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.

Anticipatory VOR suppression induced by visual and nonvisual stimuli in humans.

We compared the predictive behavior of smooth pursuit (SP) and suppression of the vestibuloocular reflex (VOR) in humans by examining anticipatory smooth eye movements, a phenomenon that arises after repeated presentations of sudden target movement preceded by an auditory warning cue. We investigated whether anticipatory smooth eye movements also occur prior to cued head motion, particularly when subjects expect interaction between the VOR and either real or imagined head-fixed targets. Subjects were presented with horizontal motion stimuli consisting of a visual target alone (SP), head motion in darkness (VOR), or head motion in the presence of a real or imagined head-fixed target (HFT and IHFT, respectively). Stimulus sequences were delivered as single cycles of a velocity sinusoid (frequency: 0.5 or 1.0 Hz) that were either cued (a sound cue 400 ms earlier) or noncued. For SP, anticipatory smooth eye movements developed over repeated trials in the cued, but not the noncued, condition. In the VOR condition, no such anticipatory eye movements were observed even when cued. In contrast, anticipatory responses were observed under cued, but not noncued, HFT and IHFT conditions, as for SP. Anticipatory HFT responses increased in proportion to the velocity of preceding stimuli. In general, anticipatory gaze responses were similar in cued SP, HFT, and IHFT conditions and were appropriate for expected target motion in space. Anticipatory responses may represent the output of a central mechanism for smooth-eye-movement generation that operates during predictive SP as well as VOR modulations that are linked with SP even in the absence of real visual targets.

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.

Nystagmus and postural instability after headshake in patients with vestibular dysfunction.

Nystagmus after rapid head-shaking (post-headshake nystagmus) is often seen in patients with vestibulopathy. Post-headshake nystagmus is transient and is frequently associated with symptoms of dizziness, dysequilibrium, or vertigo. The phenomenon presumably reflects headshake-induced asymmetry in vestibulo-ocular reflex pathways, which persists after head-shaking stops. We postulated that the same vestibular imbalance that underlies post-headshake nystagmus might produce an equivalent in postural instability. To test this hypothesis, we investigated the effect of headshake on postural control and eye movements in patients who exhibited post-headshake nystagmus, vestibulopathy, or both. Postural instability was quantified with a dynamic platform device, whereas eye movements were recorded with electrooculography. Ten normal controls and 21 patients with a history of post-headshake nystagmus or unilateral vestibulopathy were evaluated. Subjects were tested for 20 seconds before and immediately after passive horizontal headshake (+/- 30-degree amplitude) at 2 Hz for 20 seconds. Postural stability was assessed while subjects stood with eyes closed, and the floor was modulated proportionally with sway. The difference in normalized peak-to-peak sway (equilibrium score) before and after headshake was assessed in all subjects and compared between groups. Post-headshake nystagmus was documented by electro-oculography recorded during posturography. Results for normal controls and vestibulopathic subjects without post-headshake nystagmus showed only a small transient decline in postural stability after headshake. Those with post-headshake nystagmus (regardless of caloric asymmetry) showed a robust decline in postural stability.(ABSTRACT TRUNCATED AT 250 WORDS)

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)

Eye position signals in the abducens and oculomotor nuclei of monkeys during ocular convergence.

Many neurons in oculomotor pathways encode signals related to eye position. For example, motoneurons in the third, fourth, and sixth cranial nuclei discharge at highly regular rates during fixation intervals. During fixations of far targets, their tonic discharge is linearly related to conjugate eye position. Previous studies provided evidence that premotor cells in brainstem pathways also encoded conjugate eye position. McConville et al. (this volume), however, measured eye movements during binocular fixations when the eyes were converged and concluded that the position signal encoded by premotor position-vestibular-pause (PVP) cells in the vestibular nuclei is related to monocular (right or left) eye position rather than to conjugate eye position. This surprising relationship would not have been noticed in earlier studies that measured the movements of only one eye (using a single eye coil) or that measured only the conjugate movements of the two eyes (using bitemporal EOG electrodes). How general a feature of oculomotor signal processing is this finding? In this paper, we re-examine the eye position signal in abducens and oculomotor neurons when the movements of the two eyes are conjugate and when they are disjunctive and therefore disassociated. The data suggest that abducens neurons (AMNs and AINs) and oculomotor neurons (putative medial rectus motoneurons), unlike PVP cells, are not monocular but encode mixtures of right and left eye position signals.

Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging.

Natural aging entails progressive deterioration in a variety of biological systems. This study focuses on visual and vestibular influences on human eye movements as a function of aging. Eye movements were recorded (search-coil technique) during visual, vestibular, and combined stimuli in subjects across a broad range of ages (18-89 years). Two types of visual following were assessed: smooth pursuit (SP) of a small discrete target, and optokinetic (OKR) following of a large-field striped image. The vestibulo-ocular reflex (VOR) was studied during head rotation in darkness. Visual-vestibular interactions were recorded during rotation in two ways: when the optokinetic scene was earth-fixed, resulting in visual enhancement of the VOR (VVOR), and when the visual image was head-fixed, allowing visual suppression of the VOR (VSVOR). Stimuli consisted of horizontal sinusoidal oscillations over the frequency range 0.025-4 Hz. Trials were analyzed to yield response gain (peak horizontal eye/stimulus velocities) and phase (asynchrony, in degrees, between eye and stimulus velocity signals). VOR gain in young subjects was greatest (near 0.9) at 2.5-4 Hz but declined steadily with decreasing frequency, while phase hovered near zero until 0.1 Hz and then developed a progressively increasing lead. Effects of advancing age were small, given the modest head velocities presented, and were most noticeable as an increase in phase lead and decline in gain at the lowest frequencies (< or = 0.1 Hz). The two forms of visual following and all conditions of visual-vestibular interactions displayed more prominent age-dependent changes. OKR and SP response characteristics (0.25-4 Hz) closely resembled each other. Gain was greatest at 0.25 Hz, while phase was near 0 degree. As frequency increased, gain declined while phase lag rose. However, both gain and phase lag tended to be slightly greater for OKR than for SP responses. Both SP and OKR response properties deteriorated progressively with increasing age, as witnessed by a progressive decline in gain and increase in phase lag, even at modest frequencies (e.g., 0.25-1.0 Hz). VVOR responses were generally closer to the ideal of 1.0 in gain and 0 degree in phase than either the VOR or visual following alone. A subtle but significant age-dependent decline in VVOR performance occurred at the lowest frequencies. VSVOR response characteristics were close to those of the VOR and VVOR at 4 Hz, where visual influences on eye movements are generally inconsequential.(ABSTRACT TRUNCATED AT 400 WORDS)

Three dimensional eye movements of squirrel monkeys following postrotatory tilt.

Three-dimensional squirrel monkey eye movements were recorded during and immediately following rotation around an earth-vertical yaw axis (160 degrees/s steady state, 100 degrees/s2 acceleration and deceleration). To study interactions between the horizontal angular vestibulo-ocular reflex (VOR) and head orientation, postrotatory VOR alignment was changed relative to gravity by tilting the head out of the horizontal plane (pitch or roll tilt between 15 degrees and 90 degrees) immediately after cessation of motion. Results showed that in addition to post rotatory horizontal nystagmus, vertical nystagmus followed tilts to the left or right (roll), and torsional nystagmus followed forward or backward (pitch) tilts. When the time course and spatial orientation of eye velocity were considered in three dimensions, the axis of eye rotation always shifted toward alignment with gravity, and the postrotatory horizontal VOR decay was accelerated by the tilts. These phenomena may reflect a neural process that resolves the sensory conflict induced by this postrotatory tilt paradigm.

Linear vestibuloocular reflex during motion along axes between nasooccipital and interaural.

