Translational motion perception and vestiboocular responses in the absence of non-inertial cues.

Path integration studies in humans show that we have the ability to accurately reproduce our path in the absence of visual information. It has been suggested that this ability is supported by acceleration signals, as transduced by the otolith organs, which may then be integrated twice to produce path excursion. Vestibuloocular responses to linear translations (LVOR), however, show considerable frequency dependence, with substantial attenuation in response to low frequency translational motion. If otolith information were processed similarly by path integration mechanisms, the resulting signal would not be sufficient to account for robust path integration for stimuli typically used in such studies. We hypothesized that such behavior relies upon cognitive skill and transient otolith cues, typically combined with non-directional cues of motion, such as vibration and noise produced by the mechanics apparatus used to produce linear motion. Continuous motion estimation tasks were used to assess translation perception, while eye movement recordings revealed LVOR responses, in 12 normal and 2 vestibulopathic human subjects while riding on a sled designed to specifically minimize non-directional motion cues. In the near absence of such cues, perceptual responses, like the LVOR, showed high-pass characteristics. This implies that otolith signals are not sufficient to support previously observed path integration behaviors, which must be supplemented by non-directional motion cues.

Multiple sensory cues underlying the perception of translation and path.

The translational linear vestibuloocular reflex compensates most accurately for high frequencies of head translation, with response magnitude decreasing with declining stimulus frequency. However, studies of the perception of translation typically report robust responses even at low frequencies or during prolonged motion. This inconsistency may reflect the incorporation of nondirectional sensory information associated with the vibration and noise that typically accompany translation, into motion perception. We investigated the perception of passive translation in humans while dissociating nondirectional cues from actual head motion. In a cue-dissociation experiment, interaural (IA) motion was generated using either a linear sled, the mechanics of which generated noise and vibration cues that were correlated with the motion profile, or a multiaxis technique that dissociated these cues from actual motion. In a trajectory-shift experiment, IA motion was interrupted by a sudden change in direction (+/-30 degrees diagonal) that produced a change in linear acceleration while maintaining sled speed and therefore mechanical (nondirectional) cues. During multi-axis cue-dissociation trials, subjects reported erroneous translation perceptions that strongly reflected the pattern of nondirectional cues, as opposed to nearly veridical percepts when motion and nondirectional cues coincided. During trajectory-shift trials, subjects' percepts were initially accurate, but erroneous following the direction change. Results suggest that nondirectional cues strongly influence the perception of linear motion, while the utility of cues directly related to translational acceleration is limited. One key implication is that "path integration" likely involves complex mechanisms that depend on nondirectional and contextual self-motion cues in support of limited and transient otolith-dependent acceleration input.

Linearity of canal-otolith interaction during eccentric rotation in humans.

During natural behavior, the head may simultaneously undergo rotation, transduced by the semicircular canals, and translation, transduced by the otolith organs. It has been demonstrated in monkey that the vestibulo-ocular reflexes (VORs) elicited by both endorgans (i.e., the angular and linear VORs, or AVOR and LVOR) sum linearly during combined rotation and translation, but this finding has proven more elusive in humans. To investigate the combined AVOR/LVOR response, six human subjects underwent yaw eccentric rotation at 3 Hz in darkness while displaced from the axis of rotation. Responses to on-center yaw rotation (AVOR alone) and interaural translation (LVOR alone) were also recorded. During eccentric rotation with the subject facing away from the axis of rotation (i.e., nose out), in which a yaw to the right occurs simultaneously with a translation to the right (i.e., translation in phase with rotation), the AVOR and LVOR acted synergistically. Responses were always out of phase with rotation, and became larger in magnitude as vergence increased. For nose-in eccentric rotation, during which translation is out of phase with rotation, the LVOR acted antagonistically to the AVOR. During near viewing, the LVOR often dominated the overall response when eccentricity was sufficiently large, producing eye movements that were in phase with the rotational stimuli. As vergence decreased, the LVOR influence diminished, eventually resulting in responses that were out of phase with rotation at lowest vergence. When the response to pure yaw rotation was vectorially removed from the responses to eccentric rotation, the results proved statistically indistinguishable from the LVOR recorded during interaural translation, suggesting that the ocular response to combined angular and linear motion reflects the linear combination of the AVOR and LVOR.

