Ocular counterrolling induced by centrifugation during orbital space flight

During the 1998 Neurolab mission (STS-90), four astronauts were exposed to interaural centripetal accelerations (Gy centrifugation) of 0.5g and 1g during rotation on a centrifuge, both on Earth and during orbital space flight. Subjects were oriented either left-ear out or right-ear out, facing or back to motion. Binocular eye movements were measured in three dimensions using a video technique. On Earth, tangential centrifugation that produces 1g of interaural linear acceleration combines with gravity to tilt the gravitoinertial acceleration (GIA) vector 45° in the roll plane relative to the head vertical, generating a summed vector of 1.4g. Before flight, this elicited mean ocular counterrolling (OCR) of 5.7°. Due to the relative absence of gravity during flight, there was no linear acceleration along the dorsoventral axis of the head. As a result, during in-flight centrifugation, gravitoinertial acceleration was strictly aligned with the centripetal acceleration along the interaural axis. There was a small but significant decrease (mean 10%) in the magnitude of OCR in space (5.1°). The magnitude of OCR during postflight 1g centrifugation was not significantly different from preflight OCR (5.9°). Findings were similar for 0.5g centrifugation, but the OCR magnitude was approximately 60% of that induced by centrifugation at 1g. OCR during pre- and postflight static tilt was not significantly different and was always less than OCR elicited by centrifugation on Earth for an equivalent interaural linear acceleration. In contrast, there was no difference between the OCR generated by in-flight centrifugation and by static tilt on Earth at equivalent interaural linear accelerations. These data support the following conclusions: (1) OCR is generated predominantly in response to interaural linear acceleration; (2) the increased OCR during centrifugation on Earth is a response to the head dorsoventral 1g linear acceleration component, which was absent in microgravity. The dorsoventral linear acceleration could have activated either the otoliths or body-tilt receptors that responded to the larger GIA magnitude (1.4g), to generate the increased OCR during centrifugation on Earth. A striking finding was that magnitude of OCR was maintained throughout and after flight. This is in contrast to most previous postflight OCR studies, which have generally registered decreases in OCR. We postulate that intermittent exposure to artificial gravity, in the form of the centripetal acceleration experienced during centrifugation, acted as a countermeasure to deconditioning of this otolith-ocular orienting reflex during the 16-day mission. Electronic Publication     

Spatial orientation of optokinetic nystagmus and ocular pursuit during orbital space flight

On Earth, eye velocity of horizontal optokinetic nystagmus (OKN) orients to gravito-inertial acceleration (GIA), the sum of linear accelerations acting on the head and body. We determined whether adaptation to microgravity altered this orientation and whether ocular pursuit exhibited similar properties. Eye movements of four astronauts were recorded with three-dimensional video-oculography. Optokinetic stimuli were stripes moving horizontally, vertically, and obliquely at 30°/s. Ocular pursuit was produced by a spot moving horizontally or vertically at 20°/s. Subjects were either stationary or were centrifuged during OKN with 1 or 0.5 g of interaural or dorsoventral centripetal linear acceleration. Average eye position during OKN (the beating field) moved into the quick-phase direction by 10° during lateral and upward field movement in all conditions. The beating field did not shift up during downward OKN on Earth, but there was a strong upward movement of the beating field (9°) during downward OKN in the absence of gravity; this likely represents an adaptation to the lack of a vertical 1-g bias in-flight. The horizontal OKN velocity axis tilted 9° in the roll plane toward the GIA during interaural centrifugation, both on Earth and in space. During oblique OKN, the velocity vector tilted towards the GIA in the roll plane when there was a disparity between the direction of stripe motion and the GIA, but not when the two were aligned. In contrast, dorsoventral acceleration tilted the horizontal OKN velocity vector 6° in pitch away from the GIA. Roll tilts of the horizontal OKN velocity vector toward the GIA during interaural centrifugation are consistent with the orientation properties of velocity storage, but pitch tilts away from the GIA when centrifuged while supine are not. We speculate that visual suppression during OKN may have caused the velocity vector to tilt away from the GIA during dorsoventral centrifugation. Vertical OKN and ocular pursuit did not exhibit orientation toward the GIA in any condition. Static full-body roll tilts and centrifugation generating an equivalent interaural acceleration produced the same tilts in the horizontal OKN velocity before and after flight. Thus, the magnitude of tilt in OKN velocity was dependent on the magnitude of interaural linear acceleration, rather than the tilt of the GIA with regard to the head. These results favor a filter model of spatial orientation in which orienting eye movements are proportional to the magnitude of low frequency interaural linear acceleration, rather than models that postulate an internal representation of gravity as the basis for spatial orientation.Abbreviations A_g Acceleration of gravity - A_c Centripetal acceleration - CCW Counterclockwise - CW Clockwise - FD- X Flight day X - g Gravity - GIA Gravito-inertial acceleration - H Horizontal - LED Left-ear-down - LEO Left-ear-out - LOB Lying-on-back - L- X Launch minus X days - NCM No-chair-motion - ND Nose-down - NU Nose-up - OCR Ocular counter-colling - OKAN Optokinetic after-nystagmus - OKN Optokinetic nystagmus - OKS Optokinetic stimulus - pos Position - REO Right-ear-out - R+ X Recovery plus X days - T Torsional - V Vertical - vel Velocity     

