5
Sensorimotor Integration

Introduction

On Earth, the force of gravity is an omnipresent influence on the physiology and behavior of organisms. Sensorimotor integration plays a key role in posture and movement control, locomotion, object manipulation, and tool use in an environment containing gravity torques that vary with body orientation and configuration. In the Goldberg report,1 the section on sensorimotor integration focused on five areas, including mechanisms of spatial orientation, postural control, vestibulo-ocular reflexes, vestibular processing, and space motion sickness. During the last 10 years, extensive experimental research has been performed in all of these areas. In particular, considerable progress has been made in understanding how the vestibulo-ocular reflex, gaze control, and thresholds for angular and linear accelerations are affected by exposure to microgravity in humans. This chapter reviews the major advances in these fields, followed by recommendations for future investigations on these and related areas of research.

Spatial Orientation

Accurate determination of the body's position relative to the external environment is critical in controlling body movements and posture, as well as for interacting with objects in the environment. On Earth, gravity plays a fundamental role in spatial orientation, accelerating the body downward. Multimodal sensory stimuli2 and motor feedback3 are important factors in the appreciation and regulation of body orientation. Extensive research has already been performed to evaluate the relative contributions of visual, vestibular, and tactile stimuli to the perception of self-orientation and motion before, during, and after spaceflight. In terrestrial experiments, moving visual stimuli are commonly used to induce illusions of self-motion and tilt in stationary subjects. These experiments permit an evaluation of the relative contributions visual and vestibular cues make in the perception of body orientation. The



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--> 5 Sensorimotor Integration Introduction On Earth, the force of gravity is an omnipresent influence on the physiology and behavior of organisms. Sensorimotor integration plays a key role in posture and movement control, locomotion, object manipulation, and tool use in an environment containing gravity torques that vary with body orientation and configuration. In the Goldberg report,1 the section on sensorimotor integration focused on five areas, including mechanisms of spatial orientation, postural control, vestibulo-ocular reflexes, vestibular processing, and space motion sickness. During the last 10 years, extensive experimental research has been performed in all of these areas. In particular, considerable progress has been made in understanding how the vestibulo-ocular reflex, gaze control, and thresholds for angular and linear accelerations are affected by exposure to microgravity in humans. This chapter reviews the major advances in these fields, followed by recommendations for future investigations on these and related areas of research. Spatial Orientation Accurate determination of the body's position relative to the external environment is critical in controlling body movements and posture, as well as for interacting with objects in the environment. On Earth, gravity plays a fundamental role in spatial orientation, accelerating the body downward. Multimodal sensory stimuli2 and motor feedback3 are important factors in the appreciation and regulation of body orientation. Extensive research has already been performed to evaluate the relative contributions of visual, vestibular, and tactile stimuli to the perception of self-orientation and motion before, during, and after spaceflight. In terrestrial experiments, moving visual stimuli are commonly used to induce illusions of self-motion and tilt in stationary subjects. These experiments permit an evaluation of the relative contributions visual and vestibular cues make in the perception of body orientation. The