Characteristics of the VOR in response to linear acceleration.

The primate linear VOR (LVOR) includes two forms. First, eye-movement responses to translation [e.g., horizontal responses to interaural (i.a.) motion] help maintain binocular fixation on targets, and therefore a stable bifoveal image. The translational LVOR is strongly modulated by fixation distance, and operates with high-pass dynamics (> 1 Hz). Second, other LVOR responses occur that cannot be compensatory for translation and instead seem compensatory for head tilt. This reflects an otolith response ambiguity--that is, an inability to distinguish head translation from head tilt relative to gravity. Thus, ocular torsion is appropriately compensatory for head roll-tilt, but also occurs during IA translation, since both stimuli entail IA acceleration. Unlike the IA-horizontal response, IA torsion behaves with low-pass dynamics (with respect to "tilt"), and is uninfluenced by fixation distance. Interestingly, roll-tilt, like IA translation, also produces both horizontal (a translational reflex) and torsional (a tilt reflex) responses, further emphasizing the ambiguity problem. Early data from subjects following unilateral labyrinthectomy, which demonstrates a general immediate decline in translational LVOR responses, are also presented, followed by only modest recovery over several months. Interestingly, the usual high-pass dynamics of these reflexes shift to an even higher cutoff. Both eyes respond roughly equally, suggesting that unilateral otolith input generates a binocularly symmetric LVOR.

Adaptive plasticity in the naso-occipital linear vestibulo-ocular reflex.

The linear vestibulo-ocular reflex (LVOR) during motion along the naso-occipital (NO) axis is governed by eye position and viewing distance. These influences are necessary for the LVOR to maintain stable foveal images during head translation. The response to NO translation must be large when eye position is eccentric from the axis of head motion (i.e., during lateral gaze) and must diminish as eye position approaches straight-ahead, eventually reaching zero when the eye is aligned with the NO axis of motion (the "null point"). As eye position crosses to the opposite side, the LVOR response must reappear, but in the opposite direction, and must grow in magnitude as eccentricity increases. To determine whether the NO-LVOR is subject to adaptive plastic mechanisms, squirrel monkeys were conditioned during NO translation while they binocularly viewed a rich visual field through parallel base-right or base-left wedge prisms. This optical method effectively shifted the visual world 9 degrees leftward or rightward, respectively, thus inducing a mismatch between vision and the NO-LVOR during head movements. To restore compensatory function, the relationship between LVOR sensitivity and horizontal eye position must shift by 9 degrees in the same direction as the visual image shift, effectively shifting the null point. After 2 h of adaptive conditioning, all monkeys exhibited an adaptive shift in the appropriate direction by an average of 3.0 degrees (range 0.7-5.0 degrees), corresponding to 33% of the geometrically required adaptation.

Human vestibuloocular reflex and its interactions with vision and fixation distance during linear and angular head movement.

Human vestibuloocular reflex and its interactions with vision and fixation distance during linear and angular head movement. J. Neurophysiol. 80: 2391-2404, 1998. The vestibuloocular reflex (VOR) maintains visual image stability by generating eye movements that compensate for both angular (AVOR) and linear (LVOR) head movements, typically in concert with visual following mechanisms. The VORs are generally modulated by the "context" in which head movements are made. Three contextual influences on VOR performance were studied during passive head translations and rotations over a range of frequencies (0.5-4 Hz) that emphasized shifting dynamics in the VORs and visual following, primarily smooth pursuit. First, the dynamic characteristics of head movements themselves ("stimulus context") influence the VORs. Both the AVOR and LVOR operate with high-pass characteristics relative to a head velocity input, although the cutoff frequency of the AVOR (<0.1 Hz) is far below that of the LVOR ( approximately 1 Hz), and both perform well at high frequencies that exceed, but complement, the capabilities of smooth pursuit. Second, the LVOR and AVOR are modulated by fixation distance, implemented with a signal related to binocular vergence angle ("fixation context"). The effect was quantified by analyzing the response during each trial as a linear relationship between LVOR sensitivity (in deg/cm), or AVOR gain, and vergence (in m-1) to yield a slope (vergence influence) and an intercept (response at 0 vergence). Fixation distance (vergence) was modulated by presenting targets at different distances. The response slope rises with increasing frequency, but much more so for the LVOR than the AVOR, and reflects a positive relationship for all but the lowest stimulus frequencies in the AVOR. A third influence is the context of real and imagined targets on the VORs ("visual context"). This was studied in two ways-when targets were either earth-fixed to allow visual enhancement of the VOR or head-fixed to permit visual suppression. The VORs were assessed by extinguishing targets for brief periods while subjects continued to "fixate" them in darkness. The influences of real and imagined targets were most robust at lower frequencies, declining as stimulus frequency increased. The effects were nearly gone at 4 Hz. These properties were equivalent for the LVOR and AVOR and imply that the influences of real and imagined targets on the VORs generally follow low-pass and pursuit-like dynamics. The influence of imagined targets accounts for roughly one-third of the influence of real targets on the VORs at 0.5 Hz.