Interaction of the body, head, and eyes during walking and turning

Body, head, and eye movements were measured in five subjects during straight walking and while turning corners. The purpose was to determine how well the head and eyes followed the linear trajectory of the body in space and whether head orientation followed changes in the gravito-inertial acceleration vector (GIA). Head and body movements were measured with a video-based motion analysis system and horizontal, vertical, and torsional eye movements with video-oculography. During straight walking, there was lateral body motion at the stride frequency, which was at half the frequency of stepping. The GIA oscillated about the direction of heading, according to the acceleration and deceleration associated with heel strike and toe flexion, and the body yawed in concert with stepping. Despite the linear and rotatory motions of the head and body, the head pointed along the forward motion of the body during straight walking. The head pitch/roll component appeared to compensate for vertical and horizontal acceleration of the head rather than orienting to the tilt of the GIA or anticipating it. When turning corners, subjects walked on a 50-cm radius over two steps or on a 200-cm radius in five to seven steps. Maximum centripetal accelerations in sharp turns were ca.0.4 g, which tilted the GIA ca.21 degrees with regard to the heading. This was anticipated by a roll tilt of the head of up to 8 degrees. The eyes rolled 1-1.5 degrees and moved down into the direction of linear acceleration during the tilts of the GIA. Yaw head deviations moved smoothly through the turn, anticipating the shift in lateral body trajectory by as much as 25 degrees. The trunk did not anticipate the change in trajectory. Thus, in contrast to straight walking, the tilt axes of the head and the GIA tended to align during turns. Gaze was stable in space during the slow phases and jumped forward in saccades along the trajectory, leading it by larger angles when the angular velocity of turning was greater. The anticipatory roll head movements during turning are likely to be utilized to overcome inertial forces that would destabilize balance during turning. The data show that compensatory eye, head, and body movements stabilize gaze during straight walking, while orienting mechanisms direct the eyes, head, and body to tilts of the GIA in space during turning.     

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

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

Compensatory manual motor responses while object wielding during combined linear visual and physical roll tilt stimulation

Dynamic signals from multiple sensory channels must be integrated by the central nervous system to create a unified perception of self-motion and spatial orientation. Using immersive virtual environments, we altered the relative contribution of visual and inertial inputs and evaluated the effects on perceptuomotor outputs. Subjects seated in a tilting chair were exposed to a combined 0.25 Hz sinusoidal roll-tilt (±7.5°) about the naso-occipital axis while viewing one of four visual conditions. One visual condition was in darkness, and the other three depicted 2 m of sinusoidal horizontal or vertical linear motion either synchronous or asynchronous with the roll-tilt. Subjects performed a perceptuomotor task of aligning a handheld object to gravitational vertical (GV) with the entire arm being free to move in six degrees of freedom. Subjects were tested with two objects, a joystick and glass of water, in counter-balanced order. Specific visual effects were as follows: (1) the phase leads of object tilt relative to chair/subject roll-tilt were affected by visual condition, (2) horizontal translation of the object was entrained with visual velocity, rather than with visual acceleration or maximum roll-tilt, and (3) when vertical visual motion was viewed during chair/subject roll-tilt, vertical object translation increased. Although the head-fixed scene meant visual vertical cues were always aligned with the subject’s median sagittal plane, object tilt showed sensitivity to inertial roll-tilt (Gain > 0.5) which was not significantly different from the dark condition. Two object effects were found: (1) tilt deviation from GV was greater when wielding a joystick compared to a full glass of water, and (2) the phase of horizontal visual motion relative to subject roll tilt affected the joystick amplitude of horizontal translation but not the glass of water. In conclusion, an attentional shift driven by postural assumptions can account for the two object effects, however, the visual effects suggest that a process for deriving the net gravitoinertial force from visual and inertial cues is involved. Inertial signals dominated the perception of verticality, but visual linear translation affected the spatiotemporal dynamics of the manual motor responses during object wielding.     

