The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey

The aim of this study was to determine if the angular vestibulo-ocular reflex (VOR) in response to pitch, roll, left anterior–right posterior (LARP), and right anterior–left posterior (RALP) head rotations exhibited the same linear and nonlinear characteristics as those found in the horizontal VOR. Three-dimensional eye movements were recorded with the scleral search coil technique. The VOR in response to rotations in five planes (horizontal, vertical, torsional, LARP, and RALP) was studied in three squirrel monkeys. The latency of the VOR evoked by steps of acceleration in darkness (3,000°/s² reaching a velocity of 150°/s) was 5.8±1.7 ms and was the same in response to head rotations in all five planes of rotation. The gain of the reflex during the acceleration was 36.7±15.4% greater than that measured at the plateau of head velocity. Polynomial fits to the trajectory of the response show that eye velocity is proportional to the cube of head velocity in all five planes of rotation. For sinusoidal rotations of 0.5–15 Hz with a peak velocity of 20°/s, the VOR gain did not change with frequency (0.74±0.06, 0.74±0.07, 0.37±0.05, 0.69±0.06, and 0.64±0.06, for yaw, pitch, roll, LARP, and RALP respectively). The VOR gain increased with head velocity for sinusoidal rotations at frequencies 4 Hz. For rotational frequencies 4 Hz, we show that the vertical, torsional, LARP, and RALP VORs have the same linear and nonlinear characteristics as the horizontal VOR. In addition, we show that the gain, phase and axis of eye rotation during LARP and RALP head rotations can be predicted once the pitch and roll responses are characterized.This work was supported by NIH grant R01 DC02390     

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     

Compensation of the human vertical vestibulo-ocular reflex following occlusion of one vertical semicircular canal is incomplete

The vestibulo-ocular reflex (VOR) was studied in nine human subjects 2–15 months after permanent surgical occlusion of one posterior semicircular canal. The stimuli used were rapid, passive, unpredictable, low-amplitude (10–20°), high-acceleration (3000–4000°/s²) head rotations in pitch and yaw planes. The responses measured were vertical and horizontal eye rotations, and the results were compared with those from 19 normal subjects. After unilateral occlusion of the posterior semi-circular canal, the gain of the head-up pitch vertical VOR — the vertical VOR generated by excitation from only one and disfacilitation from two vertical semicircular canals — was reduced to 0.61±0.06 (normal 0.92±0.06) at a head velocity of 200°/s. In contrast the gain of the head-down pitch vertical VOR — the VOR still generated by excitation from two, but disfacilitation from only one vertical semicircular canal — was within normal limits: 0.86±0.11 (normal 0.96±0.04). The gain of the horizontal VOR in response to yaw head rotations — ipsilesion 0.81±0.06 (normal 0.88±0.05) and contralesion 0.80±0.11 (normal 0.92±0.11) — was within normal limits in both directions (group means ± two-tailed 95% confidence intervals given in each case). These results show that occlusion of just one vertical semicircular canal produces a permanent deficit of about 30% in the vertical VOR gain in response to rapid pitch head rotations in the excitatory direction of the occluded canal. This observation indicates that, in response to a stimulus in the higher dynamic range, compensation of the human VOR for the loss of excitatory input from even one vertical semicircular canal is incomplete.     

Torsional and horizontal vestibular ocular reflex adaptation: three-dimensional eye movement analysis

This study used visual-vestibular conflict to effect short-term torsional and horizontal adaptation of the vestibulo-ocular reflex (VOR). Seven normal subjects underwent sinusoidal whole-body rotation about the earth-vertical axis for 40 min (±37°/s, 0.3 Hz) while viewing a stationary radial pattern fixed to the chair (×0 viewing). During adaptation and testing in darkness, the head was pitched either up or down 35° to excite both the horizontal and torsional VOR. The eyes were kept close to zero orbital elevation. Eye movements were recorded with a dual search coil in a three-field magnetic system. VOR gain was determined by averaging peak eye velocity from ten cycles of chair oscillation in complete darkness. The gain of the angular horizontal VOR (response to rotation about the head rostral-caudal axis) was significantly reduced after training in both head orientations. Angular torsional VOR gain (head rotation about the naso-occipital axis) was reduced in both head orientations, but this reached statistical significance only in the head down position. These results suggest that torsional and horizontal VOR gain adaptation, even when elicited together, may be subject to different influences depending upon head orientation. Differences between head up and down could be due to the relatively greater contribution of the horizontal semicircular canals with nose-down pitch. Alternatively, different VOR-adaptation processes could depend on the usual association of the head down posture to near viewing, in which case the torsional VOR is relatively suppressed.     

