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 1 g (resultant 45 degrees roll-tilt of 1.4 g) 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 degrees) 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 degrees 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 degrees 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.

Effect of visual surrounding motion on body sway in a three-dimensional environment.

Unidirectional motion of a uniplanar background induces a codirectional postural sway. It has been shown recently that fixation of a stationary foreground object induces a sway response in the opposite direction (Bronstein & Buckwell, 1997) when the background moves transiently. The present study investigated factors determining this contradirectional postural response. In the experiments presented, center of foot pressure and head displacements were recorded from normal subjects. The subjects faced a visual background of 2 x 3 m, at a distance of 1.5 m, which could be moved parallel to the interaural axis. Results showed that when the visual scene consisted solely of a moving background, the conventional codirectional postural response was elicited. When subjects were asked to fixate an earth-fixed foreground (window frame) placed between them and the moving background, a consistent postural response in the opposite direction to background motion was observed. In addition, we showed that this contradirectional postural response was not transient but was sustained for the 11 sec of background motion. We investigated whether this contradirectional postural response was the consequence of the induced movement of the foreground by background motion. Although induced movement was verbally reported by subjects when viewing an earth-fixed target projected onto the moving background, the contradirectional sway did not occur. These results indicate that foreground-background separation in depth was necessary for the contradirectional postural response to occur rather than induced movement. Another experiment showed that, when the fixated foreground was attached to the head of the observer, the contradirectional sway was not observed and was therefore unrelated to vergence. Finally, results showed that the contradirectional postural response was, in the main, monocularly mediated. We conclude that the direction of the postural sway produced by a moving background in a three-dimensional environment is determined primarily by motion parallax.

The human linear vestibulo-ocular reflex to transient accelerations: visual modulation of suppression and enhancement.

Visual modulation of the linear vestibulo-ocular reflex (LVOR) was investigated in 4 normal subjects exposed to translational interaural transient accelerations of 0.08 g and 0.17 g. Binocular eye movements were recorded with the scleral search-coil technique. LVOR modulation with target proximity was studied using earth-fixed targets at distances of 30 and 60 cm (LVOR-E). LVOR suppression (LVOR-S) was provoked by similar targets which were head-fixed. For both conditions, linear acceleration evoked compensatory slow-phases whose velocities were, from onset, enhanced in proportion to acceleration and target proximity. At 80 ms after motion onset, i.e. before visually-guided eye movements could aid target fixation, gains (eye velocity/relative target velocity) during LVOR-E averaged 0.32 (S.D. 0.07) over all combinations of accelerations and target distances. At this time, eye velocities for LVOR-S were on average 33% lower than for LVOR-E (1.8 degrees/s vs. 2.7 degrees/s). During LVOR-S, a marked suppression of eye movements appeared at 102 ms (S.D. 10 ms). We conclude that mechanisms other than pursuit can be used to attenuate the LVOR at < 80 ms but their effect is weak. The marked suppression observed around 100 ms might be due to an early visual effect on vestibular pathways or by some independent voluntary control mechanism.

Effect of otolith dysfunction. Impairment of visual acuity during linear head motion in labyrinthine defective subjects.

Visual symptoms emerging after the loss of vestibular function are usually attributed to the dysfunction of semicircular canal vestibulo-ocular reflexes, as they have been shown to stabilize vision during angular head movements. However, natural head displacements involve both angular and linear motion, and therefore visual instability may occur because of defective otolith-ocular reflexes (OORs) which are the eye movements evoked by linear head acceleration. In this paper, the relationship between OORs and visual acuity during linear head motion was studied in normal subjects and 14 patients with bilateral loss of caloric responses. OORs were elicited in darkness by step acceleration (0.24 g) of the whole body along the interaural axis. Latency, slow phase velocity and asymmetry of the OOR were measured from the desaccaded and averaged electrooculographic trace. Visual acuity was assessed during sinusoidal lateral oscillation of the subject viewing an earth-fixed target, and vice versa with the subject stationary and the target moving at 0.5, 1.0 and 1.5 Hz. The task was to recognize numbers flashing up on a three digit light-emitting diode visual display. Normal subjects had symmetrical OORs with short latencies (< 130 ms). In patients, OORs were either absent (n = 2) or abnormal with asymmetries (n = 8), diminished velocities (n = 4) or prolonged latencies (n = 6). At high frequency oscillation (1.5 Hz), normal subjects invariably recognized more numbers during self-motion compared with target motion, whereas most patients did not. In patients, abnormal dynamic visual acuity was correlated with absent or delayed OOR responses. This is the first demonstration of a functional role of the OORs in that they contribute to visual stabilization during high frequency linear head motion. Bilateral vestibular failure commonly affects the OORs and thereby compromises dynamic visual acuity.