Spatial orientation and balance control changes induced by altered gravitoinertial force vectors

To better understand the mechanisms of human adaptation to rotating environments, we exposed 19 healthy subjects and 8 vestibular-deficient subjects ("abnormal"; four bilateral and four unilateral lesions) to an interaural centripetal acceleration of 1g (resultant 45° roll-tilt of 1.4g) on a 0.8-m-radius centrifuge for periods of 90 min. The subjects sat upright (body z-axis parallel to centrifuge rotation axis) in the dark with head stationary, except during 4 min of every 10 min, when they performed head saccades toward visual targets switched on at 3- to 5-s intervals at random locations (within ±30°) in the earth-horizontal plane. Eight of the normal subjects also performed the head saccade protocol in a stationary chair adjusted to a static roll-tilt angle of 45° for 90 min (reproducing the change in orientation but not the magnitude of the gravitoinertial force on the centrifuge). Eye movements, including voluntary saccades directed along perceived earth- and head-referenced planes, were recorded before, during, and immediately after centrifugation. Postural center of pressure (COP) and multisegment body kinematics were also gathered before and within 10 min after centrifugation. Normal subjects overestimated roll-tilt during centrifugation and revealed errors in perception of head-vertical provided by directed saccades. Errors in this perceptual response tended to increase with time and became significant after approximately 30 min. Motion-sickness symptoms caused approximately 25% of normal subjects to limit their head movements during centrifugation and led three normal subjects to stop the test early. Immediately after centrifugation, subjects reported feeling tilted 10° in the opposite direction, which was in agreement with the direction of their earth-referenced directed saccades. Postural COP, segmental body motion amplitude, and hip-sway frequency increased significantly after centrifugation. These postural effects were short-lived, however, with a recovery time of several postural test trials (minutes). There were also asymmetries in the direction of postcentrifugation COP and head tilt which depended on the subject's orientation during the centrifugation adaptation period (left ear or right ear out). The amount of total head movements during centrifugation correlated poorly or inversely with postcentrifugation postural stability, and the most unstable subject made no head movements. There was no decrease in postural stability after static tilt, although these subjects also reported a perceived tilt briefly after return to upright, and they also had COP asymmetries. Abnormal subjects underestimated roll-tilt during centrifugation, and their directed saccades revealed permanent spatial distortions. Bilateral abnormal subjects started out with poor postural control, but showed no postural decrements after centrifugation, while unilateral abnormal subjects had varying degrees of postural decrement, both in their everyday function and as a result of experiencing the centrifugation. In addition, three unilateral, abnormal subjects, who rode twice in opposite orientations, revealed a consistent orthogonal pattern of COP offsets after centrifugation. These results suggest that both orientation and magnitude of the gravitoinertial vector are used by the central nervous system for calibration of multiple orientation systems. A change in the background gravitoinertial force (otolith input) can rapidly initiate postural and perceptual adaptation in several sensorimotor systems, independent of a structured visual surround. Electronic Publication     