The effects of head and trunk position on torsional vestibular and optokinetic eye movements in humans

We measured torsional vestibular and optokinetic eye movements in human subjects with the head and trunk erect, with the head supine and the trunk erect, and with the head and trunk supine, in order to quantify the effects of otolithic and proprioceptive modulation. During active head movements, the torsional vestibulo-ocular reflex (VOR) had significantly higher gain with the head upright than with the head supine, indicating that dynamic otolithic inputs can supplement the semicircular canal-ocular reflex. During passive earth-vertical axis rotation, torsional VOR gain was similar with the head and trunk supine and with the head supine and the trunk erect. This finding implies that static proprioceptive information from the neck and trunk has little effect upon the torsional VOR. VOR gain with the head supine was not increased by active, self-generated head movement compared with passive, whole body rotation, indicating that the torsional VOR is not augmented by dynamic proprioceptive inputs or by an efference copy of a command for head movement. Viewing earth-fixed surroundings enhanced the torsional VOR, while fixating a chair-fixed target suppressed the VOR, especially at low frequencies. Torsional optokinetic nystagmus (OKN) evoked by a full-field stimulus had a mean slow-phase gain of 0.22 for 10°/s drum rotation, but gain fell to 0.06 for 80°/s stimuli. Despite this fall in gain, mean OKN slow-phase velocities increased with drum speed, reaching maxima of 2.5°/s–8.0°/s in our subjects. Optokinetic afternystagmus (OKAN) was typically absent. Torsional OKN and OKAN were not modified by otolithic or proprioceptive changes caused by altering head and trunk position with respect to gravity. Torsional velocity storage is negligible in humans, regardless of head orientation.Presented in part at the Society for Neuroscience Annual Meeting, October 31, 1989, Phoenix, AZ     

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.     

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.     

Influence of gravity on cat vertical vestibulo-ocular reflex

Summary The vertical vestibulo-ocular reflex (VOR) was recorded in cats using electro-oculography during sinusoidal angular pitch. Peak stimulus velocity was 50°/s over a frequency range from 0.01 to 4.0 Hz. To test the effect of gravity on the vertical VOR, the animal was pitched while sitting upright or lying on its side. Upright pitch changed the cat's orientation relative to gravity, while on-side pitch did not. The cumulative slow component position of the eye during on-side pitch was less symmetric than during upright pitch. Over the mid-frequency range (0.1 to 1.0 Hz), the average gain of the vertical VOR was 14.5% higher during upright pitch than during on-side pitch. At low frequencies (<0.05 Hz) changing head position relative to gravity raised the vertical VOR gain and kept the reflex in phase with stimulus velocity. These results indicate that gravity-sensitive mechanisms make the vertical VOR more compensatory.     

Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis

Summary Horizontal and vertical eye movements were recorded from cats in response to either a) off-vertical axis rotation (OVAR) at a range of velocities (5–72 deg/s) and a range of tilts (0–60 deg) or b) horizontal (with respect to the cat) optokinetic stimulation (10–80 deg/s), also around a range of tilted axes (0–60 deg). The responses to stopping either of these stimuli were also measured: post-rotatory nystagmus (PRN) following actual rotation, and optokinetic after nystagmus (OKAN) following optokinetic stimulation. The response found during OVAR was a nystagmus with a bias slow-phase velocity that was sinusoidally modulated. The bias was dependent on the tilt and reached 50% of its maximum velocity (maximum was 73±23% of the table velocity) at a tilt of 16 deg. The phase of modulation in horizontal eye velocity bore no consistent relation to the angular rotation. The amplitude of this modulation was roughly correlated with the bias with a slope of 0.13 (deg/s) modulation/(deg/s) bias velocity. There was also a low-velocity vertical bias with the slow-phases upwardly directed. The vertical bias was also modulated and the amplitude depended on the bias velocity (0.27 (deg/s) modulation/ (deg/s) bias velocity). When separated from the canal dependent response, the build up of the OVAR response had a time constant of 5.0±0.8 s. Following OVAR there was no decline in the time constant of PRN which remained at the value measured during earth-vertical axis rotation (EVAR) (6.3±2 s). The peak amplitude of PRN was reduced, dependent on the tilt, reaching only 20% of its EVAR value for a tilt of 20 deg. When a measurable PRN was found, it was accompanied by a slowly-emerging vertical component (time constant 5.4±2s) the effect of which was to vector the PRN accurately onto the earth horizontal. OKN measured about a tilted axis showed no differences in magnitude or direction from EVAR OKN even for tilts as large as 60 deg. OKAN following optokinetic stimulation around a tilted axis appeared normal in the horizontal plane (with respect to the animal) but was accompanied by a slowly emerging (time constant 4.1±2 s) vertical component, the effect of which was to vector the overall OKAN response onto the earth horizontal for tilts less than 20 deg. These results are compared with data from monkey and man and discussed in terms of the involvement of the velocity storage mechanism.     

