Combined Influence of Vergence and Eye Position on Three-Dimensional Vestibulo-Ocular Reflex in the Monkey

2002 ◽  
Vol 88 (5) ◽  
pp. 2368-2376 ◽  
Author(s):  
H. Misslisch ◽  
B.J.M. Hess
Keyword(s):  
Three Dimensional ◽  
Head Rotation ◽  
Eye Position ◽  
Near Vision ◽  
Ocular Reflex ◽  
Rotation Axes ◽  
Eye Rotation ◽  
Visual Background ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations

This study examined two kinematical features of the rotational vestibulo-ocular reflex (VOR) of the monkey in near vision. First, is there an effect of eye position on the axes of eye rotation during yaw, pitch and roll head rotations when the eyes are converged to fixate near targets? Second, do the three-dimensional positions of the left and right eye during yaw and roll head rotations obey the binocular extension of Listing's law (L2), showing eye position planes that rotate temporally by a quarter as far as the angle of horizontal vergence? Animals fixated near visual targets requiring 17 or 8.5° vergence and placed at straight ahead, 20° up, down, left, or right during yaw, pitch, and roll head rotations at 1 Hz. The 17° vergence experiments were performed both with and without a structured visual background, the 8.5° vergence experiments with a visual background only. A 40° horizontal change in eye position never influenced the axis of eye rotation produced by the VOR during pitch head rotation. Eye position did not affect the VOR eye rotation axes, which stayed aligned with the yaw and roll head rotation axes, when torsional gain was high. If torsional gain was low, eccentric eye positions produced yaw and roll VOR eye rotation axes that tilted somewhat in the directions predicted by Listing's law, i.e., with or opposite to gaze during yaw or roll. These findings were seen in both visual conditions and in both vergence experiments. During yaw and roll head rotations with a 40° vertical change in gaze, torsional eye position followed on average the prediction of L2: the left eye showed counterclockwise (ex-) torsion in down gaze and clockwise (in-) torsion in up gaze and vice versa for the right eye. In other words, the left and right eye's position plane rotated temporally by about a quarter of the horizontal vergence angle. Our results indicate that torsional gain is the central mechanism by which the brain adjusts the retinal image stabilizing function of the VOR both in far and near vision and the three dimensional eye positions during yaw and roll head rotations in near vision follow on average the predictions of L2, a kinematic pattern that is maintained by the saccadic/quick phase system.

Oculomotor Control of Primary Eye Position Discriminates Between Translation and Tilt

1999 ◽  
Vol 81 (1) ◽  
pp. 394-398 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki
Keyword(s):  
Dynamic Control ◽  
Linear Acceleration ◽  
Oculomotor System ◽  
Oculomotor Control ◽  
Eye Position ◽  
Axis Orientation ◽  
Fast Phase ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations

Hess, Bernhard J. M. and Dora E. Angelaki. Oculomotor control of primary eye position discriminates between translation and tilt. J. Neurophysiol. 81: 394–398, 1999. We have previously shown that fast phase axis orientation and primary eye position in rhesus monkeys are dynamically controlled by otolith signals during head rotations that involve a reorientation of the head relative to gravity. Because of the inherent ambiguity associated with primary otolith afferent coding of linear accelerations during head translation and tilts, a similar organization might also underlie the vestibulo-ocular reflex (VOR) during translation. The ability of the oculomotor system to correctly distinguish translational accelerations from gravity in the dynamic control of primary eye position has been investigated here by comparing the eye movements elicited by sinusoidal lateral and fore-aft oscillations (0.5 Hz ± 40 cm, equivalent to ± 0.4 g) with those during yaw rotations (180°/s) about a vertically tilted axis (23.6°). We found a significant modulation of primary eye position as a function of linear acceleration (gravity) during rotation but not during lateral and fore-aft translation. This modulation was enhanced during the initial phase of rotation when there was concomitant semicircular canal input. These findings suggest that control of primary eye position and fast phase axis orientation in the VOR are based on central vestibular mechanisms that discriminate between gravity and translational head acceleration.

Vergence-mediated changes in the axis of eye rotation during the human vestibulo-ocular reflex can occur independent of eye position

2003 ◽  
Vol 151 (2) ◽  
pp. 238-248 ◽  
Author(s):  
Americo A. Migliaccio ◽  
Phillip D. Cremer ◽  
Swee T. Aw ◽  
G. Michael Halmagyi ◽  
Ian S. Curthoys ◽  
...  
Keyword(s):  
Eye Position ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Vestibulo Ocular Reflex

scholarly journals Enhancement of the Vestibulo-Ocular Reflex by Prior Eye Movements

1999 ◽  
Vol 81 (6) ◽  
pp. 2884-2892 ◽  
Author(s):  
Vallabh E. Das ◽  
Louis F. Dell’Osso ◽  
R. John Leigh
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Initial Perturbation ◽  
Head Rotation ◽  
Gaze Shift ◽  
Stationary Target ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations ◽  
Horizontal Head