Dynamics of maculo-ocular reflexes in the frog

Compensatory torsional and vertical eye movements were recorded in the frog during sinusoidal linear acceleration along the longitudinal and transverse body axes, respectively. Stimulus frequencies ranged between 0.1 and 1.0 Hz and peak accelerations from 0.01 g to 0.1 g corresponding to body tilts ranging from 0.57 to 5.7 degrees. In addition, static compensatory eye movements were studied during fore-and-aft and lateral body tilt over ranges of +/- 10 degrees. The evoked eye movements were generally quite small (+/- 0.5 degree). Dynamic gain (rotation of the eye/apparent rotation of gravity direction) was 0.10-0.20 at 0.1 Hz and decreased to about 0.05 at 1.0 Hz. The gain of vertical eye movements was somewhat higher than that of torsional eye movements. Phase lag relative to peak accelerations increased from about 10 degrees to about 45 degrees over the same frequency range. Static compensatory eye movements evoked by nose-up and ipsilateral side-up tilt were larger in amplitude than those evoked by nose-down and ipsilateral side-down tilt. Static gain (rotation of the eye/tilt of the whole body) was about 0.10 for vertical and about 0.06 for torsional eye movements. No consistent eye movements could be evoked by vertical sinusoidal accelerations (maximal modulation amplitudes +/- 0.025 g). The results indicate that, as in other vertebrates, maculo-ocular reflexes contribute to gaze stabilization in the frog mainly during low frequency and static head and body tilts.     

Effects of head-down bed rest and artificial gravity on spatial orientation

We studied spatial orientation before and after 21 days of 6° head-down bed rest in 15 subjects. During bed rest, 8 subjects were treated daily with 1 h Gz centrifugation (artificial gravity) (2.5 g at the feet; 1.0 g at the heart), with 7 subjects serving as controls. Ocular counter-rolling and subjective visual vertical were assessed during 90° whole body roll tilt to the left and right. Ocular counter-rolling was unaffected by bed rest and bed rest + artificial gravity. Performance on the subjective visual vertical task was unchanged in the control group, but exhibited a significant increase in error for 48 h after bed rest in the treatment (artificial gravity) group. Intermittent application of linear acceleration along the long body axis may have increased the weighting of the idiotropic vector, resulting in an increased bias of the subjective visual vertical toward the long body axis during 90° roll tilt.     

Vertical ocular responses to constant linear acceleration generated by fore-aft head translation in monkeys

We examined the vertical linear vestibuloocular reflexes (LVORs) elicited by constant linear acceleration (0-0.5 g for >95 ms) during transient fore-aft translation in three monkeys. In the dark condition, small but consistent downward ocular responses to forward translation were observed (latencies >41 ms) when the initial vertical eye positions were at 0 degrees , although eye movements following backward translation were inconsistent among animals. These downward ocular responses showed the following three characteristics: they were independent of vertical gaze eccentricities, their magnitudes were almost proportional to the forward acceleration, and they were reduced by the large-field (not the spot) visual information. These characteristics revealed that the downward ocular responses to forward translation were the tilt LVORs. In addition, we recognized that the translational LVOR, which depended on vertical gaze eccentricities, was working at the same time. Our data suggest that constant linear acceleration during forward translation evokes the tilt LVOR, as well as the illusory tilting perception.     

Effect of the mono- and tetra-sialogangliosides, GM1 and GQ1b, on long-term potentiation in the CA1 hippocampal neurons of the guinea pig

 Effects of the mono- and tetra-sialogangliosides, GM1 and GQ1b, on long-term potentiation (LTP) were investigated in the CA1 neurons of guinea-pig hippocampal slices. The magnitude of LTP induced by a strong tetanus (100 Hz, 100 pulses) was not significantly affected by application of either ganglioside. In contrast, when LTP was induced by a weak tetanus (100 Hz, 4 pulses), a significantly greater LTP was induced in the presence of either ganglioside. Similarly, when slices were incubated in low-Ca²⁺ (1.0–1.1 mM) medium for more than 2 h, the LTP was usually small or absent, but showed a significant increase in amplitude of population spike (A-PS) when the slices were incubated with either GM1 or GQ1b (4–5 μg/ml). In addition, the application of GQ1b (4 μg/ml) reversed the blocking effect of an NMDA-receptor antagonist, APP-5 (10 μM), on the induction of LTP and resulted in forming LTP. Based on these findings, we conclude that GM1 and GQ1b exert positive modulatory effects on the induction of LTP in hippocampal CA1 neurons and suggest that GM1 and GQ1b may participate in the induction of LTP as donors of Ca²⁺ ions. Received: 21 April 1998 / Accepted: 5 May 1998     