Habituation and adaptation of the vestibuloocular reflex: a model of differential control by the vestibulocerebellum

Summary We habituated the dominant time constant of the horizontal vestibuloocular reflex (VOR) of rhesus and cynomolgus monkeys by repeated testing with steps of velocity about a vertical axis and adapted the gain of the VOR by altering visual input with magnifying and reducing lenses. After baseline values were established, the nodulus and ventral uvula of the vestibulocerebellum were ablated in two monkeys, and the effects of nodulouvulectomy and flocculectomy on VOR gain adaptation and habituation were compared. The VOR time constant decreased with repeated testing, rapidly at first and more slowly thereafter. The gain of the VOR was unaffected. Massed trials were more effective than distributed trials in producing habituation. Regardless of the schedule of testing, the VOR time constant never fell below the time constant of the semicircular canals (5 s). This finding indicates that only the slow component of the vestibular response, the component produced by velocity storage, was habituated. In agreement with this, the time constant of optokinetic after-nystagmus (OKAN) was habituated concurrently with the VOR. Average values for VOR habituation were obtained on a per session basis for six animals. The VOR gain was adapted by natural head movements in partially habituated monkeys while they wore ×2.2 magnifying or ×0.5 reducing lenses. Adaptation occurred rapidly and reached about ±30%, similar to values obtained using forced rotation. VOR gain adaptation did not cause additional habituation of the time constant. When the VOR gain was reduced in animals with a long VOR time constant, there were overshoots in eye velocity that peaked at about 6–8 s after the onset or end of constant-velocity rotation. These overshoots occurred at times when the velocity storage integrator would have been maximally activated by semicircular canal input. Since the activity generated in the canals is not altered by visual adaptation, this finding indicates that the gain element that controls rapid changes in eye velocity in the VOR is separate from that which couples afferent input to velocity storage. Nodulouvulectomy caused a prompt and permanent loss of habituation, returning VOR time constants to initial values. VOR gain adaptation, which is lost after flocculectomy, was unaffected by nodulouvulectomy. Flocculectomy did not alter habituation of the VOR or of OKAN. Using a simplified model of the VOR, the decrease in the duration of vestibular nystagmus due to habituation was related to a decrement in the dominant time constant of the velocity storage integrator (1/h ₀). Nodulouvulectomy, which reversed habituation, would be effected by decreasing h ₀, thereby increasing the VOR time constant. Small values of h ₀ would cause velocity storage to approach an ideal integrative process, leading the system to become unstable. By controlling the VOR time constant through habituation, the nodulus and uvula can stabilize the slow component of the VOR. VOR gain adaptation was related to a modification of the direct vestibular path gain g ₁, without altering the coupling to velocity storage g ₀ or its time constant (1/h ₀). The mismatched direct- and indirect-pathway gains simulated the overshoots in the dynamic response to a step in velocity, that were observed experimentally. We conclude that independent distributed elements in the VOR modify its dynamic response, under control of separate parts of the vestibulocerebellum.     