Enhancement of the vestibulo-ocular reflex by prior eye movements. We investigated the effect of visually mediated eye movements made before velocity-step horizontal head rotations in eleven normal human subjects. When subjects viewed a stationary target before and during head rotation, gaze velocity was initially perturbed by ∼20% of head velocity; gaze velocity subsequently declined to zero within ∼300 ms of the stimulus onset. We used a curve-fitting procedure to estimate the dynamic course of the gain throughout the compensatory response to head rotation. This analysis indicated that the median initial gain of compensatory eye movements (mainly because of the vestibulo-ocular reflex, VOR) was 0.8 and subsequently increased to 1.0 after a median interval of 320 ms. When subjects attempted to fixate the remembered location of the target in darkness, the initial perturbation of gaze was similar to during fixation of a visible target (median initial VOR gain 0.8); however, the period during which the gain increased toward 1.0 was >10 times longer than that during visual fixation. When subjects performed horizontal smooth-pursuit eye movements that ended (i.e., 0 gaze velocity) just before the head rotation, the gaze velocity perturbation at the onset of head rotation was absent or small. The initial gain of the VOR had been significantly increased by the prior pursuit movements for all subjects ( P < 0.05; mean increase of 11%). In four subjects, we determined that horizontal saccades and smooth tracking of a head-fixed target (VOR cancellation with eye stationary in the orbit) also increased the initial VOR gain (by a mean of 13%) during subsequent head rotations. However, after vertical saccades or smooth pursuit, the initial gaze perturbation caused by a horizontal head rotation was similar to that which occurred after fixation of a stationary target. We conclude that the initial gain of the VOR during a sudden horizontal head rotation is increased by prior horizontal, but not vertical, visually mediated gaze shifts. We postulate that this “priming” effect of a prior gaze shift on the gain of the VOR occurs at the level of the velocity inputs to the neural integrator subserving horizontal eye movements, where gaze-shifting commands and vestibular signals converge.

Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum

2007 ◽  
Vol 98 (1) ◽  
pp. 295-302 ◽  
Author(s):  
Mark F. Walker ◽  
Jing Tian ◽  
David S. Zee
Keyword(s):  
Tilt Angle ◽  
Three Dimensional ◽  
Head Rotation ◽  
Normal Subjects ◽  
Eye Position ◽  
Vestibuloocular Reflex ◽  
Gaze Stabilization ◽  
Eye Rotation ◽  
Axis Rotation ◽  
Head Impulses

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.

scholarly journals Human vestibulo-ocular reflex adaptation is frequency selective

2019 ◽  
Vol 122 (3) ◽  
pp. 984-993 ◽  
Author(s):  
Carlo N. Rinaudo ◽  
Michael C. Schubert ◽  
William V. C. Figtree ◽  
Christopher J. Todd ◽  
Americo A. Migliaccio
Keyword(s):  
High Frequency ◽  
Head Rotation ◽  
Head Movements ◽  
Head Impulse ◽  
Ocular Reflex ◽  
Before And After ◽  
Vestibulo Ocular Reflex ◽  
Vor Adaptation ◽  
Frequency Selective ◽  
Head Rotations

The vestibulo-ocular reflex (VOR) is the only system that maintains stable vision during rapid head rotations. The VOR gain (eye/head velocity) can be trained to increase using a vestibular-visual mismatch stimulus. We sought to determine whether low-frequency (sinusoidal) head rotation during training leads to changes in the VOR during high-frequency head rotation testing, where the VOR is more physiologically relevant. We tested eight normal subjects over three sessions. For training protocol 1, subjects performed active sinusoidal head rotations at 1.3 Hz while tracking a laser target, whose velocity incrementally increased relative to head velocity so that the VOR gain required to stabilize the target went from 1.1 to 2 over 15 min. Protocol 2 was the same as protocol 1, except that head rotations were at 0.5 Hz. For protocol 3, head rotation frequency incrementally increased from 0.5 to 2 Hz over 15 min, while the VOR gain required to stabilize the target was kept at 2. We measured the active and passive, sinusoidal (1.3Hz) and head impulse VOR gains before and after each protocol. Sinusoidal and head impulse VOR gains increased in protocols 1 and 3; however, although the sinusoidal VOR gain increase was ~20%, the related head impulse gain increase was only ~10%. Protocol 2 resulted in no-gain adaptation. These data show human VOR adaptation is frequency selective, suggesting that if one seeks to increase the higher-frequency VOR response, i.e., where it is physiologically most relevant, then higher-frequency head movements are required during training, e.g., head impulses. NEW & NOTEWORTHY This study shows that human vestibulo-ocular reflex adaptation is frequency selective at frequencies >0.3 Hz. The VOR in response to mid- (1.3 Hz) and high-frequency (impulse) head rotations were measured before and after mid-frequency sinusoidal VOR adaptation training, revealing that the mid-frequency gain change was higher than high-frequency gain change. Thus, if one seeks to increase the higher-frequency VOR response, where it is physiologically most relevant, then higher-frequency head movements are required during training.