Responses of monkey vestibular-only neurons to translation and angular rotation

Single-unit recordings were obtained from central vestibular neurons in three monkeys during passive head movements. Neurons that discharged in relation to head translation or changes in head orientation, but not eye movement ("vestibular-only," n = 154), were examined in detail. Neuronal discharge rates were analyzed during four stimulus conditions: sinusoidal head translation in the horizontal plane (0.2-4 Hz, 0.2 g peak acceleration), static head tilt in the vertical plane (+/-20 degrees ), oscillatory head tilt (0.5-2 Hz), and sinusoidal angular rotation about an earth-vertical axis (0.5 or 1 Hz). Vestibular-only cells were divided into two groups based on the regularity of their spontaneous discharge rates (CV*). One group (low-sensitivity units) exhibited regular discharge rates (CV* < 0.2), weak discharge modulation during head translation (<25 spikes . s(-1) . g(-1) at f = 1 Hz), and persistent discharge rates related to static head tilt (0.68 spikes . s(-1) . degrees (-1) of head tilt). The second group (high sensitivity neurons) exhibited irregular discharge rates (CV* > 0.2), strong discharge modulation during head translation ( approximately 100 spikes . s(-1) . g(-1) at f = 1 Hz), and little or no change in discharge rate during static head tilt (0.32 spikes . s(-1) . degrees (-1)). The firing rates of some neurons in both groups were modulated during rotation about an earth-vertical axis (42%), but the modulation was greater for neurons classified as high sensitivity units. Previous reports have described neurons similar to the high sensitivity group; however, the low sensitivity or tilt neurons have not previously been characterized. Significantly, recent theoretical models have predicted neurons with discharge patterns similar to those of low- and high-sensitivity neurons.     

Roll rotation cues influence roll tilt perception assayed using a somatosensory technique

We investigated how the nervous system processes ambiguous cues from the otolith organs by measuring roll tilt perception elicited by two motion paradigms. In one paradigm (tilt), eight subjects were sinusoidally tilted in roll with the axis of rotation near ear level. Stimulus frequencies ranged from 0.005 to 0.7 Hz, and the peak amplitude of tilt was 20 degrees . During this paradigm, subjects experienced a sinusoidal variation of interaural gravitational force with a peak of 0.34 g. The second motion paradigm (translation) was designed to yield the same sinusoidal variation in interaural force but did not include a roll canal cue. This was achieved by sinusoidally translating the subjects along their interaural axis. For the 0.7-Hz translation trial, the subjects were simply translated from side to side. A centrifuge was used for the 0.005- to 0.5-Hz translation trials; the subjects were rotated in yaw at 250 degrees /s for 5 min before initiating sinusoidal translations yielding an interaural otolith stimulus composed of both centrifugal and radial acceleration. Using a somatosensory task to measure roll tilt perception, we found substantial differences in tilt perception during the two motion paradigms. Because the primary difference between the two motion paradigms was the presence of roll canal cues during roll tilt trials, these perceptual differences suggest that canal cues influence tilt perception. Specifically, rotational cues provided by the semicircular canals help the CNS resolve ambiguous otolith cues during head tilt, yielding more accurate tilt perception.     

Chronology of the push pull effect on nonhuman primates—shift of the arterial pressure threshold

Fighter pilots are frequently exposed to high Gz acceleration which may induce in-flight loss of consciousness (G-LOC). One factor reducing tolerance to accelerations is a previous exposure to negative accelerations. This phenomenon, which happens during the first few seconds after the onset of the positive plateau, is called the push pull effect. Our goal was to validate a non human primate model in order to study push pull physiological mechanisms and possible changes in arterial pressure, which may occur after the first ten seconds of the positive acceleration plateau. Eight rhesus monkeys were centrifuged in profile runs, including positive Gz accelerations (+1.4, +2 and +3 Gz) with or without previous negative Gz acceleration (–2 and –3 Gz vs. +1.4 Gz). Heart rate, blood pressure and esophageal pressure were recorded during the entire centrifugation run. Results showed that the push pull effect was observed in the non human primate model. Moreover, the reduced tolerance to acceleration lingered longer than that during the first ten seconds after exposure to +Gz acceleration. It was found that, after the fourteenth second, mean blood arterial pressure stabilizes at a lower value, when the positive acceleration is preceded by a negative acceleration (15.8 kPa for –1 Gz and 15.5 for –2 Gz vs. 16.9 for 1.4 Gz). The chronology of the push pull effect seems to involve two periods. One has a short time span. The other one has a longer time span and could be induced by shift of pressure threshold, coming from exposure to previous negative acceleration.     

Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics

1. The purpose of this study was to quantify the response characteristics of eye movements produced by linear head oscillations in the dark (the linear vestibuloocular reflex, or LVOR). Horizontal, vertical, and torsional eye movements were measured in adult squirrel monkeys by the use of a dual scleral search-coil technique during linear oscillations (0.5, 1.5, and 5.0 Hz, 0.36 g peak acceleration) along the animals' interaural (IA), dorsoventral (DV), and nasooccipital (NO) axes. 2. Two LVOR responses, horizontal eye movements during IA-axis translation and vertical eye movements during DV-axis motion, were in a compensatory direction for head translation. Response amplitudes increased as frequency increased, whereas phase typically showed a lead. 3. Two other LVORs, torsional responses during IA-axis translation (all frequencies) and vertical responses during NO-axis oscillations (0.5 Hz), behaved differently. These two LVORs cannot be functionally compensatory for head translation because they degrade fixation on targets, and therefore image stability, by rotating the eyes off target (NO-vertical) or torting the eyes relative to the visual world (IA-torsional). Responses to NO-axis motion at frequencies greater than 0.5 Hz depended on initial eye position and fixation distance and are described in the companion paper. 4. The effect of head orientation on the LVOR was assessed by testing four head positions in 90 degrees steps around the axis of head motion for each of the three axes of translation. This was done, first, to determine whether the LVORs are responses to the "swinging vector" of gravitoinertial force during linear head motion or to head translation; and second, to quantify potential effects of static head (otolith) orientation on the LVORs. Results showed no systematic effects of head orientation on LVOR responses in the frequency bandwidth studied. This indicates that the LVORs are dependent on the direction of linear motion relative to the head (and otolith organs) but not on the swinging vector of gravitoinertial force, and that the LVORs are uninfluenced by static orientation of the head and reloading of the otoliths.     

Vertical eye position responses to steady-state sinusoidal fore–aft head translation in monkeys

A major function of the otolith organ is to detect linear acceleration generated by two different head conditions, dynamic linear translation and static tilt relative to gravity. To investigate these sensory functions of the otolith organ, we analyzed vertical eye position in response to steady-state sinusoidal fore–aft translation over a range of frequencies (0.5–4 Hz) and amplitudes (0.10–0.33 g) in three monkeys. Vertical vestibuloocular reflexes elicited by linear acceleration (LVORs) during sinusoidal fore–aft translation were divided into translational LVOR component and tilt LVOR component taking vertical gaze-dependent properties into account. Based on geometrical considerations, the translational LVOR component, but not the tilt LVOR component, depended on vertical gaze eccentricity. To quantify these two components, we used a V-shaped function model, plotting vertical eye sensitivities (deg/cm) against vertical gaze eccentricities (deg). The slope (deg/cm per degree) and intercept (sensitivity at zero gaze eccentricity) of this function approximately reflected the translational and tilt LVOR components, respectively. Our data show that the tilt LVOR component is independent of the reciprocal of the fixation distance (MA), whereas the translational LVOR component is almost linearly related to MA. The gain of the tilt LVOR component, characterized by low-pass dynamics, was greatest (0.36) at 0.5 Hz. Visual information clearly reduced the gain of the tilt LVOR component, by approximately 50%. There was no difference between the effects of large-field and small-spot stimuli. These findings demonstrate that steady-state sinusoidal fore–aft translation at lower frequencies stimulates the otolith organs and produces a pseudo-pitch tilt in cooperation with the gravito-inertial force and as a result elicits an ocular response equivalent to the tilt LVOR.     