Vergence-mediated modulation of the human horizontal vestibulo-ocular reflex is eliminated by a partial peripheral gentamicin lesion

The angular vestibulo-ocular reflex normally has an increased response during vergence on a near target. Surgical unilateral vestibular deafferentation reduces the horizontal vestibulo-ocular reflex (VOR) in response to far target viewing and eliminates this vergence effect. Intratympanic gentamicin treatment reduces VOR gain during far viewing, but the reduction is less severe than that after unilateral vestibular deafferentation. We sought to determine how gentamicin would affect vergence-mediated modulation of the VOR. The VOR in response to passive head impulses in the horizontal plane while viewing a far (124 cm) or near (15 cm) target was evaluated in 11 subjects following intratympanic gentamicin treatment. Three of these subjects had also been tested immediately prior to receiving gentamicin. The impulses were low amplitude (~20°), high velocity (~150°/s), high acceleration (~3,000°/s²) horizontal head rotations administered manually by the investigator. Binocular eye and head velocity were recorded using the scleral search coil technique. The VOR gain was defined as eye velocity divided by inverted head velocity. Prior to intratympanic gentamicin, the VOR gain during rotations to either side was symmetric and showed the same vergence-mediated increase. Following gentamicin, head impulses towards the untreated side yielded VOR gains of 0.91±0.12 while viewing a far target and 1.27±0.22 while viewing a near target, an increase of 33%. Head impulses towards the treated side produced a hypometric VOR with no increase between far and near viewing. The average latency of the VOR was 7.6±2.5 ms towards the untreated side for either near or far viewing and 20.7±13.1 ms towards the treated side for either near or far viewing. Our findings show that a peripheral lesion caused by gentamicin does not ablate the VOR but does eliminate a component of the vestibular signal that is necessary for vergence-mediated modulation of the VOR. Gentamicin has preferential toxicity for the hair cells in the central zone of the crista, where irregular afferents predominate. Our findings are consistent with the hypothesis that irregular afferents provide the necessary signal for vergence-mediated modulation of the VOR.     

Contribution of the maculo-ocular reflex to gaze stability in the rabbit

Summary The contribution of the maculo-ocular reflex to gaze stability was studied in 10 pigmented rabbits by rolling the animals at various angles of sagittal inclination of the rotation and/or longitudinal animal axes. At low frequencies (0.005–0.01 Hz) of sinusoidal stimulation the vestibulo-ocular reflex (VOR) was due to macular activation, while at intermediate and high frequencies it was mainly due to ampullar activation. The following results were obtained: 1) maculo-ocular reflex gain decreased as a function of the cosine of the angle between the rotation axis and the earth's horizontal plane. No change in gain was observed when longitudinal animal axis alone was inclined. 2) At 0° of rotation axis and with the animal's longitudinal axis inclination also set at 0°, the maculo-ocular reflex was oriented about 20° forward and upward with respect to the earth's vertical axis. This orientation remained constant with sagittal inclinations of the rotation and/or longitudinal animal axes ranging from approximately 5° upward to 30° downward. When the longitudinal animal axis was inclined beyond these limits, the eye trajectory tended to follow the axis inclination. In the upside down position, the maculo-ocular reflex was anticompensatory, oblique and fixed with respect to orbital coordinates. 3) Ampullo-ocular reflex gain did not change with inclinations of the rotation and/or longitudinal animal axes. The ocular responses were consistently oriented to the stimulus plane. At intermediate frequencies the eye movement trajectory was elliptic because of directional differences between the ampullo- and maculo-ocular reflexes. 4) In the upright position the coactivation of the optokinetic reflex (OKR) eliminated the eye disalignment with respect to the stimulus plane and the elliptic trajectory. 5) Combined vertical OKR and VOR gain in the prone position (VOKR + VVOR 0°) was higher than that of the combined VOKR + VVOR in the 90° nose up position. The VVOR + VOKR 90° gain was in turn higher than the VVOR + VOKR gain in the 180° upside down position. 6) We suggest that, in the dark, the maculo-ocular response tends to reduce the disalignment of both eyes with respect to the horizon rather than inducing oculocompensatory responses. In the light, this maculo-ocular reflex increases the gain of combined optokinetic and vestibular responses.     

