Control of Spatial Orientation of the Angular Vestibuloocular Reflex by the Nodulus and Uvula

1998 ◽  
Vol 79 (5) ◽  
pp. 2690-2715 ◽  
Author(s):  
Susan Wearne ◽  
Theodore Raphan ◽  
Bernard Cohen
Keyword(s):  
Spatial Orientation ◽  
Three Dimensional ◽  
Cross Coupling ◽  
Velocity Storage ◽  
Coordinate Frame ◽  
Vestibuloocular Reflex ◽  
Time Constants ◽  
Vertical Roll ◽  
Eye Rotation ◽  
Eye Velocity

Wearne, Susan, Theodore Raphan, and Bernard Cohen. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J. Neurophysiol. 79: 2690–2715, 1998. Spatial orientation of the angular vestibuloocular reflex (aVOR) was studied in rhesus monkeys after complete and partial ablation of the nodulus and ventral uvula. Horizontal, vertical, and torsional components of slow phases of nystagmus were analyzed to determine the axes of eye rotation, the time constants (Tcs) of velocity storage, and its orientation vectors. The gravito-inertial acceleration vector (GIA) was tilted relative to the head during optokinetic afternystagmus (OKAN), centrifugation, and reorientation of the head during postrotatory nystagmus. When the GIA was tilted relative to the head in normal animals, horizontal Tcs decreased, vertical and/or roll time constants (Tcvert/roll) lengthened according to the orientation of the GIA, and vertical and/or roll eye velocity components appeared (cross-coupling). This shifted the axis of eye rotation toward alignment with the tilted GIA. Horizontal and vertical/roll Tcs varied inversely, with Tchor being longest and Tcvert/roll shortest when monkeys were upright, and the reverse when stimuli were around the vertical or roll axes. Vertical or roll Tcs were longest when the axes of eye rotation were aligned with the spatial vertical, respectively. After complete nodulo-uvulectomy, Tchor became longer, and periodic alternating nystagmus (PAN) developed in darkness. Tchor could not be shortened in any of paradigms tested. In addition, yaw-to-vertical/roll cross-coupling was lost, and the axes of eye rotation remained fixed during nystagmus, regardless of the tilt of the GIA with respect to the head. After central portions of the nodulus and uvula were ablated, leaving lateral portions of the nodulus intact, yaw-to-vertical/roll cross-coupling and control of Tcvert/roll was lost or greatly reduced. However, control of Tchor was maintained, and Tchor continued to vary as a function of the tilted GIA. Despite this, the eye velocity vector remained aligned with the head during yaw axis stimulation after partial nodulo-uvulectomy, regardless of GIA orientation to the head. The data were related to a three-dimensional model of the aVOR, which simulated the experimental results. The model provides a basis for understanding how the nodulus and uvula control processing within the vestibular nuclei responsible for spatial orientation of the aVOR. We conclude that the three-dimensional dynamics of the velocity storage system are determined in the nodulus and ventral uvula. We propose that the horizontal and vertical/roll Tcs are separately controlled in the nodulus and uvula with the dynamic characteristics of vertical/roll components modulated in central portions and the horizontal components laterally, presumably in a semicircular canal-based coordinate frame.

Contribution of Vestibular Commissural Pathways to Spatial Orientation of the Angular Vestibuloocular Reflex

1997 ◽  
Vol 78 (2) ◽  
pp. 1193-1197 ◽  
Author(s):  
Susan Wearne ◽  
Theodore Raphan ◽  
Bernard Cohen
Keyword(s):  
Spatial Orientation ◽  
Semicircular Canal ◽  
Vertical Axis ◽  
Vestibular Stimulation ◽  
Velocity Storage ◽  
Vestibuloocular Reflex ◽  
Time Constants ◽  
Commissural Pathways ◽  
Before And After ◽  
Axis Rotation

