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The adaptation of vestibulo-spinal reflexes as a function of spaceflight and their relationship to space motion sickness

The hypothesis that exposure to prolonged free fall is a form of sensorymotor rearrangement rather than a direct change in otolith sensitivity or sensory compensation for a reduced otolith input is discussed. Data from Spacelab-1 experiment 1NS-104 are presented to support an otolith reinterpretation hypothesis. This experiment measured vestibulo-spinal reflex changes as a function of sustained free fall. Findings indicate that when a monosynaptic reflex (H-reflex), measured from the major postural muscles (soleus) is used, adaptation to space flight includes a change in how the central nervous system interprets a fall. In a normal gravity environment a sudden unexpected fall produces a potentiated H-reflex. After 7 days inflight, an equivalent fall does not potentiate the reflex. Postflight a greatly increased reflex is observed in those crewmen most susceptible to space motion sickness.

Reschke, M. F.↗

Torsional vestibulo-ocular reflex measurements for identifying otolith asymmetries possibly related to space motion sickness susceptibility

Recent studies have identified significant correlations between space motion sickness susceptibility and measures of disconjugate torsional eye movements recorded during parabolic flights. These results support an earlier proposal which hypothesized that an asymmetry of otolith function between the two ears is the cause of space motion sickness. It may be possible to devise experiments that can be performed in the 1 g environment on earth that could identify and quantify the presence of asymmetric otolith function. This paper summarizes the known physiological and anatomical properties of the otolith organs and the properties of the torsional vestibulo-ocular reflex which are relevant to the design of a stimulus to identify otolith asymmetries. A specific stimulus which takes advantage of these properties is proposed.

Peterka, Robert J.↗

Oculomotor function during space flight and susceptibility to space motion sickness

Horizontal vestibulo-ocular reflex (VOR) and saccadic eye movements (SEM) were studied in 18 subjects before and during five Space Shuttle missions to evaluate the effects of weightlessness and correlations between results and susceptibility to and actual presence of space motion sickness (SMS). Active sinusoidal head oscillation was the stimulus for VOR tests with vision (VVOR), with eyes shaded (VOR-ES), and VOR suppression (VOR-S). Eye movements were recorded by electrooculography and head position by a potentiometer. No pathological nystagmus or other abnormal eye movements were seen. No significant in-flight changes were seen in the gain, phase shift or waveform of VVOR, VOR-ES or VOR-S. Statistically significant increases in saccadic latency and decreases in saccadic velocity were seen, with no change in saccadic accuracy. Preflight differences between SMS susceptible and nonsusceptible subjects were noted only in VOR-S, with less complete suppression in susceptible subjects, a finding also seen in flight. During flight, VVOR gain was significantly increased in three nonaffected subjects. Saccades of SMS-affected subjects showed increased latency and velocity and decreased accuracy compared to saccades of unaffected subjects.

Thornton, William E.↗

Vestibular mechanisms underlying certain problems in a rotating spacecraft

Vestibular side effects are discussed with the aid of a conceptual framework based on an analysis of vestibular input-output relations. These side effects tend to fall into two main categories: (1) Reflex phenomena, and (2) motion sickness, a delayed epiphenomenon. Although the symptomatology of motion sickness is similar wherever experienced, both the eliciting stimuli and the opportunity to adapt may differ in different motion environments. These differences not only are exemplified when motion sickness is compared in a weightless and in a rotating environment, but they also point to important differences in the problem of preventing (or treating) motion sickness in these two very different environments.

Graybiel, A.↗

Preadaptation to the stimulus rearrangement of weightlessness: Preliminary studies and concepts for trainer designs

An effort to develop preflight adaptation training (PAT) apparatus and procedures to adapt astronauts to the stimulus rearrangement of weightless spaceflight is being pursued. Based on the otolith tilt-translation reinterpretation model of sensory adaptation to weightlessness, two prototype preflight adaptation trainers (PAT) have been developed. These trainers couple pitch movement of the subject with translation of the visual surround. Subjects were exposed to this stimulus rearrangement for periods of 30 m. The hypothesis is that exposure to the rearrangement would attenuate vertical eye movements was supported by two experiments using the Miami University Seesaw (MUS) PAT prototype. The Dynamic Environment Simulator (DES) prototype failed to support this hypothesis; this result is attributed to a pecularity of the DES apparatus. A final experiment demonstrated that changes in vertical eye movements were not a consequence of fixation on an external target during exposure to a control condition. Together these experiments support the view that preflight adaptation training can alter eye movements in a manner consistent with adaptation to weightlessness. Following these initial studies, concepts for development of operational preflight trainers were proposed. The trainers are intended to: demonstrate the stimulus rearrangement of weightlessness; allow astronauts to train in altered sensory environment; modify sensory motor reflexes; and reduce/eliminate space motion sickness symptoms.

