Torsional Vestibulo-ocular Reflex Research Articles

Dynamic properties of the human vestibulo-ocular reflex during head rotations in roll

We investigated the dynamic properties of the human vestibulo-ocular reflex (VOR) during roll head rotations in three human subjects using the magnetic search coil technique. In the first of two experiments, we quantify the behavior of the ocular motor plant in the torsional plane. The subject's eye was mechanically displaced into intorsion, extorsion or abduction, and the dynamic course of return of the eye to its resting position was measured. The mean predominant time constants of return were 210 msec from intorsion, 83 msec from extorsion, and 217 msec from abduction, although there was considerable variability of results from different trials and subjects. In the second experiment, we quantify the efficacy of velocity-to-position integration of the vestibular signal. Position-step stimuli were used to test the torsional or horizontal VOR, being applied with subjects heads erect or supine. After a torsional position-step, the eye drifted back to its resting position, but after a horizontal position-step the eye held its new horizontal position. To interpret these responses we used a simple model of the VOR with parameters of the ocular motor plant set to values determined during Expt 1. The time constant of the velocity-to-position neural integrator was smaller (typically 2 sec) in the torsional plane than in the horizontal plane ( > 20 sec). No disconjugacy of torsional eye movements was observed. Thus, the dynamic properties of the VOR in roll differ significantly from those of the VOR in yaw, reflecting different visual demands placed on this reflex in these two planes.

Vestibulo-ocular reflex

Recent animal and clinical studies on the vestibulo-ocular reflex deal with a number of physiological and clinical aspects from which three were chosen for this review: (1) the torsional vestibulo-ocular reflex and its disorders; (2) the otolith contribution to the vestibulo-ocular reflex; and (3) neurotransmitters, neuropharmacological aspects, and medical treatment. Disorders of the vestibulo-ocular reflex can be classified according to the three major planes of action, yaw plane, pitch plane, and roll plane, which equate with horizontal nystagmus, upbeat or downbeat nystagmus, and torsional nystagmus, respectively. The particular interest in the torsional vestibulo-ocular reflex arises from new methods for measuring ocular torsion, especially the three-dimensional eye-movement recordings with scleral coils. These methods make it possible to do three-dimensional analysis of the differential effects of horizontal and vertical semicircular canal function and their individual disorders of the torsional vestibulo-ocular reflex. Otolith and semicircular canal inputs converge at the level of the vestibular nuclei to subserve static graviceptive and dynamic torsional and pitch function. The elaboration of the particular sensorial weight of the input from either the otoliths or the semicircular canal is currently a challenge for both physiologists and neurologists. Disorders of otolith function, still absent from the diagnostic repertoire of most neurologists, are increasingly being reported. The most promising developments in therapeutic measures may come from research on vestibular neurotransmitters, their agonists and antagonists. A number of pharmacological agents are effective suppressants of pathological eye movements. However, systematic prospective studies are needed.(ABSTRACT TRUNCATED AT 250 WORDS)

Rotational kinematics of the human vestibuloocular reflex. III. Listing's law

1. Do slow phase eye velocities generated by the vestibuloocular reflex (VOR) depend on eye position? If the purpose of the VOR is simply to stabilize the retinal image, there can be no such dependence, because eye velocity must always be equal and opposite to head velocity. But if the VOR tolerates some retinal slip to achieve other goals, such as reducing eye velocity or following Listing's law, then one should see specific patterns of dependence. We examined VOR responses of human subjects to yaw, pitch, and roll rotation looking in various directions to quantify how the input-output properties of the VOR vary with eye position. 2. Eye rotation axes during yaw and pitch tilted in the same direction as the gaze line but only one-quarter as far on average. Thus, during yaw head rotation, the axis of eye rotation was roughly aligned with the head axis when the subject looked straight ahead, but tilted up when the gaze direction was up, and down when gaze was down. The amount of tilt varied between subjects, but on average a 30 degrees change in eye position caused a 7.5 degrees tilt in the eye rotation axis. During pitch, the eye axis tilted right when gaze was right and left when gaze was left, also moving 7.5 degrees on average for a 30 degrees change in the gaze direction. 3. During roll stimulation, the axis of eye rotation tilted in the opposite direction to the gaze line, and about one-half as far. On average, when the gaze line moved 30 degrees down, the eye rotation axis tilted 12.0 degrees up; when the gaze moved 30 degrees left, the eye axis tilted 15.3 degrees right. 4. It is often argued that the torsional VOR is weak because head rotation about the line of sight causes little image displacement on the fovea. But the line of sight is collinear with the torsional axis only when the subject looks straight ahead. Does the "weak axis" of the VOR stay collinear with the gaze line when the subject looks eccentrically? We calculated the axis of head rotation for which the VOR response is weakest and found that it does vary with eye position, but does not stay parallel with the gaze direction. When subjects looked straight ahead, the weak axis was roughly collinear with the gaze line; when gaze shifted eccentrically, the weak axis shifted in the same direction but only about one-half as far.(ABSTRACT TRUNCATED AT 400 WORDS)

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

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.