Wearne, Susan, Theodore Raphan, and Bernard Cohen. Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J. Neurophysiol. 78: 1193–1197, 1997. During nystagmus induced by the angular vestibuloocular reflex (aVOR), the axis of eye velocity tends to align with the direction of gravitoinertial acceleration (GIA), a process we term “spatial orientation of the aVOR.” We studied spatial orientation of the aVOR in rhesus and cynomolgus monkeys before and after midline section of the rostral medulla abolished all oculomotor functions related to velocity storage, leaving the direct optokinetic and vestibular pathways intact. Optokinetic afternystagmus and the bias component of off-vertical-axis rotation were lost, and the aVOR time constant was reduced to a value commensurate with the time constants of primary semicircular canal afferents. Spatial orientation of the aVOR, induced either during optokinetic or vestibular stimulation, was also lost. Vertical and roll aVOR time constants could no longer be lengthened in side-down or supine/prone positions, and static and dynamic tilts of the GIA no longer produced cross-coupling from the yaw to pitch and yaw to roll axes. Consequently, the induced nystagmus remained entirely in head coordinates after the lesion, regardless of the direction of the resultant GIA vector. Gains of the aVOR and of optokinetic nystagmus to steps of velocity were unaffected or slightly increased. These results are consistent with a model in which the direct aVOR pathways are organized in semicircular canal coordinates and spatial orientation is restricted to the indirect (velocity storage) pathways.

Compensatory and Orienting Eye Movements Induced By Off-Vertical Axis Rotation (OVAR) in Monkeys

2002 ◽  
Vol 88 (5) ◽  
pp. 2445-2462 ◽  
Author(s):  
Keisuke Kushiro ◽  
Mingjia Dai ◽  
Mikhail Kunin ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
...  
Keyword(s):  
Eye Movements ◽  
Vertical Axis ◽  
Velocity Storage ◽  
Eye Position ◽  
Rotational Axis ◽  
Vestibuloocular Reflex ◽  
Time Constants ◽  
Head Velocity ◽  
Axis Rotation ◽  
Eye Velocity

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15°, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15–90°, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7–0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABAB agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by ≈90°, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3°/ g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0°/ g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ∼180° relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.

Spatial Orientation of Caloric Nystagmus in Semicircular Canal-Plugged Monkeys

2002 ◽  
Vol 88 (2) ◽  
pp. 914-928 ◽  
Author(s):  
Yasuko Arai ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
Jun-Ichi Suzuki ◽  
Theodore Raphan
Keyword(s):  
Phase Velocity ◽  
Spatial Orientation ◽  
Velocity Vector ◽  
Semicircular Canals ◽  
Velocity Storage ◽  
Slow Phase ◽  
Coordinate Frame ◽  
Slow Phase Velocity ◽  
Caloric Nystagmus ◽  
Eye Velocity

We studied caloric nystagmus before and after plugging all six semicircular canals to determine whether velocity storage contributed to the spatial orientation of caloric nystagmus. Monkeys were stimulated unilaterally with cold (≈20°C) water while upright, supine, prone, right-side down, and left-side down. The decline in the slow phase velocity vector was determined over the last 37% of the nystagmus, at a time when the response was largely due to activation of velocity storage. Before plugging, yaw components varied with the convective flow of endolymph in the lateral canals in all head orientations. Plugging blocked endolymph flow, eliminating convection currents. Despite this, caloric nystagmus was readily elicited, but the horizontal component was always toward the stimulated (ipsilateral) side, regardless of head position relative to gravity. When upright, the slow phase velocity vector was close to the yaw and spatial vertical axes. Roll components became stronger in supine and prone positions, and vertical components were enhanced in side down positions. In each case, this brought the velocity vectors toward alignment with the spatial vertical. Consistent with principles governing the orientation of velocity storage, when the yaw component of the velocity vector was positive, the cross-coupled pitch or roll components brought the vector upward in space. Conversely, when yaw eye velocity vector was downward in the head coordinate frame, i.e., negative, pitch and roll were downward in space. The data could not be modeled simply by a reduction in activity in the ipsilateral vestibular nerve, which would direct the velocity vector along the roll direction. Since there is no cross coupling from roll to yaw, velocity storage alone could not rotate the vector to fit the data. We postulated, therefore, that cooling had caused contraction of the endolymph in the plugged canals. This contraction would deflect the cupula toward the plug, simulating ampullofugal flow of endolymph. Inhibition and excitation induced by such cupula deflection fit the data well in the upright position but not in lateral or prone/supine conditions. Data fits in these positions required the addition of a spatially orientated, velocity storage component. We conclude, therefore, that three factors produce cold caloric nystagmus after canal plugging: inhibition of activity in ampullary nerves, contraction of endolymph in the stimulated canals, and orientation of eye velocity to gravity through velocity storage. Although the response to convection currents dominates the normal response to caloric stimulation, velocity storage probably also contributes to the orientation of eye velocity.

