Ross A. Black

The Human Horizontal Vestibulo-Ocular Reflex in Response to Active and Passive Head Impulses after Unilateral Vestibular Deafferentation

We studied the compensatory eye movements made by subjects with unilateral vestibular deficits in response to passive (unpredictable, manually generated) and active (predictable, self‐generated) head impulses. A typical head impulse is a brief, low‐amplitude (15‐20°), high‐velocity (150‐350°/s), high‐acceleration (4000‐6000°/s2), yaw head‐on‐trunk rotation. In the initial 75 ms of the response, the vestibulo‐ocular reflex gain was significantly higher during active head impulses to both ipsilesional and contralesional sides, than during passive impulses. Mean gains were 0.15 (ipsilesional passive), 0.44 (ipsilesional active), 0.5 (contralesional passive), and 0.76 (contralesional active). Differences between active and passive head impulses were present from near the onset of head rotation. The mechanism for producing this behavior is unclear, but the findings could be related to enhanced sensitivity of second‐order neurons during active head impulses. However, even with active movements, there is still a large and statistically significant asymmetry in the eye‐movement responses for ipsilesional as opposed to contralesional head rotations. After 75 ms, rapid corrective eye movements often were generated to reduce any remaining gaze error.

Otolith-semicircular canal interaction during postrotatory nystagmus in humans

The otolith-semicircular canal interaction during postrotatory nystagmus was studied in ten normal human subjects by applying fast, short-lasting, passive head and body tilts (15, 30, 45, or 90° in the roll or pitch plane) 2 s after sudden stop from a constant-velocity rotation (100°/s) about the earth-vertical axis in yaw. Eye movements were measured with three-dimensional magnetic search coils. Following the head tilt, activity in the semicircular canal primary afferents continues to reflect the postrotatory angular velocity vector in head-centered coordinates, whereas otolith primary afferents signal a different orientation of the head relative to gravity. Despite the change in head orientation relative to gravity, postrotatory eye velocity decayed closely along the axis of semicircular canal stimulation (horizontal in head coordinates) for large head tilts (90°) and also for small head tilts (15–45°) for reorientations in the pitch plane. Only for small head tilts (15–45°) in the roll plane was there a reorientation of the eye rotation axis toward the gravitational vector. This reorientation was approximately compensatory for 15° head tilts. For 30° and 45° head tilts the eye rotation axis tilted toward the gravitational vector by about the same amount as for 15° head tilts. These results suggest that, with the exception of small head tilts in the roll plane, there was no compelling data showing a relationship between the eye rotation axis and head tilt and that postrotatory nystagmus is largely organized in head-centered rather than gravity-centered coordinates in humans. This indicates a rudimentary, nonlinear, and direction-specific interaction of semicircular canal and otolith signals in the central vestibular system in humans.

Orientation of Listing's plane in normals and in patients with unilateral vestibular deafferentation.

The parameters characterizing Listings 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 Listings plane between either of these groups: Listings 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 Listings plane. The effect of this variability on the interpretation of three-dimensional eye position and velocity data is discussed.

Off-center yaw rotation: effect of naso-occipital linear acceleration on the nystagmus response of normal human subjects and patients after unilateral vestibular loss.

Abstract Dual search coils were used to record horizontal, vertical and torsional eye movement components of one eye during nystagmus caused by off-center yaw rotation (yaw centrifugation). Both normal healthy human subjects (n=7) and patients with only one functioning labyrinth (n=12) were studied in order to clarify how the concomitant linear acceleration affected the nystagmus response. Each subject was seated with head erect on the arm of a fixed-chair human centrifuge, 1 m away from the center of the rotation, and positioned to be facing along a radius; either towards (facing-in) or away from (facing-out) the center of rotation. Both yaw right and yaw left angular accelerations of 10°s–2 from 0 to 200°/s were studied. During rotation a centripetal linear acceleration (increasing from 0 to 1.24×g units) was directed along the subject’s naso-occipital axis resulting in a shift of the resultant angle of the gravitoinertial acceleration (GIA) of 51° in the subject’s pitch plane and an increase in the total GIA magnitude from 1.0 to 1.59×g. In normal subjects during the angular acceleration off-center there were, in addition to the horizontal eye velocity components, torsional and vertical eye velocities present. The magnitude of these additional components, although small, was larger than observed during similar experiments with on-center angular acceleration (Haslwanter et al. 1996), and the change in these components is attributed to the additional effect of the linear acceleration stimulation. In the pitch plane the average size of the shift of the axis of eye velocity (AEV) during the acceleration was about 8° for a 51° shift of the GIA (around 16% of the GIA shift) so that the AEV-GIA alignment was inadequate. There was a very marked difference in the size of the AEV shift depending on whether the person was facing-in [AEV shift forward (i.e. non-compensatory) of about 4°] or facing-out [AEV shift forward (i.e. compensatory) of around 12°]. The linear acceleration decreased the time constant of decay of the horizontal component of the post-rotatory nystagmus: from an average of 24.8°/s facing-in to an average of 11.3°/s facing-out. The linear acceleration dumps torsional eye velocity in an manner analogous to, but independent of, the dumping of horizontal eye velocity. Patients with UVD had dramatically reduced torsional eye velocities for both facing-in and facing-out headings, and there was little if any shift of the AEV in UVD patients. The relatively small effects of linear acceleration on human canal-induced nystagmus found here confirms other recent studies in humans (Fetter et al. 1996) in contrast to evidence from monkeys and emphasizes the large and important differences between humans and monkeys in otolith-canal interaction. Our results confirm the vestibular control of the axis of eye velocity of humans is essentially head-referenced whereas in monkeys that control is essentially space-referenced.