Linear vestibuloocular reflexes (LVORs) stabilize retinal images by producing eye movements to compensate for linear head motion. LVOR response characteristics depend upon gaze relative to the motion axis and binocular fixation distance. LVOR sensitivity during NO-axis motion increases as gaze eccentricity relative to the motion axis increases and as binocular fixation distance decreases. To fixate targets during forward head motion and rightward gaze, eyes must move to the right, but when looking left, the eyes must move to the left. In this study, LVORs were measured (binocular search coils) during 5.0 Hz horizontal motion along axes between and including NO and IA. This reorients head and otolith inputs relative to linear motion. We found that LVORs follow the same kinematics regardless of eye position in the head or head orientation relative to motion. Eye position information must be quickly and accurately integrated with otolith inputs to determine eye position (gaze) relative to linear head motion in space. The LVOR provides a behaviorally useful reflex for maintaining ocular fixation on visual targets during translation along any axis.

Senescence of human visual-vestibular interactions. 1. Vestibulo-ocular reflex and adaptive plasticity with aging.

The human horizontal vestibulo-ocular reflex (VOR) was studied as a function of aging (18 to 89 years) over a broad range of frequencies (0.025 to 4 Hz) and peak velocities (50 degrees to 300 degrees/s) of angular head movement. Eye movements were recorded using the search-coil technique. High stimulus frequencies and amplitudes were employed in order to challenge the VOR sufficiently to enhance potential age-related deficits in its pathways and functions. Further, the possibility that adaptive plastic mechanisms, which normally restore failing VOR function, might themselves deteriorate with aging was tested. Subjects were studied before and after an 8-h period while wearing 2 x binocular magnifying lenses. Demonstrable differences were observed in the human VOR as a function of natural aging. These differences were most pronounced in phase measures (increasing lead with aging), both at low frequency and low head velocity, and at modest frequency but high head velocity. Gain decrements were also observed with aging, but the changes were more subtle. The modifications in the VOR may be interpreted as an age-dependent deterioration in VOR performance. The course of age-related changes in response characteristics, particularly phase lead at the highest stimulus amplitude, are similar to age-related anatomical deterioration reported in peripheral vestibular structures. These changes resemble those in young patients with vestibular lesions, and are consistent with the notion that aging entails a progressive bilateral peripheral vestibular loss. Adaptive plastic mechanisms, which normally maintain VOR performance when altered responses result in visual-vestibular mismatch during head rotation, also deteriorate with aging. Again, the phenomenon resembles that in younger but vestibulopathic individuals. The effect is most profound at high frequencies and head velocities commensurate with natural behavior.

Ocular motor abnormalities in human immunodeficiency virus infection.

We studied ocular motor performance in 47 subjects with human immunodeficiency virus (HIV) infection and 25 normal control subjects. Saccade accuracy was the most sensitive measure, being significantly poorer for all four HIV-positive groups (asymptomatic, acquired immunodeficiency syndrome [AIDS] without dementia, and AIDS with dementia, and AIDS-related complex) than for control subjects. While saccade duration and peak velocity were not significantly different across groups, the scatter of saccade duration was increased in all HIV-positive groups. Saccade latency was not significantly affected. In both simple and complex antisaccade tasks, the asymptomatic, AIDS, and AIDS dementia groups made significantly fewer correct-way antisaccades than did control subjects. Latencies of correct-way antisaccades were increased for AIDS and AIDS dementia groups in the simple antisaccade trials, and for all HIV-positive groups in the complex trials. Fixation stability was significantly worse in the AIDS dementia group than in control subjects. Smooth pursuit gain was decreased in the asymptomatic, AIDS, and AIDS dementia groups for the least demanding trial. One or more ocular motor abnormalities were present in 15 (88%) asymptomatic subjects, 11 (69%) with AIDS-related complex, and 14 (100%) AIDS patients without or with dementia.