Otolith-semicircular canal interaction during postrotatory nystagmus in humans

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

The influence of head position and head reorientation on the axis of eye rotation and the vestibular time constant during postrotatory nystagmus

Summary Reorienting the head with respect to gravity during the postrotatory period alters the time course of postrotatory nystagmus (PRN), hastening its decline and thereby reducing the calculated vestibular time constant. One explanation for this phenomenon is that the head reorientation results in a corresponding reorientation of the axis of eye rotation with respect to head coordinates. This possibility was investigated in 10 human subjects whose eye movements were monitored with a three-dimensional magnetic field — search — coil technique using a variety of head reorientation paradigms in a randomized order during PRN following the termination of a 90°/s rotation about earth vertical. Average eye velocities were calculated over two time intervals: from 1 s to 2 s and from 7 s to 8 s after cessation of head rotation. The time constant was estimated as one third of the duration of PRN. For most conditions, a reorientation of the head with respect to gravity 2 s after the rotation had stopped did not significantly alter the direction of the eye velocity vector of PRN with respect to head coordinates. This strongly indicates that, in humans, PRN is mainly stabilized in head coordinates and not in space coordinates, even if the otolith input changes. This finding invalidates the notion that the shortening of PRN due to reorientation of the head could be due to a change of the eye velocity vector towards a direction (torsion), which is not detectable with the eye recording methods (electrooculography) used in earlier studies. The results regarding the vestibular time constant basically confirm earlier findings, showing a strong dependence on static head position, with the time constant being lowest if mainly the vertical canals are stimulated (60° nose up and 90° left ear down). In addition, the time constant was drastically shortened for tilts away from upright. The reduction in vestibular time constant with head reorientation cannot be explained solely on the basis of the dependence of the time constant on static head position. A clear example is provided by head reorientations back towards the upright position, which results in a decrease in the time constant, rather than an increase that would be expected on the basis of static head position.     

Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys

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 degrees, 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 degrees, 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 GABA(B) 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 approximately 90 degrees, 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 degrees /g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0 degrees /g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ~180 degrees 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.     

Nystagmus induced by circular head shaking in normal human subjects

 We recorded three-dimensional eye and head movements during circular, horizontal, vertical, and torsional head shaking in six human subjects with normal vestibular function. With circular head shaking, the stimulation of the canals by the termination of the head movement is similar to that following a step in velocity about the naso-occipital axis. A large torsional nystagmus with slow phase eye velocity of about 20°/s was observed upon cessation of circular head shaking. The three-dimensional eye movements expected from stimulation of the semicircular canals by the head-shaking maneuvers were calculated. The predicted activation of the canals was determined by projecting the head velocity (in head coordinates) into the canal planes and then processing the signal with the transfer function of the canals. The torsional eye velocity components predicted by the stimulation of the canals matched the recorded ones. We observed small horizontal eye velocities that could not be predicted by the stimulation of the canals alone. No eye movements were observed after the end of head shaking about a fixed horizontal or vertical axis. The eye velocities following the termination of head oscillations in the roll plane were small. The analysis methods developed for this study may be useful in the investigation of eye movements elicited by other types of three-dimensional head movements. Received: 24 April 1997 / Accepted: 8 July 1998     