Parker, D. E.↗

Microgravity enhances the relative contribution of visually-induced motion sensation

Visually-induced self-motion sensation and postural reflexes were first explored in microgravity on the Spacelab 1 mission where four subjects demonstrated that visual orientation effects were stronger in microgravity than preflight. Extended testing of two more subjects during the Spacelab D-1 orbital flight confirmed this finding. The development of visual substitution for inappropriate graviceptor information occurs over the first day or two in microgravity. Additional instrumentation to measure postural reactions failed to produce a more reliable indicator of visual effects than subjective orientation. Localized tactile cues applied to the feet changed the qualitative nature of vection and reduced its subjective strength.

Young, L. R.↗

Self-motion perception: assessment by real-time computer-generated animations

We report a new procedure for assessing complex self-motion perception. In three experiments, subjects manipulated a 6 degree-of-freedom magnetic-field tracker which controlled the motion of a virtual avatar so that its motion corresponded to the subjects' perceived self-motion. The real-time animation created by this procedure was stored using a virtual video recorder for subsequent analysis. Combined real and illusory self-motion and vestibulo-ocular reflex eye movements were evoked by cross-coupled angular accelerations produced by roll and pitch head movements during passive yaw rotation in a chair. Contrary to previous reports, illusory self-motion did not correspond to expectations based on semicircular canal stimulation. Illusory pitch head-motion directions were as predicted for only 37% of trials; whereas, slow-phase eye movements were in the predicted direction for 98% of the trials. The real-time computer-generated animations procedure permits use of naive, untrained subjects who lack a vocabulary for reporting motion perception and is applicable to basic self-motion perception studies, evaluation of motion simulators, assessment of balance disorders and so on.

Non-NASA Center↗

Dynamic Visual Acuity: a Functionally Relevant Research Tool

Coordinated movements between the eyes and head are required to maintain a stable retinal image during head and body motion. The vestibulo-ocular reflex (VOR) plays a significant role in this gaze control system that functions well for most daily activities. However, certain environmental conditions or interruptions in normal VOR function can lead to inadequate ocular compensation, resulting in oscillopsia, or blurred vision. It is therefore possible to use acuity to determine when the environmental conditions, VOR function, or the combination of the two is not conductive for maintaining clear vision. Over several years we have designed and tested several tests of dynamic visual acuity (DVA). Early tests used the difference between standing and walking acuity to assess decrements in the gaze stabilization system after spaceflight. Supporting ground-based studies measured the responses from patients with bilateral vestibular dysfunction and explored the effects of visual target viewing distance and gait cycle events on walking acuity. Results from these studies show that DVA is affected by spaceflight, is degraded in patients with vestibular dysfunction, changes with target distance, and is not consistent across the gait cycle. We have recently expanded our research to include studies in which seated subjects are translated or rotated passively. Preliminary results from this work indicate that gaze stabilization ability may differ between similar active and passive conditions, may change with age, and can be affected by the location of the visual target with respect to the axis of motion. Use of DVA as a diagnostic tool is becoming more popular but the functional nature of the acuity outcome measure also makes it ideal for identifying conditions that could lead to degraded vision. By doing so, steps can be taken to alter the problematic environments to improve the man-machine interface and optimize performance.

Peters, Brian T.↗

Human otolith-ocular reflexes during off-vertical axis rotation: effect of frequency on tilt-translation ambiguity and motion sickness

The purpose of this study was to examine how the modulation of tilt and translation otolith-ocular responses during constant velocity off-vertical axis rotation varies as a function of stimulus frequency. Eighteen human subjects were rotated in darkness about their longitudinal axis 30 degrees off-vertical at stimulus frequencies between 0.05 and 0.8 Hz. The modulation of torsion decreased while the modulation of horizontal slow phase velocity (SPV) increased with increasing frequency. It is inferred that the ambiguity of otolith afferent information is greatest in the frequency region where tilt (torsion) and translational (horizontal SPV) otolith-ocular responses crossover. It is postulated that the previously demonstrated peak in motion sickness susceptibility during linear accelerations around 0.3 Hz is the result of frequency segregation of ambiguous otolith information being inadequate to distinguish between tilt and translation.

