Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects

1996 ◽  
Vol 76 (6) ◽  
pp. 4009-4020 ◽  
Author(s):  
S. T. Aw ◽  
T. Haslwanter ◽  
G. M. Halmagyi ◽  
I. S. Curthoys ◽  
R. A. Yavor ◽  
...  

1. The kinematics of the human angular vestibuloocular reflex (VOR) in three dimensions was investigated in 12 normal subjects during high-acceleration head rotations (head “impulses”). A head impulse is a passive, unpredictable, high-acceleration (3,000–4,000 degrees/s2) head rotation of approximately 10–20 degrees in roll, pitch, or yaw, delivered with the subject in the upright position and focusing on a fixation target. Head and eye rotations were measured with dual search coils and expressed as rotation vectors. The first of these two papers describes a vector analysis of the three-dimensional input-output kinematics of the VOR as two indexes in the time domain: magnitude and direction. 2. Magnitude is expressed as speed gain (G) and direction as misalignment angle (delta). G is defined as the ratio of eye velocity magnitude (eye speed) to head velocity magnitude (head speed). delta is defined as the instantaneous angle by which the eye rotation axis deviates from perfect alignment with the head rotation axis in three dimensions. When the eye rotation axis aligns perfectly with the head rotation axis and when eye velocity is in a direction opposite to head velocity, delta = 0. The orientation of misalignment between the head and the eye rotation axes is characterized by two spatial misalignment angles, which are the projections of delta onto two orthogonal coordinate planes that intersect at the head rotation axis. 3. Time series of G were calculated for head impulses in roll, pitch, and yaw. At 80 ms after the onset of an impulse (i.e., near peak head velocity), values of G were 0.72 +/- 0.07 (counterclockwise) and 0.75 +/- 0.07 (clockwise) for roll impulses, 0.97 +/- 0.05 (up) and 1.10 +/- 0.09 (down) for pitch impulses, and 0.95 +/- 0.06 (right) and 1.01 +/- 0.07 (left) for yaw impulses (mean +/- 95% confidence intervals). 4. The eye rotation axis was well aligned with head rotation axis during roll, pitch, and yaw impulses: delta remained almost constant at approximately 5–10 degrees, so that the spatial misalignment angles were < or = 5 degrees. delta was 9.6 +/- 3.1 (counterclockwise) and 9.0 +/- 2.6 (clockwise) for roll impulses, 5.7 +/- 1.6 (up) and 6.1 +/- 1.9 (down) for pitch impulses, and 6.2 +/- 2.2 (right) and 7.9 +/- 1.5 (left) for yaw impulses (mean +/- 95% confidence intervals). 5. VOR gain (gamma) is the product of G and cos(delta). Because delta is small in normal subjects, gamma is not significantly different from G. At 80 ms after the onset of an impulse, gamma was 0.70 +/- 0.08 (counterclockwise) and 0.74 +/- 0.07 (clockwise) for roll impulses, 0.97 +/- 0.05 (up) and 1.09 +/- 0.09 (down) for pitch impulses, and 0.94 +/- 0.06 (right) and 1.00 +/- 0.07 (left) for yaw impulses (mean +/- 95% confidence intervals). 6. VOR latencies, estimated with a latency shift method, were 10.3 +/- 1.9 (SD) ms for roll impulses, 7.6 +/- 2.8 (SD) ms for pitch impulses, and 7.5 +/- 2.9 (SD) ms for yaw impulses. 7. We conclude that the normal VOR produces eye rotations that are almost perfectly compensatory in direction as well as in speed, but only during yaw and pitch impulses. During roll impulses, eye rotations are well aligned in direction, but are approximately 30% slower in speed.

1996 ◽  
Vol 76 (6) ◽  
pp. 4021-4030 ◽  
Author(s):  
S. T. Aw ◽  
G. M. Halmagyi ◽  
T. Haslwanter ◽  
I. S. Curthoys ◽  
R. A. Yavor ◽  
...  

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.