Human 3-D aVOR with and without otolith stimulation

We describe in detail the frequency response of the human three-dimensional angular vestibulo-ocular response (3-D aVOR) over a frequency range of 0.05-1 Hz. Gain and phase of the human aVOR were determined for passive head rotations in the dark, with the rotation axis either aligned with or perpendicular to the direction of gravity (earth-vertical or earth-horizontal). In the latter case, the oscillations dynamically stimulated both the otolith organs and the semi-circular canals. We conducted experiments in pitch and yaw, and compared the results with previously-published roll data. Regardless of the axis of rotation and the orientation of the subject, the gain in aVOR increased with frequency to about 0.3 Hz, and was approximately constant from 0.3 to 1 Hz. The aVOR gain during pitch and yaw rotations was larger than during roll rotations. Otolith and canal cues combined differently depending upon the axis of rotation: for torsional and pitch rotations, aVOR gain was higher with otolith input; for yaw rotations the aVOR was not affected by otolith stimulation. There was a phase lead in all three dimensions for frequencies below 0.3 Hz when only the canals were stimulated. For roll and pitch rotations this phase lead vanished with dynamic otolith stimulation. In contrast, the horizontal phase showed no improvement with additional otolith input during yaw rotations. The lack of a significant otolith contribution to the yaw aVOR was observed when subjects were supine, prone or lying on their sides. Our results confirm studies with less-natural stimuli (off-vertical axis rotation) that the otoliths contribute a head-rotation signal to the aVOR. However, the magnitude of the contribution depends on the axis of rotation, with the gain in otolith-canal cross-coupling being smallest for yaw axis rotations. This could be because, in humans, typical yaw head movements will stimulate the otoliths to a much lesser extent then typical pitch and roll head movements.     

The relation of motion sickness to the spatial–temporal properties of velocity storage

Tilting the head in roll to or from the upright while rotating at a constant velocity (roll while rotating, RWR) alters the position of the semicircular canals relative to the axis of rotation. This produces vertical and horizontal nystagmus, disorientation, vertigo, and nausea. With recurrent exposure, subjects habituate and can make more head movements before experiencing overpowering motion sickness. We questioned whether promethazine lessened the vertigo or delayed the habituation, whether habituation of the vertigo was related to the central vestibular time constant, i.e., to the time constant of velocity storage, and whether the severity of the motion sickness was related to deviation of the axis of eye velocity from gravity. Sixteen subjects received promethazine and placebo in a double-blind, crossover study in two consecutive 4-day test series 1 month apart, termed series I and II. Horizontal and vertical eye movements were recorded with video-oculography while subjects performed roll head movements of approx. 45° over 2 s to and from the upright position while being rotated at 138°/s around a vertical axis. Motion sickness was scaled from 1 (no sickness) to an endpoint of 20, at which time the subject was too sick to continue or was about to vomit. Habituation was determined by the number of head movements that subjects made before reaching the maximum motion sickness score of 20. Head movements increased steadily in each session with repeated testing, and there was no difference between the number of head movements made by the promethazine and placebo groups. Horizontal and vertical angular vestibulo-ocular reflex (aVOR) time constants declined in each test, with the declines being closely correlated to the increase in the number of head movements. The strength of vertiginous sensation was associated with the amount of deviation of the axis of eye velocity from gravity; the larger the deviation of the eye velocity axis from gravity, the more severe the motion sickness. Thus, promethazine neither reduced the nausea associated with RWR, nor retarded or hastened habituation. The inverse relationship between the aVOR time constants and number of head movements to motion sickness, and the association of the severity of motion sickness with the extent, strength, and time of deviation of eye velocity from gravity supports the postulate that the spatiotemporal properties of velocity storage, which are processed between the nodulus and uvula of the vestibulocerebellum and the vestibular nuclei, are likely to represent the source of the conflict responsible for producing motion sickness.     

Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex

The nodulus and sublobule d of the uvula of rhesus and cynomolgus monkeys were electrically stimulated with short trains of pulses to study changes in horizontal slow-phase eye velocity. Nodulus and uvula stimulation produced a rapid decline in horizontal slow phase velocity, one aspect of the spatial reorientation of the axis of eye rotation that occurs when the head is tilted with regard to gravity during per- and post-rotatory nystagmus and optokinetic after-nystagmus (OKAN). Nodulus and uvula stimulation also reproduced the reduction of the horizontal time constant of post-rotatory nystagmus and OKAN that occurs during visual suppression. The brief electric stimuli (4–5 s) induced little slow-phase velocity and had no effect on the initial jump in eye velocity at the onset or the end of angular rotation. Effects of stimulation were unilateral, suggesting specificity of the output pathways. Activation of more caudal sites in the uvula produced nystagmus with a rapid rise in eye velocity, but the effects did not outlast the stimulus and did not affect VOR or OKAN time constants. Thus, stimulation of caudal parts of the uvula did not affect eye velocity produced by velocity storage. We postulate that the nodulus and sublobule d of the uvula control the time constant of the yaw axis (horizontal) component of slow-phase eye velocity produced by velocity storage.     

