Virtual reality as a countermeasure for astronaut motion sickness during simulated post-flight water landings.

Entry motion sickness (EMS) affects crewmembers upon return to Earth following extended adaptation to microgravity. Anticholinergic pharmaceuticals (e.g., Meclizine) are often taken prior to landing; however, they have operationally adverse side effects (e.g., drowsiness). There is a need to develop non-pharmaceutical countermeasures to EMS. We assessed the efficacy of a technological countermeasure providing external visual cues following splashdown, where otherwise only nauseogenic internal cabin visual references are available. Our countermeasure provided motion-congruent visual cues of an Earth-fixed scene in virtual reality, which was compared to a control condition with a head-fixed fixation point in virtual reality in a between-subject design with 15 subjects in each group. We tested the countermeasure's effectiveness at mitigating motion sickness symptoms at the end of a ground-based reentry analog: approximately 1 h of 2Gx centrifugation followed by up to 1 h of wave-like motion. Secondarily, we explored differences in vestibular-mediated balance performance between the two conditions. While Motion Sickness Questionnaire outcomes did not differ detectably between groups, we found significantly better survival rates (with dropout dictated by reporting moderate nausea consecutively over 2 min) in the visual countermeasure group than the control group (79% survival vs. 33%, t(14) = 2.50, p = 0.027). Following the reentry analogs, subjects demonstrated significantly higher sway prior to recovery (p = 0.0004), which did not differ between control and countermeasure groups. These results imply that providing motion-congruent visual cues may be an effective mean for curbing the development of moderate nausea and increasing comfort following future space missions.

The oculogyral illusion: retinal and oculomotor factors.

Subjects in a dark chamber exposed to angular acceleration while viewing a head-fixed target experience motion and displacement of the target relative to their body. Competing explanations of this phenomenon, known as the oculogyral illusion, have attributed it to the suppression of the vestibulo-ocular reflex (VOR) or to retinal slip. In the dark, the VOR evokes compensatory eye movements in the direction opposite to body acceleration. A head-fixed visual target will tend to suppress these eye movements. The VOR suppression hypothesis attributes the oculogyral illusion to the signals that prevent reflexive deviation of the eyes from the target thus resulting in apparent target displacement in the direction of acceleration. The retinal slip hypothesis attributes the illusion to inadequate fixation of the target with the eyes being involuntarily deviated in the direction opposite acceleration, the retinal slip being interpreted as target displacement in the direction of acceleration. Another possibility is that the illusion could arise from a change in the representation of the perceived head midline. To evaluate these three alternative hypotheses, we tested 8 subjects at 4 acceleration rates (2, 10, 20, 30°/s²) in each of three conditions: (a) fixate and point to a target light; (b) fixate to the target light and point to the head midline; (c) look straight ahead in the dark. The displacement magnitude of the oculogyral illusion was least at 2°/s² ≈ 2° and was ≈10° at the other acceleration rates. The presence of the target light significantly attenuated eye movements relative to the dark condition, but eye movements were still present at the 10, 20, and 30°/s² accelerations. The eye velocity profiles in the dark at different acceleration rates did not show a one-to-one inverse mapping to the magnitude of the oculogyral illusion at those rates. The perceived head midline was not significantly displaced at any of the acceleration rates. The oculogyral illusion thus has at least two contributing factors: the suppression of nystagmus at low acceleration rates and at higher acceleration rates, a partial suppression coupled with an integration of the drift of the eyes with respect to the fixation target.

Vertical frames of reference and control of body orientation.

The present paper aims at critically reviewing the most outstanding and recent studies regarding the control of body orientation in the vertical space. A first part defines the general concepts used throughout this manuscript. The second part investigates the vertical perception and the main factors which affect it, while trying to overcome the five areas of theoretical and experimental controversies we have identified in the literature. The third part of this review presents the different theoretical models of the vertical perception and body orientation in space. Finally, the last part focuses on the functional coupling between perception of the vertical and orientation of the body in space. It considers more particularly how these two dimensions interact for explaining the observed behaviors.