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--> influence of simple rotating visual patterns (dots and stripes) in the frontal plane on the perceived vertical axis and perceived self-motion has been studied systematically in spaceflight and parabolic flight. 4 5 Although individual differences are considerable, the basic finding is that weightlessness enhances the magnitude of visually induced apparent roll of the body. Some individuals experience full 360° roll, which happens rarely on Earth. In orbital flight experiments, the enhanced effectiveness of visual stimuli for inducing apparent self-motion is thought to be related to the altered orientation cues from the otolith organs. On Earth, the otoliths respond to gravitoinertial acceleration by changing the pattern of their output signals, which provide information about head orientation relative to gravity. In microgravity, the otoliths are effectively unloaded and cannot provide information about static head orientation. The influence of tactile cues to the soles of the feet during rotary visual stimulation has been tested in spaceflight.6 In this situation, tactile stimulation is generated by a bungee cord apparatus that pulls the astronaut against the spacecraft deck. It was found that bungee loading could attenuate the sense of self-motion and tilt. In microgravity, astronauts often spontaneously experience spatial orientation illusions, especially during their initial exposure to weightlessness.7 In the second manned USSR flight, the cosmonaut Titov was the first to report an illusion of "feeling upside down" while in orbit. Other astronauts have since reported a variety of illusions involving virtually all possible combinations of self-orientation and vehicle orientation. Some of these effects are dependent on body orientation in relation to architecturally specified horizontals and verticals, such as the deck or walls of the spacecraft. If oriented with his or her head near the architectural "down," an astronaut may feel inverted in an upright craft. For some astronauts, the direction in which they perceive "down" corresponds to the direction their feet are pointing. For these individuals, changing the position of their feet shifts the apparent "down" direction. There are significant individual differences in the extent to which these orientation illusions are experienced, as well as fluctuations over time in their precise makeup.8 9 Researchers have attempted to relate the occurrence of orientation illusions to otolith function, especially the function of the saccule.10 11 12 At present, it is thought that a combination of visual and cognitive factors, tactile input, vestibular asymmetries, and the positioning of the feet all contribute to varying degrees in producing orientation illusions for different individuals, making it difficult to predict when orientation illusions will be experienced. 13 The otolith organs' sensitivity to linear acceleration in weightlessness has been evaluated for the three primary axes using linear sleds that can hold an astronaut in different sled orientations and provide controlled acceleration patterns.14 15 16 Overall, the results are variable, with in-flight decreases in the threshold for detection of linear acceleration in some individuals and increases in others, relative to preflight values. Postflight assessments show similar variability. In spaceflight, the detection time for reporting linear acceleration (i.e., the period of time between being accelerated and reporting a sensation of motion) seems to be lowered for the x and y axes and elevated for the z-axis.17 This could reflect decreased sensitivity of the sacculus, since the saccular receptor end organ is aligned with the z-axis of the head and is subject to constant shear when the head is in the upright position on Earth. On the other hand, somatosensory stimuli generated by contact forces between the astronaut's body and the sled apparatus could also play a role. Studies on the position sense of the limbs have been carried out both in parabolic flights and spaceflight.18 19 Position sense or limb proprioception is derived from afferent signals of the muscle spindles, and possibly also Golgi tendon organs and joint receptors, which are interpreted in relation to ongoing patterns of muscle activity. On Earth, muscle spindle sensitivity is influenced by head orientation, which is detected by the otoliths and (through spinal cord connections) modulates the antigravity muscles of the body. Proprioception has been assessed by investigating the tonic vibration reflexes, which can be measured to determine muscle spindle gain. These reflexes are elicited by mechanically