Nystagmus induced by off-vertical rotation axis in the cat

Summary 1) In the alert cat, nystagmus induced by off-vertical axis rotation (OVAR) was recorded following steps in head velocity or ramps of velocity at constant acceleration below canal threshold. Dependence of nystagmus characteristics on tilt angle of rotation axis and head velocity was studied. Similar results were obtained with both types of stimulation. 2) Mean and modulation amplitude of horizontal eye velocity increased with tilt angle in the range 0–30 degrees. 3) Both variables increased also with head velocity, but with different trends, probably because they are set by different mechanisms. When head rotational velocity was increased above 80°/s, mean eye velocity progressively decreased to zero. 4) In spite of variations from one animal to another, some regularity was observed in the phase of eye velocity modulation. In several cases, a reduction in phase lead of eye velocity with respect to conventional origin of phases (nose-down position) was observed when head velocity increased. 5) Time constant of post-OVAR nystagmus decreased with the tilt angle of the rotation axis from gravity, but not with the orientation of the head with respect to rotation axis. 6) The results could be accounted for by a general equation describing the vestibulo-ocular reflex, provided that estimates of kinematic variables of head movement (head rotational and translational velocities), and visual target distance could be computed by the Central Nervous System.     

Adaptation of the angular vestibulo-ocular reflex to head movements in rotating frames of reference

Head movements in a rotating frame of reference are commonly encountered, but their long term effects on the angular vestibulo-ocular reflex (aVOR) are not well understood. To study this, monkeys were oscillated about a naso-occipital (roll) axis for several hours while rotating about a spatial vertical axis (roll-while-rotating, RWR). This induced oscillations in roll and pitch eye velocity and continuous horizontal (yaw) nystagmus. For several hours thereafter, simple roll in darkness induced horizontal nystagmus and pitch and roll oscillations. The rising and falling time constants of the horizontal velocity indicated that the nystagmus arose in velocity storage. The continuous nystagmus was correlated with a phase shift of vertical eye velocity from 90° to 0° re head position. As the phases reverted toward pre-adaptive values, the horizontal velocity declined. Similar yaw nystagmus and pitch and roll velocities were produced by oscillation in roll after adaptation with roll and horizontal optokinetic nystagmus (OKN), but not after adaptation with pitch-while-rotating (PWR). Findings were explained by a model that shifted the roll orientation vector of velocity storage toward the pitch axis during adaptation with RWR and Roll & OKN. This shift produced modulation in vertical eye velocity in the post adaptive state, which was approximately in phase with roll head position, generating horizontal nystagmus. Similar orientation changes to prolonged exposure to complex motion environments may be responsible for producing post-stimulus motion sickness and/or mal de debarquement. Supported by DC007847, EY04148, DC05204, EY01867, DC05222.     

Spatial orientation of caloric nystagmus in semicircular canal-plugged monkeys

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 ( approximately 20 degrees 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.     

Eye-position dependence of three-dimensional ocular rotation-axis orientation during head impulses in humans