Motor function in microgravity: movement in weightlessness.

Microgravity provides unique, though experimentally challenging, opportunities to study motor control. A traditional research focus has been the effects of linear acceleration on vestibular responses to angular acceleration. Evidence is accumulating that the high-frequency vestibulo-ocular reflex (VOR) is not affected by transitions from a 1 g linear force field to microgravity (<1 g); however, it appears that the three-dimensional organization of the VOR is dependent on gravitoinertial force levels. Some of the observed effects of microgravity on head and arm movement control appear to depend on the previously undetected inputs of cervical and brachial proprioception, which change almost immediately in response to alterations in background force levels. Recent studies of post-flight disturbances of posture and locomotion are revealing sensorimotor mechanisms that adjust over periods ranging from hours to weeks.

Aspects of body self-calibration.

The representation of body orientation and configuration is dependent on multiple sources of afferent and efferent information about ongoing and intended patterns of movement and posture. Under normal terrestrial conditions, we feel virtually weightless and we do not perceive the actual forces associated with movement and support of our body. It is during exposure to unusual forces and patterns of sensory feedback during locomotion that computations and mechanisms underlying the ongoing calibration of our body dimensions and movements are revealed. This review discusses the normal mechanisms of our position sense and calibration of our kinaesthetic, visual and auditory sensory systems, and then explores the adaptations that take place to transient Coriolis forces generated during passive body rotation. The latter are very rapid adaptations that allow body movements to become accurate again, even in the absence of visual feedback. Muscle spindle activity interpreted in relation to motor commands and internally modeled reafference is an important component in permitting this adaptation. During voluntary rotary movements of the body, the central nervous system automatically compensates for the Coriolis forces generated by limb movements. This allows accurate control to be maintained without our perceiving the forces generated.

Vertical linear self-motion perception during visual and inertial motion: more than weighted summation of sensory inputs.

We evaluated visual and vestibular contributions to vertical self motion perception by exposing subjects to various combinations of 0.2 Hz vertical linear oscillation and visual scene motion. The visual stimuli presented via a head-mounted display consisted of video recordings of the test chamber from the perspective of the subject seated in the oscillator. In the dark, subjects accurately reported the amplitude of vertical linear oscillation with only a slight tendency to underestimate it. In the absence of inertial motion, even low amplitude oscillatory visual motion induced the perception of vertical self-oscillation. When visual and vestibular stimulation were combined, self-motion perception persisted in the presence of large visual-vestibular discordances. A dynamic visual input with magnitude discrepancies tended to dominate the resulting apparent self-motion, but vestibular effects were also evident. With visual and vestibular stimulation either spatially or temporally out-of-phase with one another, the input that dominated depended on their amplitudes. High amplitude visual scene motion was almost completely dominant for the levels tested. These findings are inconsistent with self-motion perception being determined by simple weighted summation of visual and vestibular inputs and constitute evidence against sensory conflict models. They indicate that when the presented visual scene is an accurate representation of the physical test environment, it dominates over vestibular inputs in determining apparent spatial position relative to external space.

Gravitoinertial force level affects the appreciation of limb position during muscle vibration.

Illusory motion and displacement of the restrained forearm can be elicited by vibrating the biceps brachii or triceps brachii muscle. We measured the influence of gravitoinertial force level on these perceptual responses to vibration during parabolic flight maneuvers where normal (1G) and high force (1.8G) background levels alternated with microgravity (0G). Subjects indicated the apparent forearm position of the vibrated arm with the other forearm and also made verbal reports. Biceps brachii vibration induced illusory extension of the forearm and triceps brachii, illusory flexion; these apparent motions and displacements were highly G force-dependent being enhanced at 1.8G and diminished at 0G relative to normal 1G force level. These alterations are discussed in terms of vestibulo-spinal and propriospinal influences on alpha-gamma motoneuronal control of muscle tone and the varying requirements for postural load support in different force backgrounds. Their implications for the control and appreciation of limb movements during exposure to different G force levels are also described.