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--> vibrating a muscle or its tendon with a physiotherapy vibrator. In parabolic flight tests, tonic vibration reflexes show immediate decreases on transition to 0 g, and increases in 2 g relative to 1-g straight-and-level flight.20 21 Kinematic studies of arm movement control, in which subjects attempt during parabolic flight to repeat arm movements practiced preflight, also suggest diminished muscle spindle gain in microgravity, at least during initial exposure. Rhythmic movements made in 0 g tend to be of smaller amplitude and have more frequent dynamic overshoots than in 1 g, both for horizontal and vertical forearm orientations (relative to the subject).22 This pattern is consistent with decreased spindle gain, and consequently decreased damping of limb movements. Diminished muscle spindle sensitivity is consistent with the frequent reports that position sense of the limbs is degraded in weightless conditions.23 During spaceflight, there may be a gradual change in the perceptual interpretation of proprioceptive signals. Initially, vibration of leg muscles of a test subject, who is attached to the deck with foot supports and restrained in position, leads to illusory tilt of the body. On the ground, this would occur under comparable conditions. However, later in-flight such vibration leads to sensations that the deck is tilting or rising under the subject's feet, depending on the muscles stimulated. 24 Lifting and manipulating objects is also an important aspect of limb movement control. Studies of the ability to discriminate between differences in the mass of objects having similar size and appearance by hefting them show degradations of performance in microgravity conditions.25 26 If the hefting frequency is increased, performance improves considerably.27 Rapid arm movements are known to be less dependent for their accurate execution on muscle spindle feedback and are less impaired than slow movements in microgravity. Consequently, the degradation in mass discrimination associated with slow movements likely reflects errors in resolution of limb trajectory, at least in part. Subjects experience postflight increases in the apparent heaviness of hefted objects and of the body and limbs. This change points to central nervous system reinterpretations of the apparent effort associated with supporting the limbs or holding up objects against gravity. Summary and Recommendations Considerable progress has been made in determining thresholds for perception of linear and angular acceleration under conditions of passive body motion in microgravity. The relative influences of visual and tactile stimulation on perceived orientation under passive conditions have been determined. Researchers have also made progress in understanding how microgravity affects limb position sense. In the future, crewed space travel, especially interplanetary exploration, will probably involve transitions between different force backgrounds, with the need for adequate sensorimotor performance and orientation control in each force level. To meet such demands will require an understanding of how human spatial behavior is affected during active body movement by transitions to different force levels and how adaptation is achieved. This will also be an important issue when Space Station Freedom becomes a permanent orbiting facility and astronauts travel back and forth between it and Earth. The deleterious effects of microgravity on bone and muscle physiology despite exercise countermeasures (described in other sections of this report) also raise the possibility that some form of artificial gravity will be necessary to ensure the success of long-term missions. There is a critical need to evaluate the influence of microgravity and other non-1-g force levels on the integrative coordination of complex body activities, including reaching and locomotory movements involving combinations of eye, head, torso, arm, and leg activity. Studies should be performed before, during, and after spaceflight so that initial disruptions and the time course of adaptation and readaptation can be identified.

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--> It is important for the success of long-duration space missions (e.g., crewed flights to Mars) to determine the sensory, motor, and cognitive factors influencing the ability to adapt and to retain adaptation to different force backgrounds. These experiments can be conducted on the International Space Station, in rotating environments, and in parabolic flight. Neural coding of spatial navigation may be affected by a change from a 1-g to a microgravity force background and may relate to some of the orientation illusions experienced by astronauts. The influence of altered force levels on orientation and geographical localization should be explored in parallel experiments with humans and animals. Ground-based centrifuges, body-loading paradigms, parabolic flight conditions, virtual reality conditions, and eventually orbital flight should be utilized for testing. The relative contribution of different sensory modalities and motor factors in influencing perceived orientation and body configuration in various force environments should be determined for conditions involving active postural control in astronauts. Posture And Locomotion The control of stance and locomotion is complex and involves vestibular, somatosensory, proprioceptive, visual, and motor mechanisms. Regulation of stance differs greatly under terrestrial and spaceflight conditions. Static balance on Earth requires maintaining the projection of the body's center of mass within the support area defined by the feet. When arm movements are made during static balance, anticipatory innervations of leg muscles compensate for the impending reaction torques and the changes in location and projection of the center of mass associated with the voluntary arm movements. Arm raising has been used in-flight with the subject's feet secured to the deck to determine whether exposure to microgravity affects the pattern of anticipatory compensations usually associated with arm-raising maneuvers.28 29 Initially, similar patterns are seen preflight and in-flight in terms of the muscle groups and timing of activity involved. This means that compensation both for dynamic and static influences of rapid arm raising still occurs early in spaceflight, although the latter is functionally unnecessary. On later flight days, the activation of the extensor component (e.g., soleus and gastrocnemius) is reduced, indicating that the compensation for a shift of center of mass (which is physically unnecessary in weightless conditions) no longer occurs. On Earth, rapidly bending the trunk forward and backward at the waist is accompanied by backward and forward displacements of the hips and knees to maintain balance. Similar trunk movements made in-flight with the feet attached to the deck show the same compensatory movements of the hips and knees, with kinematics corresponding to those that occur under terrestrial conditions. These in-flight movements must reflect reorganized patterns of muscle activation, because the the innervations necessary to achieve these axial synergies in microgravity are considerably different from those needed on Earth, given the absence of effective gravity torques in orbital flight.30 31 Initially, the basic stance patterns adopted in-flight when the feet are attached to the deck differ little from those on Earth. However, later on in-flight a more pitched forward posture appears that reflects decreased extensor tonus and increased flexor activity.32 This change is consistent with the gradual shift mentioned above in the interpretation of proprioceptive signals associated with leg muscle vibration.33 In microgravity, deep knee bends or raising and lowering the whole body with the feet anchored can evoke illusions of deck displacement. 34 The deck seems to move downward as the body moves toward it and upward as the body moves away from it. The reverse pattern occurs with exposure to high force levels. These illusions probably result from the altered relationship between motion of the body, the muscle forces necessary to produce that motion, and the associated muscle spindle feedback from