Canal-otolith interactions in the squirrel monkey vestibulo-ocular reflex and the influence of fixation distance.

Natural head movements include angular and linear components of motion. Two classes of vestibulo-ocular reflex (VOR), mediated by the semicircular canals and otoliths (the angular and linear VOR, or AVOR and LVOR, respectively), compensate for head movements and help maintain binocular fixation on targets in space. In this study, AVOR/LVOR interactions were quantified during complex head motion over a broad range of fixation distances at a fixed stimulus frequency of 4.0 Hz. Binocular eye movements were recorded (search-coil technique) in squirrel monkeys while fixation distance (assessed by vergence) was varied using brief presentations of earth-fixed targets at various distances. Stimuli consisted of rotations around an earth-vertical axis and therefore always activated the AVOR. Horizontal and vertical AVORs were assessed when the head was centered over the axis of rotation and oriented upright (UP) and right-side-down (RD), respectively. AVOR gains increased slightly with increasing vergence in darkness, as expected given the small anterior position of the eyes in the head. Combined AVOR/LVOR responses were recorded when subjects were displaced eccentrically from the rotation axis. Eccentric rotations activated the AVOR just as when the head was centered, but added a translational stimulus which generated an LVOR component in response to interaural (IA) or dorsoventral (DV) tangential accelerations, depending on whether the head was UP or RD, respectively. When the head was eccentric and facing nose-out, the AVOR and LVOR produced ocular responses in the same plane and direction (coplanar and synergistic), and response magnitudes increased with increasing vergence. With the head facing nose-in, AVOR and LVOR response components were oppositely directed (coplanar and antagonistic). The AVOR dominated the response when fixation distance was far, and phase was compensatory for head rotation. As fixation distance decreased toward the rotation axis, responses declined to near zero, and when fixation distance approached even closer, the LVOR component dominated and response phase inverted. The same pattern was observed for both horizontal (head UP) and vertical (head RD) responses. The LVOR was recorded directly by rotating subjects eccentrically but in the nose-up (NU) orientation. The AVOR then generated torsional responses to head roll, coexistent with either horizontal or vertical LVOR responses to tangential acceleration when the subject was oriented head-out or right-side-out, respectively. Only the LVOR response components were modulated by vergence. A vectorial analysis of AVOR, LVOR, and combined responses supports the conclusion that AVOR and LVOR response components combine linearly during complex head motion.

Tilt perception during dynamic linear acceleration.

Head tilt is a rotation of the head relative to gravity, as exemplified by head roll or pitch from the natural upright orientation. Tilt stimulates both the otolith organs, owing to shifts in gravitational orientation, and the semicircular canals in response to head rotation, which in turn drive a variety of behavioral and perceptual responses. Studies of tilt perception typically have not adequately isolated otolith and canal inputs or their dynamic contributions. True tilt cannot readily dissociate otolith from canal influences. Alternatively, centrifugation generates centripetal accelerations that simulate tilt, but still entails a rotatory (canal) stimulus during important periods of the stimulus profiles. We reevaluated the perception of head tilt in humans, but limited the stimulus to linear forces alone, thus isolating the influence of otolith inputs. This was accomplished by employing a centrifugation technique with a variable-radius spinning sled. This allowed us to accelerate the sled to a constant angular velocity (128 degrees/s), with the subject centered, and then apply dynamic centripetal accelerations after all rotatory perceptions were extinguished. These stimuli were presented in the subjects' naso-occipital axis by translating the subjects 50 cm eccentrically either forward or backward. Centripetal accelerations were thus induced (0.25 g), which combined with gravity to yield a dynamically shifting gravitoinertial force simulating pitch-tilt, but without actually rotating the head. A magnitude-estimation task was employed to characterize the dynamic perception of pitch-tilt. Tilt perception responded sluggishly to linear acceleration, typically reaching a peak after 10-30 s. Tilt perception also displayed an adaptation phenomenon. Adaptation was manifested as a per-stimulus decline in perceived tilt during prolonged stimulation and a reversal aftereffect upon return to zero acceleration (i.e., recentering the subject). We conclude that otolith inputs can produce tilt perception in the absence of canal stimulation, and that this perception is subject to an adaptation phenomenon and low-pass filtering of its otolith input.

Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance.

Horizontal, vertical, and torsional eye movements were recorded using the magnetic search-coil technique during linear accelerations along the interaural (IA) and dorsoventral (DV) head axes. Four squirrel monkeys were translated sinusoidally over a range of frequencies (0.5-4.0 Hz) and amplitudes (0.1-0.7 g peak acceleration). The linear vestibuloocular reflex (LVOR) was recorded in darkness after brief presentations of visual targets at various distances from the subject. With subjects positioned upright or nose-up relative to gravity, IA translations generated conjugate horizontal (IA horizontal) eye movements, whereas DV translations with the head nose-up or right-side down generated conjugate vertical (DV vertical) responses. Both were compensatory for linear head motion and are thus translational LVOR responses. In concert with geometric requirements, both IA-horizontal and DV-vertical response sensitivities (in deg eye rotation/cm head translation) were related linearly to reciprocal fixation distance as measured by vergence (in m-1, or meter-angles, MA). The relationship was characterized by linear regressions, yielding sensitivity slopes (in deg.cm-1.MA-1) and intercepts (sensitivity at 0 vergence). Sensitivity slopes were greatest at 4.0 Hz, but were only slightly more than half the ideal required to maintain fixation. Slopes declined with decreasing frequency, becoming negligible at 0.5 Hz. Small responses were observed when vergence was zero (intercept), although no response is required. Like sensitivity slope, the intercept was largest at 4.0 Hz and declined with decreasing frequency. Phase lead was near zero (compensatory) at 4.0 Hz, but increased as frequency declined. Changes in head orientation, motion axis (IA vs. DV), and acceleration amplitude produced slight and sporadic changes in LVOR parameters. Translational LVOR response characteristics are consistent with high-pass filtering within LVOR pathways. Along with horizontal eye movements, IA translation generated small torsional responses. In contrast to the translational LVORs, IA-torsional responses were not systematically modulated by vergence angle. The IA-torsional LVOR is not compensatory for translation because it cannot maintain image stability. Rather, it likely compensates for the effective head tilt simulated by translation. When analyzed in terms of effective head tilt, torsional responses were greatest at the lowest frequency and declined as frequency increased, consistent with low-pass filtering of otolith input. It is unlikely that IA-torsional responses compensate for actual head tilt, however, because they were similar for both upright and nose-up head orientations. The IA-torsional and -horizontal LVORs seem to respond only to linear acceleration along the IA head axis, and the DV-vertical LVOR to acceleration along the head's DV axis, regardless of gravity.

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 otolith-mediated linear (IVOR) 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 IVOR response could be combined with, or isolated from, the aVOR response. Eccentric rotation in the UP and RD orientations generated aVOR and IVOR responses which acted in the same head plane. Horizontal aVOR-IVOR 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 IVOR 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 IVOR 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 IVOR from the aVOR. This response pattern was identical for horizontal and vertical eye movements. aVOR and IVOR 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 (IVOR) 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 IVOR 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 IVOR (NU orientation) responses, indicates that these VOR components sum in a linear fashion during complex head motion.

Evaluation of a video tracking device for measurement of horizontal and vertical eye rotations during locomotion.