Influence of gravitoinertial force level on vestibular and visual velocity storage in yaw and pitch.

Velocity storage is an important aspect of sensory-motor control of body orientation. The effective decay rate and three-dimensional organization of velocity storage are dependent upon body orientation relative to gravity and also are influenced by gravitoinertial force (G) level. Several of the inputs to velocity storage including otolithic, somatosensory, proprioceptive, and possibly motor are highly dependent on G level. To see whether the G dependency of velocity storage is related to changes in the effective coupling of individual sensory inputs to the velocity storage mechanism or to alterations in the time constant of velocity storage per se, we have studied horizontal vestibular nystagmus, horizontal optokinetic after nystagmus (OKAN) and vertical vestibular nystagmus as a function of force level. Horizontal OKAN and vestibular nystagmus both showed no effect of G level on their initial or peak slow phase velocities but their decay rates were quicker in 0G and 1.8G than in 1G. Vertical vestibular nystagmus also showed no effect of G level on peak velocity but decayed quicker in 0G relative to 1G. These-findings indicate that the intrinsic decay rate of a common velocity storage mechanism is affected by the magnitude of G. A negligible amount of slow phase eye velocity was observed in planes outside the planes of stimulation, thus short-term changes in G across multiple body axes can change velocity storage, but the change is restricted to the axis common to the rotary stimulus and the G vector.

Spatial stability, voluntary action and causal attribution during self-locomotion.

Adaptive changes in locomotory control and perception occur in environments where the normal relationship between effort and body displacement is altered (1,2). We have further investigated this plastic relationship by altering visual feedback during voluntary walking in place on a rotary treadmill. When the velocity of optical flow was increased or reversed relative to normal for the steps being made, subjects reported changes in perceived self-motion, the size, rate, and/or direction of their voluntary steps, the extent of voluntary effort required, and the apparent stability of a hand-held support bar. The floor and the visual environment were perceived as stable. We will show that these perceptual remappings obey "terrestrial constraints."

Multisensory, cognitive, and motor influences on human spatial orientation in weightlessness.

Exposure to weightlessness affects the control and appreciation of body position and orientation. In free fall the perception of one's own orientation and that of the surroundings is dependent on the presence or absence of contact cues, whether part of the body is visible in relation to the architecturally defined verticals of the space craft, cognitive factors, and exposure history. Sensations of falling are not elicited in free fall when the eyes are closed or the visual field is stabilized. This indicates that visual and cognitive factors as well as vestibular ones must be implicated in the genesis of such sensations under normal circumstances. Position sense of the limbs is also degraded in free fall. This may be due to alterations in skeletal muscle spindle gain owing to a decreased otolith-spinal activation. We provide evidence that during initial exposure to weightlessness there is a decrease in muscle stiffness which affects movement accuracy. The altered loading of the skeletal muscles due to the head and body being weightless are shown to be significant etiological factors in space motion sickness.

The role of reafference in recalibration of limb movement control and locomotion.

The reafference model has frequently been used to explain spatial constancy during eye and head movements. We have found that its basic concepts also form part of the information processing necessary for the control and recalibration of reaching movements. Reaching was studied in a novel force environment--a rotating room that creates centripetal forces of the type that could someday substitute for gravity in space flight, and Coriolis forces which are side effects of rotation. We found that inertial, noncontacting Coriolis forces deviate the path and endpoint of reaching movements, a finding that shows the inadequacy of equilibrium position models of movement control. Repeated movements in the rotating room quickly lead to normal movement patterns and to a failure to perceive the perturbing forces. The first movements made after rotation stops, without Coriolis forces present, show mirror-image deviations and evoke perception of a perturbing force even though none is present. These patterns of sensorimotor control and adaptation can largely be explained on the basis of comparisons of efference copy, reafferent muscle spindle, and cutaneous mechanoreceptor signals. We also describe experiments on human locomotion using an apparatus similar to that which Mittelstaedt used to study the optomotor response of the Eristalis fly. These results show that the reafference principle relates as well to the perception of the forces acting on and exerted by the body during voluntary locomotion.