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--> the muscles.35 With repeated movements, adaptation takes place so that apparent stability of the "support surface" is regained during such deep knee bends. This adaptation may entail a remapping of muscle spindle and muscle innervation signals in the generation of limb position sense. Two reflexes that test the status of otolith spinal modulation of the antigravity muscles have been evaluated in spaceflight: the H-reflex (Hoffman's reflex) and the otolith-spinal reflex. The H-reflex is an index of the excitability of alpha motoneurons and is elicited by electrical stimulation in the popliteal fossa of muscle spindle afferent fibers from the gastrocnemius muscle. Initially in-flight, the H-reflex shows little change from 1-g baseline during bungee cord-induced "falls" in which the astronaut is briefly accelerated toward his or her feet, but later on the amplitude of the astronaut's reflex response diminishes.36 37 In addition, there are subjective changes that make later "falls" feel stronger and faster. The otolith-spinal response to bungee cord "falls" is lower than preflight and continues to diminish over subsequent flight days.38 39 The H-reflex has not been tested immediately after an astronaut lands back on Earth. However, the otolith-spinal reflex, measured by electromyography from the gastrocnemiussoleus muscles during the astronaut's sudden acceleration toward his or her feet, was inhibited as soon as weightlessness was achieved and declined further during the flight, but it was unchanged from preflight levels when measured shortly after the astronaut's return to Earth.40 The in-flight decreases in the otolith-spinal and H-reflexes are consistent with observations made in transient periods of weightlessness in parabolic flight. Postflight measurements of posture and locomotion were first made during the Apollo and Skylab missions.41 In these early missions, the astronauts were parachuted to Earth in a reentry capsule and recovered at sea. The severity and operational seriousness of reentry disturbances of posture and locomotion have become apparent in the space shuttle missions. Some astronauts (especially those returning from longer missions) have been unable to walk unaided immediately after landing and could not make a rapid egress in case of emergency. Postflight static posture exhibits a considerable increase in sway amplitude. On rail tests (i.e., standing heel-to-toe on rails of various widths to determine the least area necessary for balance), performance is decreased for more than 7 days postflight relative to preflight levels.42 43 44 Tests of postural responses to displacements of the support surface in translation and in rotation show considerable postflight decrements in terms of overshoots of the trunk and undershoots of the hips, and an increase in time needed to settle into a new stable posture.45 46 Tests in which platform motion and the visual surround can be manipulated independently or with sway referencing of vision (platform and visual motion spatially linked) show serious postflight decrements. This pattern of results is consistent with decreased vestibular and ankle proprioceptive contributions to balance and with increased reliance on vision.47 48 Recovery of balance control seems to follow a double exponential time course, with considerable improvement in balance within the first 12 hours or so after landing and a much more gradual return toward preflight baseline thereafter. Full recovery can take weeks. Postflight studies of locomotion involving treadmill walking indicate that the timing of both toe-off and heel-strike components are much more variable immediately after landing.49 50 These are phases of the step cycle in which accurate neural control is important because of the great energy transfer involved. Astronauts returning from their first spaceflight also show greater eye and head instability during treadmill locomotion than more experienced astronauts. These gaze instabilities have important practical implications for performing a rapid and safe egress after reentry, as do the alterations in locomotory transport timing. Head movements, especially in pitch and roll, can evoke apparent visual motion and disorientation during and after reentry.51 52 Alterations in the motor control of the head and its relationship with oculomotor control occur in spaceflight because the head is weightless and adaptive changes in control are necessary in the absence of gravity torques. On