Eye movements induced by lateral acceleration steps. Effect of visual context and acceleration levels.

Eye movement responses were obtained from six normal subjects exposed to randomly ordered rightwards/leftwards linear acceleration steps of 0.05 g, 0.1 g or 0.24 g amplitude and 650 ms duration along the interaural axis. With the instruction to gaze passively into the darkness, compensatory nystagmus was evoked with slow-phase velocity sensitivity of 49 degrees s(-1) g(-1). When subjects viewed earth-fixed targets at 30 cm, 60 cm or 280 cm, eye movements at 130 ms from motion onset were proportional to acceleration and inversely proportional to target distance, before the onset of visually guided eye movements. Our results show that a modulation with viewing distances of the earliest human otolith-ocular reflexes occurs in the presence of pure linear acceleration. However, full compensation was not attained for the nearer targets and higher accelerations.

Interaction of linear and angular vestibulo-ocular reflexes of human subjects in response to transient motion.

The possibility of synergistic interaction between the canal and otolith components of the horizontal vestibulo-ocular reflex (VOR) was evaluated in human subjects by subtracting the response to pure angular rotation (AVOR) from the response to combined angular and translational motion (ALVOR) and comparing this difference with the VOR to isolated linear motion (LVOR). Assessments were made with target fixation at 60 cm and in darkness. Linear stimuli were acceleration steps attaining 0.25 g in less than 80 ms. To elicit responses to combined translational and angular head movements, the subjects were seated on a Barany chair with the head displaced forwards 40 cm from the axis of rotation. The chair was accelerated at approximately 300 deg/s2 to 127 deg/s peak angular velocity, the tangential acceleration of the head being comparable with that of isolated translation. Estimates of the contribution of smooth pursuit to responses in the light were made from comparisons of isolated pursuit of similar target trajectories. In the dark the slow phase eye movements evoked by combined canal-otolith stimuli were higher in magnitude by approximately a third than the sum of those produced by translation and rotation alone. In the light, the relative target displacement during isolated linear motion was similar to the difference in relative target displacements during eccentric and centred rotation. However, the gain of the translational component of compensatory eye movement during combined translational and angular motion was approximately unity, in contrast to the gain of the response to isolated linear motion, which was approximately a half. Pursuit performance was always poorer than target following during self-motion. The LVOR responses in the light were greater than the sum of the LVOR responses in the dark with pursuit eye movements. We conclude that, in response to transient motion, there is a synergistic enhancement of the translational VOR with concurrent canal stimulation and that the enhancement of the LVOR in the light is not due solely to pursuit.

Influence of target distance and acceleration level on eye movements evoked by lateral acceleration steps.

Lateral eye movements produced by linear acceleration along the inter-aural axis were studied in 6 normal subjects. They were seated upright, whole-body restrained, and were exposed to randomised rightward/leftward steps of 0.05 g. 0.1 g, 0.24 g of 600 ms duration. When viewing earth-fixed targets at 30, 60 or 280 cm from their eyes, mainly pure compensatory slow-phase eye movements were evoked at latencies around 50 ms measured for the closest viewing distances. At onset, slow-phase amplitude was modulated by acceleration and target distance. When the subjects were stationary and pursued moving targets at similar distances and accelerations, latencies around 140 ms were observed, and catch-up saccades were frequently made. From these experiments, we defined the dynamics of the otolith-ocular reflex for various levels of acceleration and viewing distances.

Thresholds for perception of lateral motion in normal subjects and patients with bilateral loss of vestibular function.

Thresholds for detection of direction of whole-body lateral linear acceleration were determined for normal (N) and labyrinthine defective (LD) subjects. Thresholds for 67% correct detection of direction of acceleration steps for 5 LDs (mean 5.65 cm/s2, peak gradient = 25 cm/s3) were not significantly different from 8 Ns (mean 4.84 cm/s2, peak gradient = 22 cm/s3). High inter-subject variability was found both among the 7 Ns and 3 LDs for detection of parabolic accelerations with some individuals being unable to detect their motion direction. Mean Ns thresholds were 15.2 cm/s2 for a ramp with gradient of acceleration = 2.8 cm/s3, 26.4 cm/s2 for a ramp with gradient = 7.9 cm/s3 and 20.2 cm/s2 for a parabola with second derivative = 1.52 cm/s4. Thresholds for LDs were respectively 19.1 cm/s2, 32 cm/s2 and 26.7 cm/s2. The lower thresholds for acceleration steps demonstrate the important effect of acceleration gradient on motion detection. For all stimuli, thresholds for some LDs could be in the range of Ns showing that somatosensory signals can play a significant role in detecting lateral acceleration.