We have evaluated a video-based method for measuring binocular horizontal and vertical eye movements of human subjects by comparing it with the magnetic search coil technique. This video tracking system (VTS) uses multiple infrared light sources and small video cameras to simultaneously measure the positions of reflected corneal images and the center of the pupil. The system has a linear range of approximately +/- 40 degrees horizontally and +/- 30 degrees vertically, a sampling rate of 120 Hz (180 Hz with the head fixed), and system noise with standard deviation of < 0.04 degree. The binocular eye-tracking system is light-weight (190 g), being mounted on goggles that, with the eyes in primary position, permit a field of view of 60 degrees horizontally and vertically. The VTS is insensitive to translations of the tracker relative to the eyes. By placing the video preprocessing unit on a cart, eye movements may be recorded while subjects walk through distances up to 100 feet. In comparison with the magnetic search coil technique, the VTS generally provides reliable measurements of horizontal and vertical eye position; eye velocity is noisier than corresponding coil signals, but superior to electro-oculography.

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 Exp 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.

Vertical, horizontal, and torsional eye movement responses to head roll in the squirrel monkey.

The vestibulo-ocular reflex (VOR) serves to stabilize images on the retina by rotating the eyes in the direction which opposes angular (aVOR) or linear (IVOR) head movement. The aVOR responds to rotations in any plane. Head rotations about the naso-occipital axis (roll) are accompanied by compensatory torsional eye movements, with gains typically less than 0.7. However, geometric considerations suggest that the response should not be restricted to torsion, and that horizontal, vertical, and torsional response components should depend upon eye position relative to the axis of rotation. Since eye position can differ for the two eyes (e.g., during convergence), the response to head roll should be accordingly disconjugate. Further, because the eyes are typically displaced from the axis of rotation, head roll entails a calculable translation of the eyes in space, and compensation for this component of motion is expected to add to the response to angular motion. The translational response component should be modulated by fixation distance. To test these geometric considerations in the aVOR, we investigated the three-dimensional ocular responses of squirrel monkeys to head roll. Torsional aVOR responses were accompanied by vertical components which were modulated by horizontal gaze position, and by horizontal components which were modified by vertical gaze position. The vertical response components were often appropriately disconjugate, and even opposing, yielding responses that appeared "see-saw" in character.(ABSTRACT TRUNCATED AT 250 WORDS)

The cervico-ocular reflex of normal human subjects in response to transient and sinusoidal trunk rotations.

We used the magnetic search coil technique to measure the horizontal cervico-ocular reflex (COR) of 8 subjects in response to transient or sinusoidal (0.1-1.0 Hz) trunk rotations while their heads were firmly immobilized. Although we were able to resolve eye rotations of < 0.05 degrees, the COR was hardly measurable (gain was always < 0.07). This finding, made with the most precise measurement technique used to date, suggests that the COR makes a negligible contribution to the stability of gaze in normal subjects during natural activities.

An investigation of horizontal combined eye-head tracking in patients with abnormal vestibular and smooth pursuit eye movements.

We investigated the interaction of smooth ocular pursuit (SP) and the vestibulo-ocular reflex (VOR) during horizontal, combined eye-head tracking (CEHT) in patients with abnormalities of either the VOR or SP movements. Our strategy was to apply transient stimuli that capitalized on the different latencies to onset of SP and the VOR. During CEHT of a target moving at 15 deg/sec, normal subjects and patients with VOR deficits all tracked the target with a gain close to 1.0. When the heads of normal subjects were suddenly and unexpectedly braked to a halt during CEHT, the eye promptly began to move in the orbit to track the target, but eye-in-orbit velocity transiently fell to about 60-70% of target velocity. In patients with deficient labyrinthine function, following the onset of the head brake, eye movements to track the target were absent, and SP movements were not generated until about 100 msec later. In patients with deficient SP, CEHT was superior to SP tracking with the head stationary; after the onset of the head brake, tracking eye movements were initiated promptly, but eye velocity was less than 50% of target velocity and increased only slightly thereafter. These results indicate that at least two mechanisms operate to overcome the VOR and allow gaze to track the target during CEHT: (1) the SP system provides a signal to cancel a normally-operating VOR (this cancellation signal is not needed by labyrinthine-deficient patients who have no VOR to cancel), and (2) a reduction of the gain of the VOR is achieved, an ability that is preserved even in patients with cerebral lesions that impair SP.