Subjective somatosensory vertical during dynamic tilt is dependent on task, inertial condition, and multisensory concordance

To investigate how visual and vestibular cues are integrated for the perception of gravity during passive self-motion, we measured the ability to maintain a handheld object vertical relative to gravity without visual feedback during sinusoidal roll-tilt stimulation. Visual input, either concordant or discordant with actual dynamic roll-tilt, was delivered by a head-mounted display showing the laboratory. The four visual conditions were darkness, visual-vestibular concordance, stationary visual scene, and a visual scene 180° phase-shifted relative to actual tilt. Tilt-indication performance using a solid, cylindrical joystick was better in the presence of concordant visual input relative to the other visual conditions. In addition, we compared performance when indicating the vertical by the joystick or a full glass of water. Subjects indicated the direction of gravity significantly better when holding the full glass of water than the joystick. Matching the inertial characteristics, including fluid properties, of the handheld object to the glass of water did not improve performance. There was no effect of visual input on tilt performance when using the glass of water to indicate gravitational vertical. The gain of object tilt motion did not change with roll-tilt amplitude and frequency (±7.5° at 0.25 Hz, ±10° at 0.16 Hz, and ±20° at 0.08 Hz), however, the phase of object tilt relative to subject tilt showed significant phase-leads at the highest frequency tested (0.25 Hz). Comparison of the object and visual effects observed suggest that the task-dependent behavior change may be due to an attentional shift and/or shift in strategy.     

Difference in the perception of the horizon during true and simulated tilt in the absence of semicircular canal cues

Perception of tilt (somatogravic illusion) in response to sustained linear acceleration is generally attributed to the otolithic system which reflects either a translation of the head or a reorientation of the head with respect to gravity (tilt/translation ambiguity). The main aim of this study was to compare the tilt perception during prolonged static tilt and translation between 8 and 20° of tilt relative to the gravitoinertial forces (i.e., G and GIF, respectively) when the semicircular cues were no more available. An indirect measure of tilt perception was estimated by means of a visual and kinesthetic judgment of the gravitational horizon. The main results contrast with the interpretation regarding the tilt/translation ambiguity as the same orientation relative to the shear forces G for the true tilt or GIF in the centrifuge did not induce the same horizon perception. Visual adjustment and arm pointing in the centrifuge were always above the ones observed in a G environment. Part of the lowering of the judgment in the centrifuge may be related to the mechanical effect of GIF on the effectors as shown by the shift of the egocentric coordinates in the direction of GIF. The role of the extravestibular graviceptors in the judgment of the degree of tilt of one’s own body relative to G or GIF was discussed.     

Linear acceleration perception in the roll plane before and after unilateral vestibular neurectomy

Summary The ability of 33 patients to perceive the direction, relative to the body long axis, of a linear acceleration vector acting in the coronal plane, rolltilt perception, was studied at various times, before and from 1 week to 6 months after unilateral, selective vestibular neurectomy for Meniere's disease, acoustic neuroma or intractable paroxysmal vertigo. The results of these patients were compared with the results of 31 normal subjects and two control patients who had both vestibular nerves surgically sectioned. Rotating on a fixed-chair centrifuge in an otherwise darkened room, each observer was required to indicate his perception of the direction of the resultant gravito-inertial vector by setting a small, motor-driven, illuminated bar, attached to the chair but rotatable in the frontoparallel plane, to the perceived gravitational horizontal. Normal subjects accurately align the bar with respect to the gravito-inertial resultant vector which, in the dark, they assume to be the gravitational vertical. This percept has been called the oculogravic illusion. Accurate roll-tilt perception is due to vestibular (probably mainly otolithic) sensory information since patients with bilateral vestibular neurectomies do not perceive the resultant vector accurately. Whereas normal subjects perceive resultant vectors directed to the right and to the left equally accurately, roll-tilt perception was invariably asymmetrical one week after unilateral vestibular neurectomy. Even at rest there was an asymmetry in the baseline settings, so that patients set the bar down on the side of the operated ear, in order for it to appear gravitationally horizontal: if a patient had a right vestibular nerve section then he set the bar clockwise (from the patient's view) below the true gravitational horizontal. With increasing gravitoinertial resultant angles there was an increasing asymmetry of roll-tilt perception due both to decreased sensitivity to roll-tilt stimuli directed towards the operated ear and to transiently increased sensitivity to roll-tilt stimuli directed towards the intact ear. A progressive decrease in both perceptual asymmetries followed, rapidly in the first 3 weeks, more slowly in the next 6 months. Based on these results, which are consistent with what is known about the responses of primary and secondary otolithic neurons to linear acceleration, we propose: (1) that the asymmetric roll-tilt perceptual response following unilateral vestibular neurectomy is an otolithic analogue of Ewald's second law; (2) that the perceptual asymmetries may be due to decreased spontaneous activity in the deafferented lateral vestibular nucleus; (3) that the progressive recovery of roll-tilt perceptual symmetry after vestibular neurectomy may be part of the otolithic component of the total recovery phenomenon known as vestibular compensation; (4) that ocular torsion caused by the unilateral vestibular neurectomy is a major factor contributing to the systematic errors in baseline settings to the gravitational horizontal one week after operation.     