2007 ◽  
Vol 98 (1) ◽  
pp. 295-302 ◽  
Author(s):  
Mark F. Walker ◽  
Jing Tian ◽  
David S. Zee

We studied the effect of cerebellar lesions on the 3-D control of the rotational vestibuloocular reflex (RVOR) to abrupt yaw-axis head rotation. Using search coils, three-dimensional (3-D) eye movements were recorded from nine patients with cerebellar disease and seven normal subjects during brief chair rotations (200°/s2 to 40°/s) and manual head impulses. We determined the amount of eye-position dependent torsion during yaw-axis rotation by calculating the torsional-horizontal eye-velocity axis for each of three vertical eye positions (0°, ±15°) and performing a linear regression to determine the relationship of the 3-D velocity axis to vertical eye position. The slope of this regression is the tilt angle slope. Overall, cerebellar patients showed a clear increase in the tilt angle slope for both chair rotations and head impulses. For chair rotations, the effect was not seen at the onset of head rotation when both patients and normal subjects had nearly head-fixed responses (no eye-position-dependent torsion). Over time, however, both groups showed an increasing tilt-angle slope but to a much greater degree in cerebellar patients. Two important conclusions emerge from these findings: the axis of eye rotation at the onset of head rotation is set to a value close to head-fixed (i.e., optimal for gaze stabilization during head rotation), independent of the cerebellum and once the head rotation is in progress, the cerebellum plays a crucial role in keeping the axis of eye rotation about halfway between head-fixed and that required for Listing's Law to be obeyed.


1994 ◽  
Vol 72 (5) ◽  
pp. 2467-2479 ◽  
Author(s):  
D. Tweed ◽  
D. Sievering ◽  
H. Misslisch ◽  
M. Fetter ◽  
D. Zee ◽  
...  

1. This series of three papers aims to describe the three-dimensional, kinematic input-output relations of the rotational vestibuloocular reflex (VOR) in humans, and to identify the functional advantages of these relations. In this first paper the response to sinusoidal rotation in darkness at 0.3 Hz, maximum speed 37.5%/s, was quantified by the use of the three-dimensional analogue of VOR gain: a 3 x 3 matrix where each element describes the dependence of one component (torsional, vertical, or horizontal) of eye velocity on one component of head velocity. 2. The three matrix elements indicating collinear gains (i.e., dependence of torsional eye velocity on torsional head velocity, vertical on vertical, and horizontal on horizontal) were smaller than the -1's required for optimal retinal image stabilization. Of these three the torsional gain was weakest: -0.37 for rotation about an earth-vertical axis, versus -0.73 and -0.64 for vertical and horizontal gains. Matrix elements indicating cross talk were mostly negligible. There was a tendency to leftward eye rotation in response to clockwise head motion, but this was not statistically significant. 3. VOR responses were compared for rotation about earth-vertical and earth-horizontal axes. The varying otolith input due to the rotation of the gravity vector relative to the head during earth-horizontal axis rotation made no difference to the collinear gains. 4. There were no consistent phase leads or lags except for a torsional phase lead of up to 10 degrees, usually more marked for clock-wise head rotation versus counterclockwise, and for oblique axis rotations versus purely torsional. 5. Torsional gain was magnified, averaging -0.52, when the torsional component of head rotation was only a small part of a predominantly vertical or horizontal rotation, i.e., when the axis of head rotation was near the frontal plane. Because most natural head rotations occur about such axes, the torsional VOR is probably somewhat stronger than the response to pure torsion would suggest. 6. The speed of eye rotation in response to a given stimulus varied widely among subjects, but the direction of rotation was much more uniform. For head rotations about oblique axes out of the frontal plane, there was a systematic misalignment of eye and head axes, with eye axes tilted toward the frontal plane. These findings can be explained on the basis of a strategy where the VOR balances the muscular effort of rotating the eyes against the cost of retinal slip.


1999 ◽  
Vol 9 (3) ◽  
pp. 173-180
Author(s):  
S.T. Aw ◽  
G.M. Halmagyi ◽  
R.A. Black ◽  
I.S. Curthoys ◽  
R.A. Yavor ◽  
...  

We studied individual semicircular canal responses in three dimensions to high-acceleration head rotations (“head impulses”) in subjects with known surgical lesions of the semicircular canals, and compared their results to those of normal subjects. We found that vestibular-ocular reflex (VOR) gains at close to peak head velocity in response to yaw, pitch and roll impulses were reliable indicators of semicircular canal function. When compared to normals, lateral canal function showed a 70–80% gain at peak of yaw head velocity during ipsilesional yaw impulses. After the loss of one vertical canal function there was a 30–50% and torsional VOR gain in response to ipsilesional pitch and roll impulses respectively. Bilateral deficits in anterior or posterior canal function resulted in a 80–90% impulses, while the loss of ipsilateral anterior and posterior canal functions will result in a 80–90% ipsilesional roll impulses. Three-dimensional vector analysis and animation of the VOR responses in a unilateral vestibular deafferented subject to yaw, pitch and roll impulses further demonstrated the deficits in magnitude and direction of the VOR responses following the loss of unilateral lateral, anterior and posterior canal functions.


