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Reaching for an object while simultaneously rotating induces Coriolis and centrifugal inertial forces on the arm that require compensatory actions to maintain accuracy. We investigated whether the nervous system uses vestibular signals of head rotation to predict inertial forces. Human subjects reached in darkness to a remembered target 33 cm distant. Subjects were stationary, but experienced a strong vestibular rotation signal. We achieved this by rotating subjects at 360 degrees /s in yaw for 2 min and then stopping, and subjects reached during the 'post-rotary' period when the deceleration is interpreted by the vestibular system as a rotation in the opposite direction. Arm trajectories were straight in control trials without a rotary stimulus. With vestibular stimulation, trajectory curvature increased an average of 3 cm in the direction of the vestibular stimulation (e.g., to the right for a rightward yaw stimulus). Vestibular-induced curvature returned rapidly to normal, with an average time constant of 6 s. Movements also became longer as the vestibular stimulus diminished, and returned towards normal length with an average time constant of 5.6 s. In a second experiment we compared reaching with preferred and non-preferred hands, and found that they were similarly affected by vestibular stimulation. The reach curvatures were in the expected direction if the nervous system anticipated and attempted to counteract the presence of Coriolis forces based on the vestibular signals. Similarly, the shorter reaches may have occurred because the nervous system was attempting to compensate for an expected centrifugal force. Since vestibular stimulation also alters the perceived location of targets, vestibular signals probably influence all stages of the sensorimotor pathway transforming the desired goal of a reach into specific motor-unit innervation.

We describe in detail the frequency response of the human three-dimensional angular vestibulo-ocular response (3-D aVOR) over a frequency range of 0.05-1 Hz. Gain and phase of the human aVOR were determined for passive head rotations in the dark, with the rotation axis either aligned with or perpendicular to the direction of gravity (earth-vertical or earth-horizontal). In the latter case, the oscillations dynamically stimulated both the otolith organs and the semi-circular canals. We conducted experiments in pitch and yaw, and compared the results with previously-published roll data. Regardless of the axis of rotation and the orientation of the subject, the gain in aVOR increased with frequency to about 0.3 Hz, and was approximately constant from 0.3 to 1 Hz. The aVOR gain during pitch and yaw rotations was larger than during roll rotations. Otolith and canal cues combined differently depending upon the axis of rotation: for torsional and pitch rotations, aVOR gain was higher with otolith input; for yaw rotations the aVOR was not affected by otolith stimulation. There was a phase lead in all three dimensions for frequencies below 0.3 Hz when only the canals were stimulated. For roll and pitch rotations this phase lead vanished with dynamic otolith stimulation. In contrast, the horizontal phase showed no improvement with additional otolith input during yaw rotations. The lack of a significant otolith contribution to the yaw aVOR was observed when subjects were supine, prone or lying on their sides. Our results confirm studies with less-natural stimuli (off-vertical axis rotation) that the otoliths contribute a head-rotation signal to the aVOR. However, the magnitude of the contribution depends on the axis of rotation, with the gain in otolith-canal cross-coupling being smallest for yaw axis rotations. This could be because, in humans, typical yaw head movements will stimulate the otoliths to a much lesser extent then typical pitch and roll head movements.

Patients with bilateral vestibular deficits experience unsteady gait and oscillopsia that can reduce the quality of life, though many patients adapt remarkably well and lead mostly normal lives. One source of adaptation could be the ability of sensory-motor systems to compensate for the vestibular loss by adaptive enhancement of their performance. We studied smooth-pursuit eye movements in five patients and six healthy control subjects using a step-ramp paradigm. Eye movements were measured with scleral search coils. Patients showed open- and closed-loop pursuit gains that were about 9% higher than controls. We suggest that the challenge of living with a deficient vestibular system caused an enhancement in the pursuit system, which contributes to the patient's overall compensation.

We recorded three-dimensional eye movements elicited by velocity steps about axes that were tilted with respect to the earth-vertical. Subjects were accelerated in 1 s from zero to 100 degrees/s, and the axis of rotation was tilted by 15 degrees, 30 degrees, 60 degrees, or 90 degrees. This stimulus induced a constant horizontal velocity component that was directed opposite to the direction of rotation, as well as a modulation of the horizontal, vertical and torsional components with the frequency of the rotation. The maximum steady-state response in the horizontal constant-velocity component was much smaller than in other species (about 6 degrees/s), reaching a maximum at a tilt angle of about 60 degrees. While the amplitude of the horizontal modulation component increased up to a tilt angle of 90 degrees (8.4 degrees/s), the vertical and torsional modulation amplitudes saturated around 60 degrees (ca. 2.5 degrees/s). At small tilt angles, the horizontal modulation component showed a small phase lag with respect to the chair position, which turned into a small phase lead at large tilt angles. The torsional component showed a phase lead that increased with increasing tilt angle. The vertical and torsional velocity modulation at large tilt angles was not predicted by a recent model of otolith-canal interaction by Merfeld. Agreement between model and experimental data could be achieved, however, by introducing a constant force along the body's z-axis to compensate for the gravitational pull on the otoliths in the head-upright position. This approach had been suggested previously to explain the direction of the perceived subjective vertical during roll under different g-levels, and produced in our model the observed vertical and torsional modulation components at large tilt angles.

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.

The parameters characterizing Listing's plane have been determined in a group of normal subjects, and in patients who have had unilateral vestibular deafferentation on the right or left side. All patients were well compensated. There was no statistically significant difference in the orientation of Listing's plane between either of these groups: Listing's plane was approximately perpendicular to the horizontal stereotaxic plane and showed a systematic temporal tilt, i.e., it tilted right for the right eye, and left for the left eye. We also found a considerable intersubject variability in the orientation of Listing's plane. The effect of this variability on the interpretation of three-dimensional eye position and velocity data is discussed.