NASA Discipline Neuroscience↗

Instability of ocular torsion in zero gravity - Possible implications for space motion sickness

It is proposed that study of the eye torsion reflex and its behavior under novel gravitational states may possibly provide the basis for a long-sought test to predict space motion sickness (SMS). Measures of eye torsion such as ocular counterrolling and spontaneous eye torsion, were examined during hypo- and hypergravity in parabolic flight on the NASA KC-135 aircraft. Ten subjects, including two astronauts, one who had experienced SMS and one who had not, were ranked according to scores of torsional inability at 0 G and divided into two equal groups of high and low susceptibility to SMS. At 1.8 G the groups were significantly different in both the instability measure and the measure of torsional ability. No differences were detected in eye torsion in either 0 G or 1.8 G and none of the tests were significantly different in 1 G. Results suggest that tests of eye torsion on the KC-135 might differentiate those who would experience SMS from those who would not, although it is noted that this is not yet proven.

Diamond, Shirley G.↗

Functional organization of primate translational vestibulo-ocular reflexes and effects of unilateral labyrinthectomy

Translational vestibulo-ocular reflexes (trVORs) are characterized by distinct spatio-temporal properties and sensitivities that are proportional to the inverse of viewing distance. Anodal (inhibitory) labyrinthine stimulation (100 microA, < 2 s) during motion decreased the high-pass filtered dynamics, as well as horizontal trVOR sensitivity and its dependence on viewing distance. Cathodal (excitatory) currents had opposite effects. Translational VORs were also affected after unilateral labyrinthectomy. Animals lost their ability to modulate trVOR sensitivity as a function of viewing distance acutely after the lesion. These deficits partially recovered over time, albeit a significant reduction in trVOR sensitivity as a function of viewing distance remained in compensated animals. During fore-aft motion, the effects of unilateral labyrinthectomy were more dramatic. Both acute and compensated animals permanently lost their ability to modulate fore-aft trVOR responses as a function of target eccentricity. These results suggest that (1) the dynamics and viewing distance-dependent properties of the trVORs are very sensitive to changes in the resting firing rate of vestibular afferents and, consequently, vestibular nuclei neurons; (2) the most irregularly firing primary otolith afferents that are most sensitive to labyrinthine electrical stimulation might contribute to reflex dynamics and sensitivity; (3) inputs from both labyrinths are necessary for the generation of the translational VORs.

Non-NASA Center↗

Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt

Model simulations of the squirrel monkey vestibulo-ocular reflex (VOR) are presented for two motion paradigms: constant velocity eccentric rotation and roll tilt about a naso-occipital axis. The model represents the implementation of three hypotheses: the "internal model" hypothesis, the "gravito-inertial force (GIF) resolution" hypothesis, and the "compensatory VOR" hypothesis. The internal model hypothesis is based on the idea that the nervous system knows the dynamics of the sensory systems and implements this knowledge as an internal dynamic model. The GIF resolution hypothesis is based on the idea that the nervous system knows that gravity minus linear acceleration equals GIF and implements this knowledge by resolving the otolith measurement of GIF into central estimates of gravity and linear acceleration, such that the central estimate of gravity minus the central estimate of acceleration equals the otolith measurement of GIF. The compensatory VOR hypothesis is based on the idea that the VOR compensates for the central estimates of angular velocity and linear velocity, which sum in a near-linear manner. During constant velocity eccentric rotation, the model correctly predicts that: (1) the peak horizontal response is greater while "facing-motion" than with "back-to-motion"; (2) the axis of eye rotation shifts toward alignment with GIF; and (3) a continuous vertical response, slow phase downward, exists prior to deceleration. The model also correctly predicts that a torsional response during the roll rotation is the only velocity response observed during roll rotations about a naso-occipital axis. The success of this model in predicting the observed experimental responses suggests that the model captures the essence of the complex sensory interactions engendered by eccentric rotation and roll tilt.

NASA Discipline Neuroscience↗

Three-dimensional organization of vestibular related eye movements to rotational motion in pigeons

During rotational motions, compensatory eye movement adjustments must continually occur in order to maintain objects of visual interest as stable images on the retina. In the present study, the three-dimensional organization of the vestibulo-ocular reflex in pigeons was quantitatively examined. Rotations about different head axes produced horizontal, vertical, and torsional eye movements, whose component magnitude was dependent upon the cosine of the stimulus axis relative to the animal's visual axis. Thus, the three-dimensional organization of the VOR in pigeons appears to be compensatory for any direction of head rotation. Frequency responses of the horizontal, vertical, and torsional slow phase components exhibited high pass filter properties with dominant time constants of approximately 3 s.