2006 ◽  
Vol 96 (2) ◽  
pp. 925-930 ◽  
Author(s):  
Swee T. Aw ◽  
Michael J. Todd ◽  
G. Michael Halmagyi

Cathodal galvanic currents activate primary vestibular afferents, whereas anodal currents inhibit them. Pulsed galvanic vestibular stimulation (GVS) was used to determine the latency and initiation of the human vestibuloocular reflex. Three-dimensional galvanic vestibuloocular reflex (g-VOR) was recorded with binocular dual-search coils in response to a bilateral bipolar 100-ms rectangular pulse of current at 0.9 (near-threshold), 2.5, 5.0, 7.5, and 10.0 mA in 11 normal subjects. The g-VOR consisted of three components: conjugate torsional eye rotation away from cathode toward anode; vertical divergence (skew deviation) with hypertropia of the eye on the cathodal and hypotropia of the eye on the anodal sides; and conjugate horizontal eye rotation away from cathode toward anode. The g-VOR was repeatable across all subjects, its magnitude a linear function of the current intensity, its latency about 9.0 ms with GVS of ≥2.5 mA, and was not suppressed by visual fixation. At 10-mA stimulation, the g-VOR [ x, y, z] on the cathodal side was [0.77 ± 0.10, −0.05 ± 0.05, −0.18 ± 0.06°] (mean ± 95% confidence intervals) and on the anodal side was [0.79 ± 0.10, 0.16 ± 0.05, −0.19 ± 0.06°], with a vertical divergence of 0.20°. Although the horizontal g-VOR could have arisen from activation of the horizontal semicircular canal afferents, the vertical-torsional g-VOR resembled the vestibuloocular reflex in response to roll-plane head rotation about an Earth-horizontal axis and might be a result of both vertical semicircular canal and otolith afferent activations. Pulsed GVS is a promising technique to investigate latency and initiation of the human vestibuloocular reflex because it does not require a large mechanical apparatus nor does it pose problems of head inertia or slippage.


1987 ◽  
Vol 58 (4) ◽  
pp. 832-849 ◽  
Author(s):  
D. Tweed ◽  
T. Vilis

1. This paper develops three-dimensional models for the vestibuloocular reflex (VOR) and the internal feedback loop of the saccadic system. The models differ qualitatively from previous, one-dimensional versions, because the commutative algebra used in previous models does not apply to the three-dimensional rotations of the eye. 2. The hypothesis that eye position signals are generated by an eye velocity integrator in the indirect path of the VOR must be rejected because in three dimensions the integral of angular velocity does not specify angular position. Computer simulations using eye velocity integrators show large, cumulative gaze errors and post-VOR drift. We describe a simple velocity to position transformation that works in three dimensions. 3. In the feedback control of saccades, eye position error is not the vector difference between actual and desired eye positions. Subtractive feedback models must continuously adjust the axis of rotation throughout a saccade, and they generate meandering, dysmetric gaze saccades. We describe a multiplicative feedback system that solves these problems and generates fixed-axis saccades that accord with Listing's law. 4. We show that Listing's law requires that most saccades have their axes out of Listing's plane. A corollary is that if three pools of short-lead burst neurons code the eye velocity command during saccades, the three pools are not yoked, but function independently during visually triggered saccades. 5. In our three-dimensional models, we represent eye position using four-component rotational operators called quaternions. This is not the only algebraic system for describing rotations, but it is the one that best fits the needs of the oculomotor system, and it yields much simpler models than do rotation matrix or other representations. 6. Quaternion models predict that eye position is represented on four channels in the oculomotor system: three for the vector components of eye position and one inversely related to gaze eccentricity and torsion. 7. Many testable predictions made by quaternion models also turn up in models based on other mathematics. These predictions are therefore more fundamental than the specific models that generate them. Among these predictions are 1) to compute eye position in the indirect path of the VOR, eye or head velocity signals are multiplied by eye position feedback and then integrated; consequently 2) eye position signals and eye or head velocity signals converge on vestibular neurons, and their interaction is multiplicative.(ABSTRACT TRUNCATED AT 400 WORDS)


2011 ◽  
Vol 106 (5) ◽  
pp. 2151-2166 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Jakob S. Thomassen