The cerebellar nodulus and ventral uvula control the torsional vestibulo-ocular reflex

1. The vestibulo-ocular reflex (VOR) was investigated in rhesus monkeys before and after surgical ablation of the cerebellar nodulus and ventral uvula. The lesion resulted in an alteration of the torsional VOR: compensatory eye movements were poor in the low frequency range and the time constant was reduced to values comparable to those of primary semicircular canal afferents. In addition, animals permanently lost their ability to generate torsional optokinetic nystagmus (OKN). 2. The effects of the lesion on the torsional VOR differed from those observed in the horizontal and vertical vestibulo-ocular systems. While the vertical VOR and OKN were unaltered, the horizontal VOR and OKN were characterized by increased time constants and smaller phase leads during low frequency head oscillations. 3. These results suggest that the cerebellar nodulus and/or ventral uvula exert a distinct and specific dynamic control on the torsional vestibulo-ocular and optokinetic reflexes. Such specific effects on the torsional system could reflect a functional segregation of the vestibulo-cerebellum in terms of the controls of torsional versus horizontal and vertical slow phase eye movements.

Torsional vestibulo-ocular reflex measurements for identifying otolith asymmetries possibly related to space motion sickness susceptibility

Recent studies by Diamond and Markham 1,2 have identified significant correlations between space motion sickness susceptibility and measures of disconjugate torsional eye movements recorded during parabolic flights. These results support an earlier proposal by von Baumgarten and Thümler 3 which hypothesized that an asymmetry of otolith function between the two ears is the cause of space motion sickness. It may be possible to devise experiments that can be performed in the 1 g environment on earth that could identify and quantify the presence of asymmetric otolith function. This paper summarizes the known physiological and anatomical properties of the otolith organs and the properties of the torsional vestibulo-ocular reflex which are relevant to the design of a stimulus to identify otolith asymmetries. A specific stimulus which takes advantage of these properties is proposed.

Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex

1. The spatial organization of the vestibuloocular reflex (VOR) was studied in six rhesus monkeys by applying fast, short-lasting, passive head and body tilts immediately after constant-velocity rotation (+/- 90 degrees/s) about an earth-vertical axis. Two alternative hypotheses were investigated regarding the reference frame used for coding angular motion. 1) If the vestibular system is organized in head-centered coordinates, postrotatory eye velocity would decay invariably along the direction of applied head angular acceleration. 2) Alternatively, if the vestibular system codes angular motion in inertial, gravity-centered coordinates, postrotatory eye velocity would decay along the direction of gravity. 2. Horizontal VOR was studied with the monkeys upright. Pitch (roll) tilts away from upright elicited a transient vertical (torsional) VOR and shortened the time constant of the horizontal postrotatory slow phase velocity. In addition, an orthogonal torsional (after pitch tilts) or vertical (after roll tilts) response gradually built up. As a result, the eye velocity vector transiently deviated in the roll (pitch) plane and then gradually rotated in the same direction as gravity in the pitch (roll) head plane until the orthogonal component reached a peak value. Subsequently, the residual postrotatory eye velocity decayed along a line parallel to gravity. 3. The time constant of the horizontal postrotatory response was maximal in upright position (21.5 +/- 5.7 s, mean +/- SD) and minimal after tilts to prone (3.8 +/- 0.7 s), supine (4.5 +/- 1.2 s), and ear-down (5.2 +/- 1.6 s) positions. A similar dependence on head orientation relative to gravity characterized the dynamics of the resultant eye velocity vector in the pitch and roll planes. 4. Torsional VOR was studied with the monkeys in supine or prone position. Pitch (yaw) tilts from the supine or prone position toward upright (ear-down) position elicited a transient vertical (horizontal) VOR and shortened the time constant of the torsional postrotatory response while a horizontal (vertical) orthogonal component slowly built up. As a result the eye velocity vector gradually rotated in the pitch (yaw) plane until the orthogonal component reached a peak value. Subsequently residual postrotatory eye velocity decayed along a line parallel to gravity. 5. The time constant of the torsional postrotatory response in supine/prone positions was 16.5 +/- 6.8 s. After tilts from supine/prone positions toward upright position, time constants decreased and were minimal after tilts to upright position (2.7 +/- 0.7 s).(ABSTRACT TRUNCATED AT 400 WORDS)

Head position dependent adjustment of the three-dimensional human vestibuloocular reflex.