Off-center yaw rotation: effect of naso-occipital linear acceleration on the nystagmus response of normal human subjects and patients after unilateral vestibular loss

 Dual search coils were used to record horizontal, vertical and torsional eye movement components of one eye during nystagmus caused by off-center yaw rotation (yaw centrifugation). Both normal healthy human subjects (n=7) and patients with only one functioning labyrinth (n=12) were studied in order to clarify how the concomitant linear acceleration affected the nystagmus response. Each subject was seated with head erect on the arm of a fixed-chair human centrifuge, 1 m away from the center of the rotation, and positioned to be facing along a radius; either towards (facing-in) or away from (facing-out) the center of rotation. Both yaw right and yaw left angular accelerations of 10°s^–2 from 0 to 200°/s were studied. During rotation a centripetal linear acceleration (increasing from 0 to 1.24×g units) was directed along the subject’s naso-occipital axis resulting in a shift of the resultant angle of the gravitoinertial acceleration (GIA) of 51° in the subject’s pitch plane and an increase in the total GIA magnitude from 1.0 to 1.59×g. In normal subjects during the angular acceleration off-center there were, in addition to the horizontal eye velocity components, torsional and vertical eye velocities present. The magnitude of these additional components, although small, was larger than observed during similar experiments with on-center angular acceleration (Haslwanter et al. 1996), and the change in these components is attributed to the additional effect of the linear acceleration stimulation. In the pitch plane the average size of the shift of the axis of eye velocity (AEV) during the acceleration was about 8° for a 51° shift of the GIA (around 16% of the GIA shift) so that the AEV-GIA alignment was inadequate. There was a very marked difference in the size of the AEV shift depending on whether the person was facing-in [AEV shift forward (i.e. non-compensatory) of about 4°] or facing-out [AEV shift forward (i.e. compensatory) of around 12°]. The linear acceleration decreased the time constant of decay of the horizontal component of the post-rotatory nystagmus: from an average of 24.8°/s facing-in to an average of 11.3°/s facing-out. The linear acceleration dumps torsional eye velocity in an manner analogous to, but independent of, the dumping of horizontal eye velocity. Patients with UVD had dramatically reduced torsional eye velocities for both facing-in and facing-out headings, and there was little if any shift of the AEV in UVD patients. The relatively small effects of linear acceleration on human canal-induced nystagmus found here confirms other recent studies in humans (Fetter et al. 1996) in contrast to evidence from monkeys and emphasizes the large and important differences between humans and monkeys in otolith-canal interaction. Our results confirm the vestibular control of the axis of eye velocity of humans is essentially head-referenced whereas in monkeys that control is essentially space-referenced. Received: 22 September 1997 / Accepted: 30 June 1998     

Context-specific adaptation of the gain of the oculomotor response to lateral translation using roll and pitch head tilts as contexts

Previous studies established that vestibular and oculomotor behaviors can have two adapted states (e.g., gain) simultaneously, and that a context cue (e.g., vertical eye position) can switch between the two states. The present study examined this phenomenon of context-specific adaptation for the oculomotor response to interaural translation (which we term "linear vestibulo-ocular reflex" or LVOR even though it may have extravestibular components). Subjects sat upright on a linear sled and were translated at 0.7 Hz and 0.3 gpeak acceleration while a visual-vestibular mismatch paradigm was used to adaptively increase (x2) or decrease (x0) the gain of the LVOR. In each experimental session, gain increase was asked for in one context, and gain decrease in another context. Testing in darkness with steps and sines before and after adaptation, in each context, assessed the extent to which the context itself could recall the gain state that was imposed in that context during adaptation. Two different contexts were used: head pitch (26 degrees forward and backward) and head roll (26 degrees or 45 degrees, right and left). Head roll tilt worked well as a context cue: with the head rolled to the right the LVOR could be made to have a higher gain than with the head rolled to the left. Head pitch tilt was less effective as a context cue. This suggests that the more closely related a context cue is to the response being adapted, the more effective it is.