 If horizontal saccades or smooth-pursuit eye movements are made with the line-of-sight at different elevations, the three-dimensional (3D) angular rotation axis of the globe tilts by half the vertical eye eccentricity. This phenomenon is named ”half-angle rule” and is a consequence of Listing’s law. It was recently found that the ocular rotation axis during the horizontal vestibulo-ocular reflex (VOR) on a turntable also tilts in the direction of the line-of-sight by about a quarter of the eye’s vertical eccentricity. This is surprising, since, in a ”perfect” VOR, the angular rotation axis of the eye should be independent from the position of the eye to fully compensate for the 3D angular head rotation. We asked whether this quarter-angle strategy is a general property of the VOR or whether the 3D kinematics of ocular movements evoked by vestibular stimulation would be less eye-position dependent at higher stimulus frequencies. Nine healthy subjects were exposed to horizontal head impulses (peak velocity ∼250°/s). The line-of-sight was systematically changed along the vertical meridian of a tangent screen. Three-dimensional eye and head movements were monitored with dual search coils. The 3D orientation of the angular eye-in-head rotation axis was determined by calculating the average angular velocity vectors of the initial 10° displacements. Then, the difference between the tilt angles of the ocular rotation axis during upward and downward viewing was determined and divided by the difference of vertical eccentricity (”tilt angle coefficient”). Control experiments included horizontal saccades, smooth-pursuit eye movements, and eye movements evoked by slow, passive head rotations at the same vertical eye eccentricities. On average, the ocular rotation axis during horizontal head-impulse testing at different elevations of the line-of-sight was closely aligned with the rotation axis of the head (tilt angle coefficient of pooled abducting and adducting eye movements: 0.11±0.17 SD). Values for slow head impulses, however, exceeded somewhat the quarter angle (0.33±0.12), while smooth-pursuit movements (0.50±0.09) and saccades (0.44±0.11) were closest to the half angle. These results demonstrate that the 3D orientation of the ocular rotation axis during rapid head thrusts is relatively independent of the direction of the line-of-sight and that ocular rotations elicited by head impulses are kinematically different from saccades, despite similar movement dynamics. Received: 17 July 1998 / Accepted: 17 May 1999     

Three-dimensional organization of vestibular-related eye movements to off-vertical axis rotation and linear translation in pigeons

During linear accelerations, compensatory reflexes should continually occur in order to maintain objects of visual interest as stable images on the retina. In the present study, the three-dimensional organization of the vestibulo-ocular reflex in pigeons was quantitatively examined during linear accelerations produced by constant velocity off-vertical axis yaw rotations and translational motion in darkness. With off-vertical axis rotations, sinusoidally modulated eye-position and velocity responses were observed in all three components, with the vertical and torsional eye movements predominating the response. Peak torsional and vertical eye positions occurred when the head was oriented with the lateral visual axis of the right eye directed orthogonal to or aligned with the gravity vector, respectively. No steady-state horizontal nystagmus was obtained with any of the rotational velocities (8–58°/s) tested. During translational motion, delivered along or perpendicular to the lateral visual axis, vertical and torsional eye movements were elicited. No significant horizontal eye movements were observed during lateral translation at frequencies up to 3 Hz. These responses suggest that, in pigeons, all linear accelerations generate eye movements that are compensatory to the direction of actual or perceived tilt of the head relative to gravity. In contrast, no translational horizontal eye movements, which are known to be compensatory to lateral translational motion in primates, were observed under the present experimental conditions. Received: 29 January 1999 / Accepted: 14 June 1999     

Eye movements induced by off-vertical axis rotation (OVAR) at small angles of tilt

Summary Off-vertical rotation (OVAR) in darkness induced continuous horizontal nystagmus in humans at small tilts of the rotation axis (5 to 30 degrees). The horizontal slow eye velocity had two components: a mean velocity in the direction opposite to head rotation and a sinusoidal modulation around the mean. Mean velocity generally did not exceed 10 deg/s, and was less than or equal to the maximum velocity of optokinetic after-nystagmus (OKAN). Both the mean and modulation components of horizontal nystagmus increased with tilt angle and rotational velocity. Vertical slow eye velocity was also modulated sinusoidally, generally around zero. The amplitude of the vertical modulation increased with tilt angle, but not with rotational velocity. In addition to modulations in eye velocity, there were also modulations in horizontal and vertical eye positions. These would partially compensate for head position changes in the yaw and pitch planes during each cycle of OVAR. Modulations in vertical eye position were regular, increased with increases in tilt angle and were separated from eye velocity by 90 deg. These results are compatible with the interpretation that, during OVAR, mean slow velocity of horizontal nystagmus is produced by the velocity storage mechanism in the vestibular system. In addition, they indicate that the otolith organs induce compensatory eye position changes with regard to gravity for tilts in the pitch, yaw and probably also the roll planes. Such compensatory changes could be utilized to study the function of the otolith organs. A functional interpretation of these results is that nystagmus attempts to stabilize the image on the retina of one point of the surrounding world. Mean horizontal velocity would then be opposite to the estimate of head rotational velocity provided by the output of the velocity storage mechanism, as charged by an otolithic input during OVAR. In spite of the lack of actual translation, an estimate of head translational velocity could, in this condition, be constructed from the otolithic signal. The modulation in horizontal eye position would then be compensatory for the perceived head translation. Modulation of vertical eye velocity would compensate for actual changes in head orientation with respect to gravity.     