We studied the influence of static head position relative to the rotation axis on the three-dimensional (3-D) vestibuloocular reflex (VOR). By means of a 3-D rotating chair and a 3-D magnetic search-coil system, eye movements were recorded in 6 normal human subjects during sinusoidal rotation about an earth-vertical axis (yaw) with the head positioned at different pitch angles and about an earth-horizontal axis (pitch) with the head positioned at different yaw angles. We confirmed that torsional VOR gain is about 2/3 of horizontal and vertical VOR gain leading to non-collinear axes of eye and head rotation whenever torsional head movement components were present with eye movement axes tilting away from the torsional direction. Despite this non-collinearity of stimulus and eye movement rotation axes there was close to perfect adjustment of the different VOR components depending on the angle between gaze direction and stimulation axis, indicating a vectorial summation of gains obtained for rotations in the major body axes (roll, pitch and yaw). The horizontal and vertical eye movement components followed a cosine function of the angle between the plane of rotation and gaze direction. The torsional component followed a sine function.

Evaluation of the Torsional VOR in Weightlessness

The experimental concept and findings from a recent manned orbital spaceflight are described. Together with ongoing terrestrial and parabolic studies, the present experiment is intended to further our knowledge of the sensory integrative processing of information from the semicircular canals and the otolithic receptors, and to quantify the presumed otolithic adaptation to altered gravito-inertial force environments in a more reliable manner than to date. The experiment included measurement of the basic vestibulo-oculomotor response during active head rotation about each of the three orthogonal axes. Priority was given to the recording of ocular torsion, as elicited by head oscillation about the roll axis, and thus due to the concomitant stimulation of the semicircular canals and otolith receptors. Videooculography was employed for the measurement of eye movements; head movement was measured by three orthogonally arranged angular rate sensors and a triaxial linear accelerometer device. All signals were recorded synchronously on a video/data recorder. Preliminary results indicate alterations in the torsional VOR under zero-g conditions, suggesting an adaptive modification of the torsional VOR gain over the course of the 6-day orbital flight. In addition, the inflight test findings yielded discrepancies between intended and performed head movement, indicating impairment in sensorimotor coordination under prolonged microgravity conditions.

The torsional vestibuloocular reflex can be canceled but not enhanced by visual stimuli.

The torsional vestibuloocular reflex can be canceled but not enhanced by visual stimuli.

The squirrel monkey vestibulo-ocular reflex and adaptive plasticity in yaw, pitch, and roll

The vestibulo-ocular reflex (VOR) was studied in adult squirrel monkeys before and after adaptation to magnifying and minifying viewing conditions. Monkeys were subjected to broadband (0.05-0.71 Hz) conditioning rotation for six hours in head yaw, pitch, and roll on separate occasions, and the VORs in these three planes were studied in darkness to assess adaptive plasticity in the reflexes. The gain of the horizontal VOR (H-VOR) averaged 0.8 across the frequency bandwidth studied (0.025-4 Hz). Phase was near 0 degrees from 4 to around 0.1 Hz, but developed a progressive lead as frequency declined further. Normal vertical VOR (V-VOR) gain climbed from 0.6 at 0.025 Hz to near 1 as frequency increased to 4 Hz. Phase lead was more pronounced at low frequencies than in the H-VOR. The normal torsional VOR (T-VOR) qualitatively resembled the V-VOR, showing similar phase but lower gains (0.3-0.7) across the frequency bandwidth. These findings suggest that the dynamics of the V-VOR and T-VOR resemble canal characteristics more closely than does the H-VOR. After adaptation to visual minification and conditioning rotation (0.5X for yaw and pitch, 0X for roll), gain decreased in each of the planes of conditioning. Similarly, gain increased in the plane of conditioning after adaptation to visual magnification (2X). The adaptive changes were greater at low (0.025-1 Hz) than at high (2.5-4 Hz) frequencies, and were more robust when gain was driven downward than upward. However, control (sham) adaptation experiments showed that VOR gain tended to drop slightly over 6 h in the absence of adaptive drive to do so, suggesting that the gain modifications may be more symmetric when referenced to the control. Adaptive VOR gain enhancement or decrement in the plane of conditioning did not result in systematic and parallel changes in orthogonal VOR planes.