The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation

Latencies of normal and adapted feline vestibulo-ocular reflex (VOR) were studied in five cats by applying ± 20°/s horizontal head velocity steps (4000°/s₂ acceleration) and measuring the elicited horizontal or vertical reflex eye responses. Normal VOR latency was 13.0 ms ± 1.9 SD. Short-term adaptation was then accomplished by using 2 h of paired horizontal sinusoidal vestibular stimulation and phase-synchronized vertical optokinetic stimulation (cross-axis adaptation). For long-term adaptation, cats wore ×0.25 or ×2.2 magnifying lenses for 4 days. The cats were passively rotated for 2 h/day and allowed to walk freely in the laboratory or their cages for the remainder of the time. The latency of the early (primary) adaptive response was 15.2ms±5.2 SD for crossaxis adaptation and 12.5 ms±3.9 SD for lens adaptation. This short-latency response appeared within 30 min after beginning the adaptation procedure and diminished in magnitude overnight. A late (secondary) adaptive response with latency of 76.8 ms±7.0 SD for cross-axis adaptation and 68.1 ms±8.8 SD for lens adaptation appeared after approximately 2 h of adaptation. It had a more gradual increase in magnitude than the primary response and did not diminish in magnitude overnight. These data suggest that brainstem VOR pathways are a site of learning for adaptive VOR modification, since the primary latency is short and has a similar latency to that of the normal VOR.     

Changes in the dynamics of the vertical vestibulo-ocular reflex due to linear acceleration in the frontal plane of the cat

Summary The vertical and horizontal components of the vestibulo-ocular reflex (VOR) were recorded in alert, restrained cats who were placed on their sides and subjected to whole-body rotations in the horizontal plane. The head was either on the axis or 45 cm eccentric from the axis of rotation. During off-axis rotation there was a change in the linear force acting on the otolith organs due to the presence of a centripetal acceleration along the animal's vertical axis. Otolith forces (defined to be opposite to the centripetal acceleration) directed ventrally with respect to the animal (negative) decreased both the amplitude and time constant of the first-order approximation to the slow phase eye velocity of the vertical vestibulo-ocular reflex (VVOR). Otolith forces directed dorsally (positive) increased the amplitude and time constant. The effects were greater for the up VOR. The asymmetry in the VVOR time constant also depended on the otolith forces, being less in the presence of negative otolith forces that caused the resultant otolith force to move ventrally, towards the direction along which gravity normally acts when the animal is in the upright position. The effects of otolith forces on the up VVOR were independent of whether the animals were tested in the dark or in the light with a stationary visual surround (i.e., during visual suppression). In contrast, the changes in the time constant of the down VVOR were smaller during visual suppression. Simulations of the eye velocity storage mechanism suggest that the gain of the feedback in the storage integrator was modified by the angle between the resultant otolith force and an animal-fixed reference. This could be the animal's vertical, i.e., the direction along which gravity normally acts. For larger angles the feedback was less and the amplitude and time constant of the VVOR increased. The transformation of the otolith input was the same for both the up and down VOR, even though the final effect on the eye velocity was asymmetric (larger for up VOR) due to a separate, asymmetric gain element in the velocity storage feedback pathway.     

Combined influence of vergence and eye position on three-dimensional vestibulo-ocular reflex in the monkey

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 degrees vergence and placed at straight ahead, 20 degrees up, down, left, or right during yaw, pitch, and roll head rotations at 1 Hz. The 17 degrees vergence experiments were performed both with and without a structured visual background, the 8.5 degrees vergence experiments with a visual background only. A 40 degrees 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 degrees 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.     

Eye movements during multi-axis whole-body rotations

The semi-circular canals and the otolith organs both contribute to gaze stabilization during head movement. We investigated how these sensory signals interact when they provide conflicting information about head orientation in space. Human subjects were reoriented 90 degrees in pitch or roll during long-duration, constant-velocity rotation about the earth-vertical axis while we measured three-dimensional eye movements. After the reorientation, the otoliths correctly indicated the static orientation of the subject with respect to gravity, while the semicircular canals provided a strong signal of rotation. This rotation signal from the canals could only be consistent with a static orientation with respect to gravity if the rotation-axis indicated by the canals was exactly parallel to gravity. This was not true, so a cue-conflict existed. These conflicting stimuli elicited motion sickness and a complex tumbling sensation. Strong horizontal, vertical, and/or torsional eye movements were also induced, allowing us to study the influence of the conflict between the otoliths and the canals on all three eye-movement components. We found a shortening of the horizontal and vertical time constants of the decay of nystagmus and a trend for an increase in peak velocity following reorientation. The dumping of the velocity storage occurred regardless of whether eye velocity along that axis was compensatory to the head rotation or not. We found a trend for the axis of eye velocity to reorient to make the head-velocity signal from the canals consistent with the head-orientation signal from the otoliths, but this reorientation was small and only observed when subjects were tilted to upright. Previous models of canal-otolith interaction could not fully account for our data, particularly the decreased time constant of the decay of nystagmus. We present a model with a mechanism that reduces the velocity-storage component in the presence of a strong cue-conflict. Our study, supported by other experiments, also indicates that static otolith signals exhibit considerably smaller effects on eye movements in humans than in monkeys.     