One of the open questions in oculomotor control of visually guided eye movements is whether it is possible to smoothly track a target along a curvilinear path across the visual field without changing the torsional stance of the eye. We show in an experimental study of three-dimensional eye movements in subhuman primates ( Macaca mulatta) that although the pursuit system is able to smoothly change the orbital orientation of the eye's rotation axis, the smooth ocular motion was interrupted every few hundred milliseconds by a small quick phase with amplitude <1.5° while the animal tracked a target along a circle or ellipse. Specifically, during circular pursuit of targets moving at different angular eccentricities (5°, 10°, and 15°) relative to straight ahead at spatial frequencies of 0.067 and 0.1 Hz, the torsional amplitude of the intervening quick phases was typically around 1° or smaller and changed direction for clockwise vs. counterclockwise tracking. Reverse computations of the eye rotation based on the recorded angular eye velocity showed that the quick phases facilitate the overall control of ocular orientation in the roll plane, thereby minimizing torsional disturbances of the visual field. On the basis of a detailed kinematic analysis, we suggest that quick phases during curvilinear smooth tracking serve to minimize deviations from Donders' law, which are inevitable due to the spherical configuration space of smooth eye movements.


2005 ◽  
Vol 94 (5) ◽  
pp. 3417-3429 ◽  
Author(s):  
Mark F. Walker ◽  
David S. Zee

L. W. Schultheis and D. A. Robinson showed that the axis of the rotational vestibuloocular reflex (RVOR) cannot be altered by visual-vestibular mismatch (“cross-axis adaptation”) when the vestibulocerebellum is lesioned. This suggests that the cerebellum may calibrate the axis of eye velocity of the RVOR under natural conditions. Thus we asked whether patients with cerebellar disease have alterations in the RVOR axis and, if so, what might be the mechanism. We used three-axis scleral coils to record head and eye movements during yaw, pitch, and roll head impulses in 18 patients with cerebellar disease and in a comparison group of eight subjects without neurologic disease. We found distinct shifts of the eye-velocity axis in patients. The characteristic finding was a disconjugate upward eye velocity during yaw. Measured at 70 ms after the onset of head rotation, the median upward gaze velocity was 15% of yaw head velocity for patients and <1% for normal subjects ( P < 0.001). Upward eye velocity was greater in the contralateral (abducting) eye during yaw and in the ipsilateral eye during roll. Patients had a higher gain (eye speed/head speed) for downward than for upward pitch (median ratio of downward to upward gain: 1.3). In patients, upward gaze velocities during both yaw and roll correlated with the difference in anterior (AC) and posterior canal excitations, scaled by the respective pitch gains. Our findings support the hypothesis that upward eye velocity during yaw results from AC excitation, which must normally be suppressed by the intact cerebellum.


ORL ◽  
2002 ◽  
Vol 64 (6) ◽  
pp. 417-423 ◽  
Author(s):  
Takao Imai ◽  
Noriaki Takeda ◽  
Atsuhiko Uno ◽  
Masahiro Morita ◽  
Izumi Koizuka ◽  
...  

1991 ◽  
Vol 1 (3) ◽  
pp. 263-277 ◽  
Author(s):  
J.L. Demer ◽  
J. Goldberg ◽  
F.I. Porter ◽  
H.A. Jenkins ◽  
K. Schmidt

Vestibularly and visually driven eye movements interact to compensate for head movements to maintain the necessary retinal image stability for clear vision. The wearing of highly magnifying telescopic spectacles requires that such compensatory visual-vestibular interaction operate in a quantitative regime much more demanding than that normally encountered. We employed electro-oculography to investigate the effect of wearing of 2×, 4×, and 6× binocular telescopic spectacles on visual-vestibular interactions during sinusoidal head rotation in 43 normal subjects. All telescopic spectacle powers produced a large, immediate increase in the gain (eye velocity/head velocity) of compensatory eye movements, called the visual-vestibulo-ocular reflex (VVOR). However, the amount of VVOR gain augmentation became limited as spectacle magnification and the amplitude of head velocity increased. Optokinetic responses during wearing of telescopic spectacles exhibited a similar nonlinearity with respect to stimulus amplitude and spectacle magnification. Computer simulation was used to demonstrate that the nonlinear response of the VVOR with telescopic spectacles is a result of nonlinearities in visually guided tracking movements. Immediate augmentation of VVOR gain by telescopic spectacles declined significantly with increasing age in the subject pool studied. Presentation of unmagnified visual field peripheral to the telescopic spectacles reduced the immediate VVOR gain-enhancing effect of central magnified vision. These results imply that the VVOR may not be adequate to maintain retinal image stability during head movements when strongly magnifying telescopic spectacles are worn.


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