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.

Spatial orientation of the angular vestibulo-ocular reflex

1999 ◽  
Vol 9 (3) ◽  
pp. 163-172
Author(s):  
Bernard Cohen ◽  
Susan Wearne ◽  
Mingjia Dai ◽  
Theodore Raphan
Keyword(s):  
Spatial Orientation ◽  
Optokinetic Nystagmus ◽  
Vestibular Nuclei ◽  
Velocity Storage ◽  
Gravitational Acceleration ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Slow Velocity ◽  
Vestibulo Ocular Reflex ◽  
Vector Sum

During vestibular nystagmus, optokinetic nystagmus (OKN), and optokinetic afternystagmus (OKAN), the axis of eye rotation tends to align with the vector sum of linear accelerations acting on the head. This includes gravitational acceleration and the linear accelerations generated by translation and centrifugation. We define the summed vector of gravitational and linear accelerations as gravito-inertial acceleration (GIA) and designate the phenomenon of alignment as spatial orientation of the angular vestibuloocular reflex (aVOR). On the basis of studies in the monkey, we postulated that the spatial orientation of the aVOR is dependent on the slow (velocity storage) component of the aVOR, not on the short latency, compensatory aVOR component, which is in head-fixed coordinates. Experiments in which velocity storage was abolished by midline medullary section support this postulate. The velocity storage component of the aVOR is likely to be generated in the vestibular nuclei, and its spatial orientation was shown to be controlled through the nodulus and uvula of the vestibulo-cerebellum. Separate regions of the nodulus/uvula appear to affect the horizontal and vertical/torsional components of the response differently. Velocity storage is weaker in humans than in monkeys, but responds in a similar fashion in both species. We postulate that spatial orientation of the aVOR plays an important role in aligning gaze with the GIA and in maintaining balance during angular locomotion.

Spatial orientation of postrotatory nystagmus during static roll tilt in cats

2002 ◽  
Vol 12 (1) ◽  
pp. 15-23
Author(s):  
Keiko Yasuda ◽  
Hiroaki Fushiki ◽  
Rinnosuke Wada ◽  
Yukio Watanabe
Keyword(s):  
Spatial Orientation ◽  
Vertical Axis ◽  
Longitudinal Axis ◽  
Velocity Storage ◽  
Slow Phase ◽  
Storage Mechanism ◽  
Spatial Disorientation ◽  
Acceleration And Deceleration ◽  
Eye Velocity ◽  
Roll Tilt

While the stimulation of otolith inputs reduces the duration of postrotatory nystagmus (PRN), there is still room for dialogue about the effect of static tilt on the orientation of PRN. We studied one possible influence of static roll tilt on the spatial orientation of PRN in cats. The animal was rotated about an earth-vertical axis (EVA) at a constant velocity of 100 deg/s with an acceleration and deceleration of 120 deg / s 2 . Within two seconds after stopping EVA rotation, the animal was passively tilted at 45 deg/s about its longitudinal axis by as much as ± 90 deg in steps of 15 deg. Eye movements were measured with magnetic search coils. The angle of the PRN plane and its slow phase eye velocity were measured. The time constant of PRN decreased with an increase in roll tilt. The PRN plane remained earth horizontal within a range of ± 30 deg roll tilt. Beyond this range, the velocity of PRN decreased too rapidly to measure any change in orientation. Our results indicate a spatially limited and temporally short interaction of the semicircular canal and otolith signals in the velocity storage mechanism of cat PRN. Our data, along with previous studies, suggest that different species show different solutions to the problem of the imbalance and spatial disorientation during contradictory stimuli.