Axes of eye rotation and Listing's law during rotations of the head

1. The vestibuloocular reflex (VOR) was examined in four alert monkeys during rotations of the head about torsional, vertical, horizontal, and intermediate axes. Eye positions and axes were recorded in three dimensions (3-D). Visual targets were used to optimize gaze stabilization. 2. Axes of eye rotation during slow phases showed small but systematic deviations from collinearity with the axes of head rotation. These noncollinearities apparently resulted from vector summation of torsional, vertical, and horizontal VOR components with different gains. 3. VOR gain was lowest about a head-fixed torsional axis that was correlated with the primary gaze direction, as determined by Listing's law for saccades. As a result, rotation of the head about a partially torsional axis produced noncollinear slow phases, with axes that tilted toward Listing's plane. 4. During slow phases, eye position changed not only in the direction of rotation, but also systematically in other directions. Even axes of eye rotation within Listing's plane caused eye position to move out of the plane to a torsional position that was then held. Thus Listing's law for saccades cannot be a product of plant mechanics. 5. VOR slow phases were simulated with the use of a model that incorporated 3-D rotational kinematics into the indirect path and the oculomotor plant. This demonstrated that the observed pattern of position changes is the expected consequence of rotating the eye about a fixed axis and that to hold these positions the indirect path must employ a 3-D velocity-to-position transformation. 6. Quick phases not only corrected the violations of Listing's law produced by slow phases but anticipated them by directing the eye toward a plane rotated in the direction of head rotation. This was modeled by inputting the vestibular signal to a Listing's law operator that is shared by the quick phase and saccadic systems.

The human torsional vestibulo-ocular reflex during rotation about an earth-vertical axis

Using the magnetic search coil technique, we have measured the gain and time constant ( T vor) of the torsional vestibulo-ocular reflex (VOR) in 4 subjects who were rotated about an earth-vertical axis with their necks extended and faces supine. Following a 1-min period of rotation in darkness at 50°/s, the post-rotational response to a velocity off-step had a group mean gain of 0.43 and T vor of 3.7 s. Following a 1-min period of rotation in the light at 50°/s, the post-rotational response indarkness had a group mean gain of 0.29 and T vor of 4.1 s. Following rotation in darkness with the neck flexed and head prone, the post-rotational response, measured in two subjects, had a mean gain of 0.39 and T vor of 5.7. Similar results were obtained with 100°/s stimuli. In all subjects, the gain and T vor of the torsional VOR were smaller than corresponding values for their horizontal VOR; these smaller values can be related to the different visual demands made of the torsional VOR.

Visual cancellation of the torsional vestibulo-ocular reflex in humans.

Using the eye-coil/magnetic field method, we measured the torsional vestibulo-ocular reflex (VOR) in ten subjects during active head rotations in roll at about 0.5 Hz. In the dark, regardless of instructions or mental effort, the gains (eye velocity/head velocity) had a mean value of around 0.61. When they viewed a visual display that was stationary, gains rose to 0.72. When viewing a visual display that moved in roll with their heads, subjects could decrease their gains to a mean of 0.46. Separate experiments showed that, as expected at this frequency, the optokinetic system made only a weak contribution. It has been proposed that the horizontal VOR is cancelled by the smooth pursuit system. Since there is no torsional pursuit system, some other mechanism must be used to augment or partially cancel the torsional VOR. Attempts to show that imagination could change this gain showed only weak effects. When asked to imagine an earth-fixed scene, gains were around 0.63; when asked to imagine a subject-fixed scene, gains decreased to only 0.60. When allowed to use a tactile contribution to aid the imagination in cancelling the VOR, the gain dropped further but only to 0.57. We conclude that mental effort in the dark has little influence on the torsional VOR but vision does by a mechanism that is not optokinetic or pursuit.

Differential visual adaptation of vertical canal-dependent vestibulo-ocular reflexes.

Reversing vision in the horizontal (left-right) plane in humans induces adaptive mechanisms and even reversal of the horizontal vestibulo-ocular reflex (HVOR). The present experiments were aimed at investigating if such adaptive modifications could be observed in the frontal plane by reversal of the torsional visual world movements. Torsional vestibulo-ocular reflex (TVOR) was measured in one subject who wore Dove prisms for 19 days. The gain of TVOR was tested in the dark with the head leaned backward and rotating around an earth vertical axis with sinusoidal rotation (1/6 HZ). The gain decreased from 0.27 to 0.13 at 70 degrees peak-to-peak amplitude, and from 0.3 to 0.11 at 45 degrees peak-to-peak amplitude after 19 days of prism-wearing. Full gain recovery was observed 10 days after prism removal. The results are compared with the observation that in the same situation the vertical VOR (up-down) is not reversed (Dove prisms do not reverse visual images in this plane). As the same four (vertical) canals produce both reflexes, it is suggested that central neuronal mechanisms allow the recognition of the geometrical pattern of visual reversals and selectively adapt the reflex in the relevant planes.