervals). Because gamma is equal to [Gcos (delta)], it is significantly different from its corre sponding G during ipsilesional roll and yaw, and during all pitch impu lses, but not during contralesional roll and yaw impulses. 6. After uP CO, pitch-vertical gamma during pitch-up impulses was reduced to the s ame 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 wa s 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 i mpulses, and 0.76 +/- 0.06 (ipsile sional) and 0.73 +/- 0.09 (contrale sional) for yaw impulses (mean +/- 95% confidence intervals). 7. The e ye rotation axis, after uVD, deviates in the yaw plane, away from the normal interaural axis, toward the nasooccipital axis, during all pitc h impulses. After uPCO, the eye rotation axis deviates in same directi on as after uVD during pitch-up impulses, but is well aligned with the head rotation axis during pitch-down impulses. These misalignments ca n be explained by activation of the direct neural connections between the vertical SCCs and the extraocular muscles. During all pitch impuls es after uVD, and during pitch-up impulses after uPCO, there is excita tion and reciprocal inhibition of single, instead of pairs of, vertica l SCCs, producing vertical as well as contralesional torsional eye rot ations. The torsional eye rotations occur because the oppositely direc ted torsional eye rotations arising from stimulation of pairs of verti cal SCCs are no longer canceled. 8. The eye rotation axis, after uVD, deviates in the pitch plane away from the normal rostrocaudal axis tow ard the nasooccipital axis during ipsilesional yaw impulses. In contra st, 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 do minant excitation from the ipsilesional lateral SCC is absent. The rel ative magnitude of excitation from the intact posterior SCC is larger than that from the anterior SCC on the same side, which results in sma ll horizontal, downward vertical, and large ipsilesional torsional eye rotations.