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--> reentry, the return of a g-load on the head is probably responsible for many aspects of postflight gaze instabilities. Postflight locomotory disturbances are commonplace and include feelings of bobbing of the ground during stepping, an inability to walk in a straight line with eyes closed, loss of balance when turning corners, and the sense that movements require extra "effort."53 54 The difficulty in making turns has a perceptual component known as the "giant hand" effect, which feels as if some external force is making the body deviate from its intended course. An analogous phenomenon can be experienced during disorientation in aircraft, when the controls do not feel as if they are responding appropriately because a "giant hand" is tilting the aircraft. Similar processes may be involved in the two types of illusions.55 Attempts have been made to relate postflight disturbances of head and locomotory control to central reinterpretations of otolith function. 56 57 58 59 The basic notion is that static head tilt in spaceflight is no longer associated with modulation of otolith output. Consequently, the central nervous system reinterprets all changes in otolith activity as indicating linear translation and oculomotor, postural, and subjective responses are remapped in accordance with the reinterpreted otolith output. After return from spaceflight, persistence of this remapping would mean that tilting movements of the head would initially be interpreted as linear translation—for example, a forward head tilt would be interpreted as backward translation of the head, because the same otolith displacement would result from an actual linear acceleration of the head backward. Such reinterpretation of otolith output, although conceptually appealing, is unlikely to be the sole factor responsible for the postflight illusions evoked by head movements, because the magnitude, character, and time course of the perceptual responses are not completely appropriate. Some of the confounding factors that need to be considered in interpreting reentry disturbances—especially for flights lasting more than several days—are the alterations in muscle fiber type and the decreases in muscle strength and muscle mass that occur during spaceflight. Such changes (along with alterations in sensorimotor control mechanisms, brain maps of motor control, and somatosensation) could all be contributing factors to postflight postural and locomotory deficits. Summary and Recommendations The severe reentry disturbances of posture and locomotion that astronauts and cosmonauts exhibit after even relatively brief spaceflights pose potentially dangerous operational problems. These disturbances would be especially critical in long-duration missions involving transitions between force levels on arrival, coupled with the need for accurate postural, locomotory, and prehension control. The time course of postural and locomotory adaptation to variations in background force level and to variations in effective body weight should be determined. Attention should be paid to determining whether the rate of adaptation is affected by age. Techniques should be developed to provide ancillary sensory inputs or aids to heighten postural and locomotory control and to hasten adaptation during transitions between gravitational force environments. Animal models of reentry disturbances could be developed to elucidate the underlying physiological processes. Vestibulo-Ocular Reflexes And Oculomotor Control The vestibulo-ocular reflexes (VORs) are important for controlling the direction of gaze (eye and head position relative to space) during active and passive movements of the head, as well as those of the