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

Summary 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° 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.     

Canal-otolith interactions driving vertical and horizontal eye movements in the squirrel monkey

The vestibulo-ocular reflex (VOR) was studied in three squirrel monkeys subjected to rotations with the head either centered over, or displaced eccentrically from, the axis of rotation. This was done for several different head orientations relative to gravity in order to determine how canal-mediated angular (aVOR) and otolithmediated linear (lVOR) components of the VOR are combined to generate eye movement responses in three-dimensional space. The aVOR was stimulated in isolation by rotating the head about the axis of rotation in the upright (UP), right-side down (RD), or nose-up (NU) orientations. Horizontal and vertical aVOR responses were compensatory for head rotation over the frequency range 0.25–4.0 Hz, with mean gains near 0.9. The horizontal aVOR was relatively constant across the frequency range, while vertical aVOR gains increased with increasing stimulation frequency. In the NU orientation, compensatory torsional aVOR responses were of relatively low gain (0.54) compared with horizontal and vertical responses, and gains remained constant over the frequency range. When the head was displaced eccentrically, rotation provided the same angular stimuli but added linear stimulus components, due to the centripetal and tangential accelerations acting on the head. By manipulating the orientation of the head relative to gravity and relative to the axis of rotation, the lVOR response could be combined with, or isolated from, the aVOR response. Eccentric rotation in the UP and RD orientations generated aVOR and lVOR responses which acted in the same head plane. Horizontal aVOR-lVOR interactions were recorded when the head was in the UP orientation and facing toward (nose-in) or away from (nose-out) the rotation axis. Similarly, vertical responses were recorded with the head RD and in the nose-out or nose-in positions. For both horizontal and vertical responses, gains were dependent on both the frequency of stimulation and the directions and relative amplitudes of the angular and linear motion components. When subjects were positioned nose-out, the angular and linear stimuli produced synergistic interactions, with the lVOR driving the eyes in the same direction as the aVOR. Gains increased with increasing frequency, consistent with an addition of broad-band aVOR and high-pass lVOR components. When subjects were nose-in, angular and linear stimuli generated eye movements in opposing directions, and gains declined with increasing frequency, consistent with a subtraction of the lVOR from the aVOR. This response pattern was identical for horizontal and vertical eye movements. aVOR and lVOR interactions were also assessed when the two components acted in orthogonal response planes. By rotating the monkeys into the NU orientation, the aVOR acted primarily in the roll plane, generating torsional ocular responses, while the translational (lVOR) component generated horizontal or vertical ocular responses, depending on whether the head was oriented such that linear accelerations acted along the interaural or dorsoventral axes, respectively. Horizontal and vertical lVOR responses were negligible at 0.25 Hz and increased dramatically with increasing frequency. Comparison of the combined responses (UP and RD orientations) with the isolated aVOR (head-centered) and lVOR (NU orientation) responses, indicates that these VOR components sum in a linear fashion during complex head motion.     

Interaction between otolith organ and semicircular canal vestibulo-ocular reflexes during eccentric rotation in humans