Rotational kinematics of the human vestibuloocular reflex. II. Velocity steps

1994 ◽  
Vol 72 (5) ◽  
pp. 2480-2489 ◽  
Author(s):  
D. Tweed ◽  
M. Fetter ◽  
D. Sievering ◽  
H. Misslisch ◽  
E. Koenig
Keyword(s):  
Cross Talk ◽  
Human Subjects ◽  
Head Rotation ◽  
Horizontal Axis ◽  
Main Diagonal ◽  
Velocity Storage ◽  
Vestibuloocular Reflex ◽  
Simple Explanation ◽  
Time Constants ◽  
Axis Rotation

1. Gain matrices were used to quantify the three-dimensional vestibuloocular reflex (VOR) in five human subjects who were accelerated over 1 s and then spun at a constant 150 degrees/s for 29 s in darkness. Rotations were torsional, vertical and horizontal, about earth-vertical and earth-horizontal axes. 2. Elements on the main diagonal of the gain matrices were much smaller than the optimal value of -1, and torsional gain was weaker than vertical or horizontal. Off-diagonal elements, indicating cross talk, were minimal except for a small but consistent horizontal response to torsional head rotation. 3. Downward slow phases were more than twice as fast as upward at the start of rotation about both earth-vertical and earth-horizontal axes, but the asymmetry vanished later in the rotation. 4. During earth-vertical-axis rotation, all matrix elements decayed to zero. The main-diagonal torsional and vertical gains waned with time constants close to that of the cupula (6.7 and 7.3 s). Velocity storage prolonged the horizontal response to horizontal head rotation (time constant 14.2 s) but not the horizontal response to torsion (7.7 s). A simple explanation is that velocity storage acts on a central estimate of head motion that accurately distinguishes horizontal from torsional and that the inappropriate horizontal eye velocity response to torsion occurs because of cross talk downstream from velocity storage. 5. During earth-horizontal-axis rotation, the torsional, vertical, and horizontal main-diagonal elements declined, with time constants of 7.6, 8.2, and 7.9 s, to maintained nonzero values, all equal to about -0.1. Off-diagonal elements, including the horizontal response to torsion, decayed to zero, so that the otolith-driven reflex, late in the rotation, was equally strong in all dimensions and almost free of detectable cross talk. 6. The difference between gain curves over the course of earth-vertical- and earth-horizontal-axis rotations was not constant but increased with time, suggesting that the VOR response to earth-horizontal-axis rotation is not a simple sum of canal and otolith reflexes.

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.

Model-based study of the human cupular time constant

1999 ◽  
Vol 9 (4) ◽  
pp. 293-301 ◽  
Author(s):  
Mingjia Dai ◽  
Avniel Klein ◽  
Bernard Cohen ◽  
Theodore Raphan
Keyword(s):  
Time Constant ◽  
Human Subjects ◽  
Vestibular Nerve ◽  
Velocity Storage ◽  
Slow Phase ◽  
Initial Portion ◽  
Time Constants ◽  
Model Based ◽  
Double Exponential ◽  
Eye Velocity

The time constant of the angular vestibulo-ocular reflex (aVOR), measured from the response to steps of rotation about a yaw axis, has frequently been estimated as a single exponential. However, the slow phase velocity envelope during per- or post-rotatory nystagmus is more accurately represented by two exponential modes. One represents activity in the vestibular nerve induced by deflection of the cupula, the other by activation that the input from the canals produces in the central velocity storage integrator. The sum of the cupula and the integrator responses describes the overall response of slow phase eye velocity and can be approximated by a double exponential. Frequently, there is a plateau in the initial portion of eye velocity response, but this may be masked by habituation, making the cupula contribution unobservable and impossible to estimate. Using a model-based technique to analyze responses with a clear plateau, we estimated peripheral and central vestibular time constants by double exponential fits to slow phase eye velocity. Cupular time constants were varied from 1 to 10 s to identify values that gave optimal fits of the data according to a Chi-square criterion. The mean cupular time constant for 10 human subjects was 4.2 ± 0.6 s. Fits of the data were also good for time constants between 3.5 to 7 s, but not for 1 to 3 or 7.5 to 10 s. The estimated cupular time constants also fit responses where there was no plateau. In 8 monkeys, cupular time constants were estimated as 3.9 ± 0.5 s, which agreed with those derived from activity in the vestibular nerve. There was no difference between monkey and human cupular time constants from these estimates. It is likely that the human cupular time constant is similar to that of the monkey and shorter than previously thought.

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