Velocity storage in the human vertical rotational vestibulo-ocular reflex

Human horizontal rotational vestibulo-ocular reflex (rVOR) has been extensively investigated: the horizontal semicircular canals sense yaw rotations with high-pass filter dynamics and a time constant (TC) around 5 s, yet the rVOR response shows a longer TC due to a central processing stage, known as velocity storage mechanism (VSM). It is generally assumed that the vertical rVOR behaves similarly to the horizontal one; however, VSM processing of the human vertical rVOR is still to be proven. We investigated the vertical rVOR in eight healthy human subjects using three experimental paradigms: (1) per- and post-rotatory around an earth-vertical axis (ear down rotations, EDR), (2) post-rotatory around an earth-horizontal axis with different stopping positions (static otolith stimulation), (3) per-rotatory around an earth-horizontal axis (dynamic otolith stimulation). We found that the TC of vertical rVOR responses ranged 3–10 s, depending both on gravity and on the direction of rotation. The shortest TC were found in response to post-rotatory earth-horizontal stimulation averaging 3.6 s, while they were prolonged in EDR stimulation, i.e. when the head angular velocity vector is aligned with gravity, with a mean value of about 6.0 s. Overall, the longest TC were observed in per-rotatory earth-horizontal stimulation, averaging 7.8 s. The finding of longer TC in EDR than in post-rotatory earth-horizontal stimulation indicates a role for the VSM in the vertical rVOR, although its contribution appears to be weaker than on the horizontal rVOR and may be directionally asymmetric. The results from per-rotatory earth-horizontal stimulation, instead, imply a role for the otoliths in controlling the duration of the vertical rVOR response. We found no reorientation of the response toward earth horizontal, indicating a difference between human and monkey rVOR.     

Angular velocity detection by head movements orthogonal to the plane of rotation

Sinusoidal oscillation of rhesus monkeys about a head-fixed, earth-horizontal axis while rotating at constant velocity about an earth-vertical axis generates a characteristic ocular nystagmus where the three-dimensional slow phase eye velocity is compensatory to the spatially and temporally changing head angular velocity vector. This includes the generation of a unidirectional nystagmus characterised by a bias slow phase velocity component, albeit of small gain (0.2–0.7), that persists for the duration of the combined two-axes stimulation and is compensatory to the constant velocity earth-vertical axis rotation. Specifically, there is a torsional bias velocity in supine position, a vertical bias velocity in ear down position and a horizontal bias velocity in upright position. Since the semicircular canals can not sense prolonged constant velocity rotation, the ocular bias velocity must be centrally constructed from canal afferent signals using head position information. Thus, optimal performance of the vestibular system as a three-dimensional rate sensor relies on afferent information from both the semicircular canals and the otolith organs.     

Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation.

Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation. Interaction of the horizontal linear and angular vestibuloocular reflexes (lVOR and aVOR) was studied in rhesus and cynomolgus monkeys during centered rotation and off-center rotation at a constant velocity (centrifugation). During centered rotation, the eye velocity vector was aligned with the axis of rotation, which was coincident with the direction of gravity. Facing and back to motion centrifugation tilted the resultant of gravity and linear acceleration, gravito-inertial acceleration (GIA), inducing cross-coupled vertical components of eye velocity. These components were upward when facing motion and downward when back to motion and caused the axis of eye velocity to reorient from alignment with the body yaw axis toward the tilted GIA. A major finding was that horizontal time constants were asymmetric in each monkey, generally being longer when associated with downward than upward cross coupling. Because of these asymmetries, accurate estimates of the contribution of the horizontal lVOR could not be obtained by simply subtracting horizontal eye velocity profiles during facing and back to motion centrifugation. Instead, it was necessary to consider the effects of GIA tilts on velocity storage before attempting to estimate the horizontal lVOR. In each monkey, the horizontal time constant of optokinetic after-nystagmus (OKAN) was reduced as a function of increasing head tilt with respect to gravity. When variations in horizontal time constant as a function of GIA tilt were included in the aVOR model, the rising and falling phases of horizontal eye velocity during facing and back to motion centrifugation were closely predicted, and the estimated contribution of the compensatory lVOR was negligible. Beating fields of horizontal eye position were unaffected by the presence or magnitude of linear acceleration during centrifugation. These conclusions were evaluated in animals in which the low-frequency aVOR was abolished by canal plugging, isolating the contribution of the lVOR. Postoperatively, the animals had normal ocular counterrolling and horizontal eye velocity modulation during off-vertical axis rotation (OVAR), suggesting that the otoliths were intact. No measurable horizontal eye velocity was elicited by centrifugation with angular accelerations 相似文献   

Influence of eye and head position on the vestibulo-ocular reflex

Summary For the vestibulo-ocular reflex (VOR) to function properly, namely to ensure a stable retinal image under all circumstances, it should be able to take into account varying eye positions in the orbit and varying orientations of the head with respect to the axis about which it is rotating. We tested this capability by quantifying the gain and the time constant of the horizontal component of the VOR during rotation about an earth vertical axis when the line of sight (optical axis) was moved out of the plane of head rotation — either by rotating the eyes up or down in the orbit or by pitching the head up or down with respect to earth-horizontal. In either case the gain of the horizontal component of the VOR was attenuated precisely by the cosine of the angle made between the optical axis and the plane of head rotation. Furthermore, if the head was pitched up or down but the eye rotated oppositely in the orbit so as to keep the line of sight in the plane of head rotation the gain of the horizontal component of the VOR was the same value as with the head and eyes both straight ahead. In contrast, the time constant of the VOR varied only as a function of the orientation of the head and not as a function of eye position in the orbit. During rotation about an earth vertical axis, the time constant was longest (about 18 s) when the head was pitched forward to place the lateral canals near earth-horizontal and shortest (about 11 s) when the head was pitched backward to place the vertical canals near earth-horizontal. Finally, since during rotation in yaw the pattern of stimulation of the lateral and vertical semicircular canals varies with different head orientations one can use measurements of the horizontal component of the VOR, under varying degrees of pitch of the head, to calculate the relative ability of the lateral and vertical semicircular canals to transduce head velocity.Dr. Fetter is a visiting scientist from the Neurologische Universitätsklinik, Eberhard-Karls-Universität, Liebermeisterstr. 18-20, D-7400 Tübingen, Federal Republic of Germany     

Spatial properties of central vestibular neurons

We studied the spatial characteristics of 45 vestibular-only (VO) and 12 vestibular-plus-saccade (VPS) neurons in two cynomolgus monkeys using angular rotation and static tilt. The purpose was to determine the contribution of canal and otolith-related inputs to central vestibular neurons whose activity is associated with the central velocity storage integrator. Lateral canal-related neurons responded maximally during vertical axis rotation when the head was tilted 25 +/- 6 and 22 +/- 3 degrees forward relative to the axis of rotation in the two animals, and vertical canal-related neurons responded maximally with the head tilted back 63+/- 5 and 57 +/- 7 degrees . The origin of the vertical canal-related input was verified by rotation about a spatial horizontal axis. Thirty-one percent of cells received input in a single canal plane. Sixty-seven percent of canal-related cells received otolith input, 31% of vertical canal neurons had lateral canal input, and 43% of lateral canal neurons had vertical canal input. Twenty percent of neurons had convergent input from the lateral canals, the vertical canals, and the otolith organs. Some VO and VPS cells had spatial-temporal convergent (STC) properties; more of these cells had STC properties at lower frequencies of rotation. Thus VO and VPS neurons associated with velocity storage receive a broad range of convergent inputs from each portion of the vestibular labyrinth. This convergence could provide the basis for gravity-dependent eye velocity orientation induced through velocity storage.     