Controversy remains about the linearity of the interaction between horizontal semicircular canal and otolith organ vestibulo-ocular reflexes (VORs) in the generation of horizontal eye movements during head movements including both rotational and translational components. We used three eccentric rotation techniques to investigate this interaction in human subjects: (1) the tangential interaural acceleration was varied using three head positions (on-axis, 25 and 40 cm ahead of the rotational axis), while angular head velocity remained unchanged; (2) the magnitude of the angular head velocity was varied with head eccentricity to keep the tangential interaural acceleration unchanged; (3) the subject’s head was oriented either upright or 90° forward from upright (nose-down). Experiments were performed in complete darkness with the subjects remembering a close earth-fixed target (20 cm distant) while being rotated at 1.2 and 1.8 Hz. Our data showed that the translational component of the VOR evoked during eccentric yaw rotation increased proportionally with an increase in head eccentricity, i.e. with tangential acceleration. We also found that the translational component of the VOR was equal for motion stimuli producing identical interaural tangential accelerations even when angular velocities differed. In addition, we found that the translational component of the VOR evoked during head upright eccentric rotation was equal to the translational VOR evoked during nose-down rotation for a given stimulus and head eccentricity. We conclude that these three findings are in agreement with what would be expected from a linear interaction (i.e. algebraic summation) between otolith organ and horizontal canal VORs for the generation of horizontal compensatory eye movements during head motion.

Neuronal activity related to vertical eye movement in the region of the interstitial nucleus of Cajal in alert cats

Summary (1) Discharge characteristics of neurons in the region of the interstitial nucleus of Cajal (INC) were studied in alert cats during spontaneous or visually induced eye movement and sinusoidal vertical (pitch) rotation. Activity of a majority of cells (n = 68) was closely related to vertical eye position with or without bursting activity during on-direction saccades. They were called vertical burst-tonic (n = 62) and tonic (n = 6) neurons. Mean discharge rates for individual cells when the eye was near the primary position ranged from 35 to 133 (mean 75) spikes/s with a coefficient of variation (CV) ranging from 0.04 to 0.29 (mean 0.15). Average rate position curves were linear for the great majority of these cells with a mean slope of 3.9 ± 1.2 SD spikes/s/deg. (2) The burst index was defined as the difference in discharge rate between maximal rate during an on-direction saccade and the tonic rate after the saccade. The values of mean burst index for individual cells ranged from 8 to 352 (mean 135) spikes/s. Tonic neurons had a burst index lower than 60 spikes/s and were distributed in the lower end of the continuous histogram, suggesting that burst-tonic and tonic neurons may be a continuous group with varying degrees of burst components. During off-direction saccades, a pause was not always observed, although discharge rate consistently decreased and pauses were seen when saccades were made further in the off-direction toward recruitment thresholds. Significant positive correlation was observed between average discharge rate during off- as well as on-direction saccades and tonic discharge rate after saccades for individual cells, which was not due to cats making saccades mainly from the primary position. (3) During pitch rotation at 0.11 Hz (±10 deg), burst-tonic and tonic neurons had mean phase lag and gain of 128 (±13 SD) deg and 4.2 (±1.7 SD) spikes/s/deg/s² relative to head acceleration. During pitch rotation of a wide frequency range (0.044–0.495 Hz), the values of phase lag were mostly constant (120–140 deg), while simultaneously recorded vertical VOR showed the mean phase lag of 178 deg. Vertical eye position sensitivity and pitch gain (re head position) showed significant positive correlation. (4) Comparison of the discharge characteristics of vertical burst-tonic and tonic neurons with those of secondary vestibulo-ocular neurons (Perlmutter et al. 1988) and extraocular motoneurons (Delgado-Garcia et al. 1986) in alert cats suggests that signals carried by burst-tonic and tonic neurons are partially processed signals in vertical VOR and saccades, and different from oculomotor signals. (5) The INC region also contained many cells that did not belong to the above groups but whose activity was clearly modulated by pitch rotation (called pitch cells for the present study, n = 44). Many (n = 23) showed some correlation with vestibular quick phases, and some (n = 12) with visually elicited eye movement, although they showed significantly lower and more irregular discharge rates than burst-tonic and tonic neurons (mean discharge rate when the eye was near the primary position 34, range 3–91, spikes/s; mean CV 0.61, range 0.15–1.7). During pitch rotation they showed the mean phase lag and gain of 119(±26 SD) deg and 3.2(±2.1 SD) spikes/s/deg/s². Some cells showed a much lower phase lag of about 90 deg. (6) More than half the burst-tonic, tonic and pitch cells tested were antidromically activated by stimuli applied to the ponto-medullary medial longitudinal fasciculus at the level of abducens nucleus, while none of them were activated from the inferior olive, suggesting that vertical eye position signals carried by some burst-tonic and tonic neurons are carried to the lower brainstem.