Rotational kinematics of the human vestibuloocular reflex. I. Gain matrices

1994 ◽  
Vol 72 (5) ◽  
pp. 2467-2479 ◽  
Author(s):  
D. Tweed ◽  
D. Sievering ◽  
H. Misslisch ◽  
M. Fetter ◽  
D. Zee ◽  
...  
Keyword(s):  
Three Dimensional ◽  
Frontal Plane ◽  
Head Rotation ◽  
Maximum Speed ◽  
Vestibuloocular Reflex ◽  
Matrix Elements ◽  
Head Velocity ◽  
Eye Rotation ◽  
Eye Velocity ◽  
Head Rotations

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.

Torsional dynamics and cross-coupling in the human vestibulo-ocular reflex during active head rotation

2000 ◽  
Vol 10 (2) ◽  
pp. 119-125 ◽  
Author(s):  
H. Misslisch ◽  
D. Tweed
Keyword(s):  
Cross Coupling ◽  
Head Rotation ◽  
Adaptive Networks ◽  
Low Frequencies ◽  
3 Dimensional ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Eye Motion ◽  
Vestibulo Ocular Reflex ◽  
Save Energy

Six subjects fixated an imagined space-fixed target in darkness, or a visible target against a structured visual background, while rotating their heads actively in yaw, pitch and roll at four different frequencies, from 0.3 to 2.4 Hz. We used search coils to measure the 3-dimensional rotations of the head and eye, and described the relation between them – the input-output function of the rotational vestibulo-ocular reflex (VOR) – using gain matrices. We found consistent cross-coupling in which torsional head rotation evoked horizontal eye rotation. The reason may be that the eyes are above the axis of torsional head rotation, and therefore may translate horizontally during the head motion, so the VOR rotates them horizontally to compensate. Torsional gain was lower than horizontal or vertical, more variable from subject to subject and decreased at low frequencies. One reason for the low gain may be that torsional head rotation produces little retinal slip near the fovea; hence little compensatory eye motion is needed, and so the VOR reduces its torsional gain to save energy or to approximate Listing's law by keeping ocular torsion near zero. In addition, the human VOR has little experience with purely torsional head rotations and so its adaptive networks may be poorly trained for such stimuli. The drop in torsional gain at low frequencies can be explained based on the leak in the neural integrator that helps convert torsional eye-velocity commands into eye-position commands.

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

1996 ◽  
Vol 76 (6) ◽  
pp. 4021-4030 ◽  
Author(s):  
S. T. Aw ◽  
G. M. Halmagyi ◽  
T. Haslwanter ◽  
I. S. Curthoys ◽  
R. A. Yavor ◽  
...  
Keyword(s):  
Confidence Intervals ◽  
Rotation Axis ◽  
Three Dimensional ◽  
Head Rotation ◽  
Vestibuloocular Reflex ◽  
Dimensional Vector ◽  
Head Impulse ◽  
High Acceleration ◽  
Eye Rotation ◽  
Head Rotations

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.

Three Dimensional Eye Movements of Squirrel Monkeys Following Postrotatory Tilt

1993 ◽  
Vol 3 (2) ◽  
pp. 123-139 ◽  
Author(s):  
Daniel M. Merfeld ◽  
Laurence R. Young ◽  
Gary D. Paige ◽  
David L. Tomko
Keyword(s):  
Eye Movements ◽  
Time Course ◽  
Three Dimensional ◽  
Three Dimensions ◽  
Head Orientation ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Acceleration And Deceleration ◽  
Vestibulo Ocular Reflex ◽  
Vertical Nystagmus

Three-dimensional squirrel monkey eye movements were recorded during and immediately following rotation around an earth-vertical yaw axis (160∘/s steady state, 100∘/s2 acceleration and deceleration). To study interactions between the horizontal angular vestibulo-ocular reflex (VOR) and head orientation, postrotatory VOR alignment was changed relative to gravity by tilting the head out of the horizontal plane (pitch or roll tilt between 15∘ and 90∘) immediately after cessation of motion. Results showed that in addition to post rotatory horizontal nystagmus, vertical nystagmus followed tilts to the left or right (roll), and torsional nystagmus followed forward or backward (pitch) tilts. When the time course and spatial orientation of eye velocity were considered in three dimensions, the axis of eye rotation always shifted toward alignment with gravity, and the postrotatory horizontal VOR decay was accelerated by the tilts. These phenomena may reflect a neural process that resolves the sensory conflict induced by this postrotatory tilt paradigm.

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