Combined influences of gravitoinertial force level and visual field pitch on visually perceived eye level.

Psychophysical measurements of the level at which observers set a small visual target so as to appear at eye level (VPEL) were made on 13 subjects in 1.0 g and 1.5 g environments in the Graybiel Laboratory rotating room while they viewed a pitched visual field or while in total darkness. The gravitoinertial force was parallel to the z-axis of the head and body during the measurements. The visual field consisted of two 58 degrees high, luminous, pitched-from-vertical, bilaterally symmetric, parallel lines, viewed in otherwise total darkness. The lines were horizontally separated by 53 degrees and presented at each of 7 angles of pitch ranging from 30 degrees with the top of the visual field turned away from the subject (top backward) to 30 degrees with the top turned toward the subject (top forward). At 1.5 g, VPEL changed linearly with the pitch of the 2-line stimulus and was depressed with top backward pitch and elevated with top forward pitch as had been reported previously at 1.0 g (1,2); however, the slopes of the VPEL-vs-pitch functions at 1.0 g and 1.5 g were indistinguishable. As reported previously also (3,4), the VPEL in darkness was considerably lower at 1.5 g than at 1.0 g; however, although the y-intercept of the VPEL-vs-pitch function in the presence of the 2-line visual field (visual field erect) was also lower at 1.5 g than at 1.0 g as it was in darkness, the G-related difference was significantly attenuated by the presence of the visual field. The quantitative characteristics of the results are consistent with a model in which VPEL is treated as a consequence of an algebraic weighted average or a vector sum of visual and nonvisual influences although the two combining rules lead to fits that are equally good.

Motion sickness susceptibility in parabolic flight and velocity storage activity.

In parabolic flight experiments, we have found post-rotary nystagmus to be differentially suppressed in free fall (OG) and in a high gravitoinertial force (1.8G) background relative to 1G. In addition, the influence of postrotary head movements on nystagmus suppression was found to be contingent on G level. The nature of this pattern indicated a G-dependency of the velocity storage and dumping mechanisms. Here, we have rank-correlated susceptibility to motion sickness during head movements in OG and 1.8G with the following: a) the decay time constant of the slow phase velocity of post-rotary nystagmus under 1G, no head movement, baseline conditions, b) the extent of time constant reduction elicited in OG and 1.8G; c) the extent of time constant reduction elicited by head tilts in 1G; and d) changes in the extent of time constant reduction in OG and 1.8G over repeated tests. Susceptibility was significantly correlated with the extent to which a head movement reduced the time constant in 1G, was weakly correlated with the baseline time constant, but was not correlated with the extent of reduction in OG or 1.8G. This pattern suggests a link between mechanisms evoking symptoms of space motion sickness and the mechanisms of velocity storage and dumping. Experimental means of evaluating this link are described.

Decreased susceptibility to motion sickness during exposure to visual inversion in microgravity.

Head and body movements made in microgravity tend to bring on symptoms of motion sickness. Such head movements, relative to comparable ones made on Earth, are accompanied by unusual combinations of semicircular canal and otolith activity owing to the unloading of the otoliths in OG. Head movements also bring on symptoms of motion sickness during exposure to visual inversion (or reversal) on Earth because the vestibulo-ocular reflex is rendered anti-compensatory. Here, we present evidence that susceptibility to motion sickness during exposure to visual inversion is decreased in a 0G relative to a 1G force background. This difference in susceptibility appears related to the alteration in otolith function in 0G. Some implications of this finding for the etiology of space motion sickness are described.

The influence of gravitoinertial force level on oculomotor and perceptual responses to Coriolis, cross-coupling stimulation.