Loss of ipsidirectional quick phases of torsional nystagmus with a unilateral midbrain lesion.

We report a patient with a long-standing, unilateral lesion of the midbrain who showed ipsidirectional loss of torsional quick phases, impairment of all vertical eye movements and normal horizontal eye movements. The findings are consistent with recent reports of the effects of experimental lesions, in monkeys, of the rostral interstitial nucleus of the medial longitudinal fasciculus and the interstitial nucleus of Cajal.

Experimental tests of a superposition hypothesis to explain the relationship between the vestibuloocular reflex and smooth pursuit during horizontal combined eye-head tracking in humans.

1. We used a modeling approach to test the hypothesis that, in humans, the smooth pursuit (SP) system provides the primary signal for cancelling the vestibuloocular reflex (VOR) during combined eye-head tracking (CEHT) of a target moving smoothly in the horizontal plane. Separate models for SP and the VOR were developed. The optimal values of parameters of the two models were calculated using measured responses of four subjects to trials of SP and the visually enhanced VOR. After optimal parameter values were specified, each model generated waveforms that accurately reflected the subjects' responses to SP and vestibular stimuli. The models were then combined into a CEHT model wherein the final eye movement command signal was generated as the linear summation of the signals from the SP and VOR pathways. 2. The SP-VOR superposition hypothesis was tested using two types of CEHT stimuli, both of which involved passive rotation of subjects in a vestibular chair. The first stimulus consisted of a "chair brake" or sudden stop of the subject's head during CEHT; the visual target continued to move. The second stimulus consisted of a sudden change from the visually enhanced VOR to CEHT ("delayed target onset" paradigm); as the vestibular chair rotated past the angular position of the stationary visual stimulus, the latter started to move in synchrony with the chair. Data collected during experiments that employed these stimuli were compared quantitatively with predictions made by the CEHT model. 3. During CEHT, when the chair was suddenly and unexpectedly stopped, the eye promptly began to move in the orbit to track the moving target. Initially, gaze velocity did not completely match target velocity, however; this finally occurred approximately 100 ms after the brake onset. The model did predict the prompt onset of eye-in-orbit motion after the brake, but it did not predict that gaze velocity would initially be only approximately 70% of target velocity. One possible explanation for this discrepancy is that VOR gain can be dynamically modulated and, during sustained CEHT, it may assume a lower value. Consequently, during CEHT, a smaller-amplitude SP signal would be needed to cancel the lower-gain VOR. This reduction of the SP signal could account for the attenuated tracking response observed immediately after the brake. We found evidence for the dynamic modulation of VOR gain by noting differences in responses to the onset and offset of head rotation in trials of the visually enhanced VOR.(ABSTRACT TRUNCATED AT 400 WORDS)

Comparison of predictable smooth ocular and combined eye-head tracking behaviour in patients with lesions affecting the brainstem and cerebellum.

We compared the ability of eight normal subjects and 15 patients with brainstem or cerebellar disease to follow a moving visual stimulus smoothly with either the eyes alone or with combined eye-head tracking. The visual stimulus was either a laser spot (horizontal and vertical planes) or a large rotating disc (torsional plane), which moved at one sinusoidal frequency for each subject. The visually enhanced vestibulo-ocular reflex (VOR) was also measured in each plane. In the horizontal and vertical planes, we found that if tracking gain (gaze velocity/target velocity) for smooth pursuit was close to 1, the gain of combined eye-hand tracking was similar. If the tracking gain during smooth pursuit was less than about 0.7, combined eye-head tracking was usually superior. Most patients, irrespective of diagnosis, showed combined eye-head tracking that was superior to smooth pursuit; only two patients showed the converse. In the torsional plane, in which optokinetic responses were weak, combined eye-head tracking was much superior, and this was the case in both subjects and patients. We found that a linear model, in which an internal ocular tracking signal cancelled the VOR, could account for our findings in most normal subjects in the horizontal and vertical planes, but not in the torsional plane. The model failed to account for tracking behaviour in most patients in any plane, and suggested that the brain may use additional mechanisms to reduce the internal gain of the VOR during combined eye-head tracking. Our results confirm that certain patients who show impairment of smooth-pursuit eye movements preserve their ability to smoothly track a moving target with combined eye-head tracking.