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--> head and body. They are mediated by the semicircular canals of the inner ear, which are activated by angular acceleration; by the otolith organs, which are sensitive to gravitoinertial acceleration; and (to a lesser extent) by neck proprioceptive inputs. Both semicircular canal and otolith-driven eye movements have been studied in spaceflight. Caloric irrigation of the external ear canal (with hot or cold water, or with air) can be used under terrestrial conditions to stimulate the horizontal semicircular canals and other sources, depending on the mode of body motion. Irrigation leads to a pattern of rhythmic eye movements known as nystagmus, consisting of slow and fast phases. Such nystagmus is thought to result from density differences between the endolymph and cupula of the canal created by the thermal stimulus, thus rendering the canal "sensitive" to gravity. Caloric irrigation was first used in the Spacelab-1 flight, and nystagmus was elicited. 60 61 This response was surprising, since the generally accepted thermoconvection theory of Barany predicts that density differences should be irrelevant in weightlessness. Subsequent observations, made with controls for noise levels and other possible artifacts, have confirmed the original finding and support the view that there may be a direct thermal effect on canal activity.62 63 Swivel or yaw head movements stimulate the semicircular canals and elicit compensatory eye movements in the direction opposite to the displacement of the head. The yaw VOR has been studied with voluntary head movements during attempted visual fixation at frequencies from 0.25 to 1.0 Hz.64 Few changes are apparent in-flight, other than a slight decrease in gain. The yaw VOR for passive rotation has been studied systematically in parabolic and orbital flight.65 66 The basic finding is that gravitoinertial force level has no influence on the peak slow-phase velocity of the nystagmus elicited by sudden deceleration to rest. This means that the peripheral response of the semicircular canals is not influenced by alterations in linear background force—at least not by brief exposures. The time constant of nystagmus decay has been studied in weightlessness and at greater than 1-g force levels to evaluate "velocity storage."67 Velocity storage refers to the observation that the nystagmus response to a velocity step outlasts the physical return of the cupula-endolymph system of the semicircular canal to resting levels. Velocity storage is thought to reflect the midbrain integration of a velocity signal originating from the semicircular canals.68 The overall eye movement response is thought to reflect the contribution of a "direct pathway" from the canal as well as velocity storage activity from an "indirect pathway." When the otolith organs are ablated, velocity storage is abolished.69 Interestingly, under microgravity conditions in spaceflight and the microgravity phases of parabolic flights, the time constant of nystagmus decay is significantly shorter than on Earth.70 71 This suggests that the velocity storage mechanism is sensitive to linear acceleration. The time constant is also shorter in a 1.8-g force background, showing that departures in either direction from 1 g tend to suppress storage.72 The three-dimensional organization of velocity storage is also influenced by gravity. The attenuation of postrotary nystagmus by tilting of the head (so-called "dumping" of velocity storage) appears to be absent during brief as well as prolonged exposure to microgravity.73 74 Velocity storage can also be generated by visually driven eye movements. Motion of a large portion of the visual field elicits tracking movements of the eyes followed by rapid eye flick, known as optokinetic nystagmus. If the background illumination is eliminated, eye movements will persist in darkness for some seconds. This phenomenon of optokinetic after-nystagmus is another index of velocity storage.75 Optokinetic after-nystagmus is also attenuated and spatially drifts in microgravity—further evidence for a gravity dependence of velocity storage.76 VOR responses to voluntary head oscillation in pitch vary and are hard to interpret because the data have so much intra- and interindividual variability.77 78 Adequate on-axis studies to separate otolith and canal contributions have not yet been done in spaceflight. On Earth, static tilts of the head evoke counterrolling of the eyes in the direction opposite the head tilt. This effect is mediated by the otolith organs. Dynamic tilts of the head stimulate the semicircular