The effect of gravity on the horizontal and vertical vestibulo-ocular reflex in the rat

Horizontal and vertical eye movements were recorded in alert pigmented rats using chronically implanted scleral search coils or temporary glue-on coils to test the dependence of the vestibulo-ocular reflex (VOR) upon rotation axis and body orientation. The contributions of semicircular-canal versus otolith-organ signals to the VOR were investigated by providing canal-only (vertical axis) and canal plus otolith (horizontal axis) stimulation conditions. Rotations that stimulated canals only (upright yaw and nose-up roll) produced an accurate VOR during middle- and high-frequency rotations (0.2-2 Hz). However, at frequencies below 0.2 Hz, the canal-only rotations elicited a phase-advanced VOR. The addition of a changing gravity stimulus, and thus dynamic otolith stimulation, to the canal signal (nose-up yaw, on-side yaw, and upright roll) produced a VOR response with accurate phase down to the lowest frequency tested (0.02 Hz). In order to further test the dependence of the VOR on gravitational signals, we tested vertical VOR with the head in an inverted posture (inverted roll). The VOR in this condition was advanced in phase across all frequencies tested. At low frequencies, the VOR during inverted roll was anticompensatory, characterized by slow-phase eye movement in the same direction as head movement. The substantial differences between canalonly VOR and canal plus otolith VOR suggest an important role of otolith organs in rat VOR. Anticompensatory VOR during inverted roll suggests that part of the otolith contribution arises from static tilt signals that are inverted when the head is inverted.     

Vertical divergence and counterroll eye movements evoked by whole-body position steps about the roll axis of the head in humans

In healthy human subjects, a head tilt about its roll axis evokes a dynamic counterroll that is mediated by both semicircular canal and otolith stimulation, and a static counterroll that is mediated by otolith stimulation only. The vertical ocular divergence associated with the static counterroll too is otolith-mediated. A previous study has shown that, in humans, there is also a vertical divergence during dynamic head roll, but this report was not conclusive on whether this response was mediated by the semicircular canals only or whether the otoliths made a significant contribution. To clarify this issue, we applied torsional whole-body position steps (amplitude 10 degrees, peak acceleration of 90 degrees /s(2), duration 650 ms) about the earth-vertical (supine body position) and earth-horizontal (upright body position) axis to healthy human subjects who were monocularly fixating a straight-ahead target. Eye movements were recorded binocularly with dual search coils in three dimensions. The dynamic parameters were determined 120 ms after the beginning of the turntable movement, i.e., before the first fast phase of nystagmus. The static parameters were measured 4 s after the beginning of the turntable movement. The dynamic gain of the counterroll was larger in upright (average gain: 0.48 +/- 0.10 SD) than in supine (0.36 +/- 0.10) position. The static gain of the counterroll in the upright position (0.21 +/- 0.06) was smaller than the dynamic gain. Divergent eye movements (intorting eye hypertropic) evoked during the dynamic phase were not significantly different between supine (average vergence velocity: 0.87 +/- 0.51 degrees /s) and upright (0.84 +/- 0.64 degrees /s) positions. The static vertical divergence in upright position was 0.32 +/- 0.14 degrees. The results indicate that the dynamic vertical divergence in contrast to the dynamic ocular counterroll is not enhanced by otolith input. These results can be explained through the different patterns of connectivity between semicircular canals and utricles to the eye muscles. Alternatively, we hypothesize that the small dynamic vertical divergence represents the remaining vertical error necessary to drive an adaptive control mechanism that normally maintains a vertical eye alignment.