NASA Discipline Neuroscience↗

Binocular Coordination of the Human Vestibulo-Ocular Reflex during Off-axis Pitch Rotation

Head movements in the sagittal pitch plane typically involve off-axis rotation requiring both vertical and horizontal vergence ocular reflexes to compensate for angular and translational motion relative to visual targets of interest. The purpose of this study was to compare passive pitch VOR responses during rotation about an Earth-vertical axis (canal only cues) with off-axis rotation (canal and otolith cues). Methods. Eleven human subjects were oscillated sinusoidally at 0.13, 0.3 and 0.56 Hz while lying left-side down with the interaural axis either aligned with the axis of rotation or offset by 50 cm. In a second set of measurements, twelve subjects were also tested during sinusoidally varying centrifugation over the same frequency range. The modulation of vertical and horizontal vergence ocular responses was measured with a binocular videography system. Results. Off-axis pitch rotation enhanced the vertical VOR at lower frequencies and enhanced the vergence VOR at higher frequencies. During sinusoidally varying centrifugation, the opposite trend was observed for vergence, with both vertical and vergence vestibulo-ocular reflexes being suppressed at the highest frequency. Discussion. These differential effects of off-axis rotation over the 0.13 to 0.56 Hz range are consistent with the hypothesis that otolith-ocular reflexes are segregated in part on the basis of stimulus frequency. At the lower frequencies, tilt otolith-ocular responses compensate for declining canal input. At higher frequencies, translational otolith-ocular reflexes compensate for declining visual contributions to the kinematic demands required for fixating near targets.

Wood, S. J.↗

Some of the mechanisms underlying motion sickness

Some of the mechanisms contributing to the occurrence of motion sickness are discussed. It is stated that the primary factor is a loss of stability in the vestibular system caused by repetitive sensory inputs that are abnormal in terms of the central vestibular patterning encountered. Evidence is presented supporting the opinion that motion sickness is an epiphenomenon superimposed on any responses in the reflex category due to vestibular influences that cross a temporary linkage to reach nonvestibular sites where first-order motion sickness symptoms have their immediate origin.

Graybiel, A.↗

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 0G. 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, evidence is presented that susceptibility to motion sickness during exposure to visual inversion is decreased in a 0G relative to 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.

Lackner, James R.↗

Vestibulo-spinal reflex mechanisms

The specific objectives of experiments designed to investigate postural reflex behavior during sustained weightlessness are discussed. The first is to investigate, during prolonged weightlessness with Hoffmann response (H-reflex) measurement procedures, vestibulo-spinal reflexes associated with vestibular (otolith) responses evoked during an applied linear acceleration. This objective includes not only an evaluation of otolith-induced changes in a major postural muscle but also an investigation with this technique of the adaptive process of the vestibular system and spinal reflex mechanisms to this unique environment. The second objective is to relate space motion sickness to the results of this investigation. Finally, a return to the vestibulo-spinal and postural reflexes to normal values following the flight will be examined. The flight experiment involves activation of nerve tissue (tibial N) with electrical shock and the recording of resulting muscle activity (soleus) with surface electrodes. Soleus/spinal H-reflex testing procedures will be used in conjuction with linear acceleration through the subject's X-axis.

Reschke, M. F.↗

Ground-based training for the stimulus rearrangement encountered during spaceflight

Approximately 65-70% of the crew members now experience motion sickness of some degree during the first 72 h of orbital flight on the Space Shuttle. Lack of congruence among signals from spatial orientation systems leads to sensory conflict, which appears to be the basic cause of space motion sickness. A project to develop training devices and procedures to preadapt astronauts to the stimulus rearrangements of microgravity is currently being pursued. The preflight adaptation trainers (PATs) are intended to: demonstrate sensory phenomena likely to be experienced in flight, allow astronauts to train preflight in an altered sensory environment, alter sensory-motor reflexes, and alleviate or shorten the duration of space motion sickness. Four part-task PATs are anticipated. The trainers are designed to evoke two adaptation processes, sensory compensation and sensory reinterpretation, which are necessary to maintain spatial orientation in a weightless environment. Recent investigations using one of the trainers indicate that self-motion perception of linear translation is enhanced when body tilt is combined with visual surround translation, and that a 270 degrees phase angle relationship between tilt and surround motion produces maximum translation perception.

Non-NASA Center↗