Susceptibility to motion sickness during exposure to constant levels of Coriolis, cross-coupling stimulation is lower in zero G and higher in 1.8 G than in a 1-G force environment (10, 13). The goal of the present experiment was to determine whether gravitoinertial force magnitude also influences oculomotor and perceptual responses to Coriolis, cross-coupling stimulation. We had blind-folded subjects who were rotating at constant velocity make standardized head movements during the free-fall and high force phases of parabolic flight, and we measured both the characteristics of their horizontal nystagmus and the magnitude of their experienced self-motion. Both responses were less intense in the free-fall periods than in the high force periods. Although the slow phase velocity of nystagmus reached the same initial, peak level in both conditions, it decayed more quickly in zero G. These findings suggest that the response to semicircular canal stimulation depends on the background level of gravitoinertial force.

The influence of gravitoinertial force level on oculomotor and perceptual responses to sudden stop stimulation.

Our goal was to determine whether the vestibular response to vertical, z-axis body rotation in the dark is influenced by the magnitude of gravitoinertial force. We measured the nystagmus and the duration of illusory self-motion elicited in blindfolded subjects by cessation of such rotation during the free-fall, high, and terrestrial force phases of parabolic flight maneuvers. Both measures were significantly lower in zero G than in 1 G, and lower to a smaller extent in 1.8 G. The decreased intensity of nystagmus was due specifically to a decrease in the time constant of slow phase velocity decay with no decrement in peak velocity. This pattern of findings is consistent with the responses we had observed earlier to constant levels of Coriolis, cross-coupled stimulation during parabolic flight maneuvers both in terms of the mode of nystagmus suppression and the effect of G-level. Attenuation of the vestibular response to rotary acceleration in free-fall causes sensory-motor mismatches during natural head movements in orbital flight that may be important factors in the evocation of space motion sickness.

Altered sensorimotor control of the body as an etiological factor in space motion sickness.

Exposure to nonterrestrial force levels affects the activity of gravitoinertial force sensitive receptors of the body, both of labyrinthine and nonlabyrinthine origin. It also disrupts the normal patterning of motor control of body orientation and movement. The patterns and levels of muscle innervation necessary to achieve particular body configurations and to bring about particular body movements are greatly affected by background force level and body orientation relative to the force vector. The present studies demonstrate that such altered sensorimotor control of head and body posture along with altered vestibulomotor control are evocative of motion sickness. This observation has explanatory significance both for space motion sickness and the re-entry disturbances that occur after prolonged spaceflight.

The effect of optokinetic stimulation on daytime sleepiness.

This study examined the effect of optokinetic stimulation on objective sleepiness, as measured by the Multiple Sleep Latency Test (MSLT). The Nightcap, a portable sleep monitor, was used in a novel way to perform MSLTs, as well as record sleep in the home. Subjects wore the Nightcap for seven consecutive nights. On days 3 and 5 of the protocol, subjects came into the lab for an MSLT. On the experimental day, subjects underwent 10 minutes optokinetic stimulation (OKS), resulting in moderate motion sickness prior to each MSLT trial. Although subjects in the OKS condition reported significantly more drowsiness than controls, this did not result in significantly reduced sleep latencies.

Altered sensory-motor control of the head as an etiological factor in space-motion sickness.

Mechanical unloading during head movements in weightlessness may be an etiological factor in space-motion sickness. We simulated altered head loading on Earth without affecting vestibular stimulation by having subjects wear a weighted helmet. Eight subjects were exposed to constant velocity rotation about a vertical axis with direction reversals every 60 sec. for eight reversals with the head loaded and eight with the head unloaded. The severity of motion sickness elicited was significantly higher when the head was loaded. This suggests that altered sensory-motor control of the head is also an etiological factor in space-motion sickness.

Altered sensory-motor control of the head as an etiological factor in space-motion sickness.

Mechanical unloading during head movements in weightlessness may be an etiological factor in space-motion sickness. We simulated altered head loading on Earth without affecting vestibular stimulation by having subjects wear a weighted helmet. Eight subjects were exposed to constant velocity rotation about a vertical axis with direction reversals every 60 sec. for eight reversals with the head loaded and eight with the head unloaded. The severity of motion sickness elicited was significantly higher when the head was loaded. This suggests that altered sensory-motor control of the head is also an etiological factor in space-motion sickness.