Unilateral vestibular deafferentation produces no long-term effects on human active eye-head coordination

Abstract We tested the hypothesis that the reason some patients compensate well after unilateral vestibular deafferentation (uVD) and others do not could be due to differences in eye-head coordination or in blink characteristics during natural, active head movements. Patients with well-compensated uVDs do not report distressing postural unsteadiness or an aversive sensation of apparent motion of a visual scene (oscillopsia) or ”visual confusion” upon rapid head rotation as do those patients with poorly compensated uVDs. It has been suggested that well-compensated subjects eliminate the subjective sensations associated with retinal slip, which must occur as a result of an inadequate vestibuloocular reflex (VOR), either by restricting head movement to the lesioned side or by blinking during head turns. To test this, subjects stood at the curbside of a busy road with a 180o view of regular, fast-moving traffic, which they scanned in preparation of crossing the road, and their eye and head movements and blinks were measured in this natural situation. Both normals and uVDs generated similar ranges of head position, head velocity and gaze magnitude, and all subjects performed a blink during the gaze saccade. Contrary to the hypothesis, no systematic differences were found between normals and either group of uVDs.

The three-dimensional human vestibulo-ocular reflex: response to long-duration yaw angular accelerations

We recorded three-dimensional eye movements during angular acceleration steps from 0 to 250°/s at 20°/s2 about an earth-vertical axis. Experiments were performed on 27 normal subjects and on 19 patients who had recovered well from unilateral vestibular deafferentation on the right or left side. In addition to compensatory horizontal eye movements, significant vertical and torsional eye movement components were elicited. These vertical and torsional eye velocity traces led to a shift of the axis of eye velocity away from the axis of head velocity. Horizontal, vertical, and torsional velocity components showed clear differences between normals and patients with unilateral vestibular deafferentation. In normals, the axis of eye velocity tilted backward and slightly away from the axis of head velocity. Patients showed similar, but more pronounced, shifts during rotations toward the intact ear and shifts in the opposite direction for rotations toward the operated ear. Eye velocity traces were analyzed with special consideration given to the orientation of the axis of eye velocity. We speculate that the vertical and torsional velocity components may be due to the effects of Listings plane, as well as the contributions of the otolith signals.

On-road assessment of driving performance in bilateral vestibular-deficient patients.

This study measured on‐road driving behavior in subjects with bilateral vestibular loss (BVL). Data included point‐of‐regard (what the driver is looking at and attending to), gaze stability (the performance of the vestibulo‐ocular reflex), and head movement, during complex maneuvers such as changing lanes, cornering, pulling into traffic, and parking. Subjective and objective measures showed few differences between BVL subjects and age‐matched controls, and that it is possible to drive well with little or no peripheral vestibular function. This has important implications for driver licensing, road‐safety policy, and for the potential successful rehabilitation of vestibular patients. Patients with unilateral vestibular dysfunction may have more difficulty driving than their bilateral counterparts.

Three-dimensional kinematics of saccadic eye movements in humans with cerebellar degeneration.

During saccades, the orientation of the eye velocity axis varies depending on the instantaneous eye position. The means by which this eye velocity axis tilting arises remains contentious. Some have argued that muscle pulleys in the orbit implement the tilts, since they cause the pulling directions of the extraocular muscles to change in a manner that depends on instantaneous eye position. Others have suggested that the tilting is centrally programmed. In the current study, three-dimensional eye and head rotation data were acquired, using the magnetic search coil technique, to confirm the presence of eye position-dependent eye velocity axis tilting during saccades. We studied normal humans and humans with inherited or sporadic cerebellar degeneration. While the humans with cerebellar degeneration were noted to have abnormalities in the two-dimensional metrics and consistency of their saccades, the eye velocity axis tilts were similar to those observed in the normal subjects. Our findings suggest that the cerebellum does not encode eye velocity axis tilting during saccades, further supporting the notion that these phenomena arise due to the effects of muscle pulleys.

Torsional Eye Velocity Components During Yaw Angular Acceleration Identify the Side of Unilateral Vestibular Deafferentation

Using dual torsion scleral search coils we have recorded 3-dimensional eye position during yaw angular accelerations of 20 degrees/s2 about an earth vertical axis in healthy subjects and in patients with unilateral vestibular deafferentation (UVD). These experiments produced two interesting results: i) even in healthy subjects, the axis of eye velocity did not coincide with the (earth vertical) stimulus axis during centred rotation; ii) Patients with UVD had torsional eye velocity components that were systematically different from those in normal subjects. While in normals the direction of the torsional component of the eye velocity depended on the direction of rotation and was on average approximately symmetric for CW and CCW yaw rotation, there was a clear asymmetry in patients, which was distinctly different for left and right UVD.