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--> canals as well and elicit a torsional VOR.79 Linear acceleration along the y-axis of the head (the orientation that runs through the ears) can also evoke torsion of the eyes. Astronauts and cosmonauts show diminished ocular counterrolling during static head tilts after return from spaceflight.80 81 The reduction can persist for 10 days or more following flights lasting more than several weeks. Postflight assessments using a linear sled also show diminished torsional responses. 82 Rhesus monkeys show postflight reduction of ocular counterrolling as well.83 Observations of the torsional VOR elicited by voluntary head movements during spaceflight suggest initial decreases in gain followed by increases to levels even greater than preflight values. 84 In general, all of the postflight VOR assessments both for angular and linear stimulation are consistent with a decreased contribution of otolith function to the responses. Optokinetic, voluntary pursuit, and saccadic eye movements have all been studied in spaceflight and parabolic flight.85 86 87 88 89 90 Optokinetic responses tend to vary, with some individuals showing changes and others not. There are occasional reports of astronauts and cosmonauts exhibiting a spontaneous vertical or horizontal nystagmus during spaceflight.91 Studies of pursuit eye movements so far have found that horizontal pursuit is not affected by weightlessness either for head-fixed or head-free test conditions.92 Striking changes can occur in vertical pursuit, however. Upward pursuit is accomplished in-flight mainly by saccadic eye movements and downward pursuit by a combination of smooth pursuit and saccades. Saccadic eye movements tend to display increased latencies and decreased peak velocities relative to preflight control values. Summary and Recommendations Considerable progress has been made in understanding how microgravity affects vestibulo-ocular behavior and control of gaze in humans, and experiments using primates have also made gains. Future studies should be directed toward bringing experimental and theoretical closure to understanding vestibulo-ocular function under different background force levels. Systematic parametric studies of pursuit, saccadic, and optokinetic eye movements should be carried out as a function of background force level in humans from microgravity to 2 g. Human and animal experiments should be directed toward developing an adequate three-dimensional model of the VOR and velocity storage for both angular and linear accelerations in both space and ground-based environments. The coordination of eye-head-torso synergies should be evaluated in humans under different force backgrounds, including microgravity. Vestibular Processing During Microgravity Morphological data concerning potential changes in the vestibular end organs as a consequence of exposure to microgravity are scarce so far but point to significant changes that occur. In the rat, about a twofold increase in ribbon synapses of Type II hair cells and a 50 percent increase in Type I cell synapses of the otoliths have been found after 2 weeks of exposure to microgravity, compared with ground-based controls. The increased synaptic levels were still apparent in animals assayed 14 days postflight.93 By contrast, animals exposed to increased g levels through centrifugation exhibit decreased synaptic density levels.94 The functional significance of these synaptic changes has not been determined. Data on whether there are alterations in otoconia are less clear, with some studies suggesting that there are changes while others do not.

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--> Few data are available concerning the physiological activity of vestibular afferents in microgravity. Early observations did not have adequate controls that would allow conclusions to be drawn. Recent work is preliminary, with few animals tested so far.95 Two studies performed on Rhesus monkeys have reported a postflight increase in gain of the horizontal semicircular canal afferents after a 14-day mission, but no change in the gain of the horizontal VOR postflight or in velocity storage relative to preflight values. In contrast, experiments performed on two other monkeys from a different mission found a decrease in afferent gain postflight (M.J. Correia, personal communication, August 1996). Physiological data concerning activity at other levels of the vestibular pathways are lacking. Summary and Recommendations Very little is known about how exposure to weightlessness affects peripheral and central vestibular function and how development of the vestibular system (especially the otolith organs) would be affected. These are areas that warrant extensive study using animal models and state-of-the-art electrophysiological, morphological, and molecular biological approaches. The effect of altered calcium regulation in microgravity on otoconial development and regeneration should be determined using animal models. In-flight electrophysiological recordings of otolith afferent and efferent activity and signal processing within the brain should be made in test animals. This is best accomplished by a trained physiologist serving as a payload specialist. Space Motion Sickness Space motion sickness (SMS) affects at least 70 percent of astronauts on their first flights.96 An individual's susceptibility to space motion sickness seems to change little with widely separated repeat exposures. Most of the symptoms, with the exception of those characteristic of the Sopite syndrome (including extreme drowsiness, fatigue, lack of initiative, and apathy), abate within about 3 days.97 98 99 It is still not known whether SMS is a form of sickness fully analogous to terrestrial motion sickness.100 Some symptoms seem different from those expressed under provocative conditions on Earth. For example, sweating and pallor are rarely reported with SMS, but episodes of sudden vomiting without clear prodromal signs can occur. However, under terrestrial conditions, the pattern and expression of signs and symptoms of motion sickness are highly dependent on the provocativeness of the test situation, and "head symptoms" tend to predominate under mildly provocative conditions.101 Environmental factors also play a role. For example, in cool test conditions, sweating does not usually accompany motion sickness on Earth. Also, sudden vomiting can occur with terrestrial motion sickness, indicating that the lack of obvious symptoms is not equivalent to lack of sensitization.102 In fact, common features of SMS, including lack of appetite, apathy, fatigue, difficulty in sleeping, and irritability, are characteristic features of the Sopite syndrome, which occurs with prolonged exposure to relatively low-grade stimulation on Earth. It is not yet known how long the Sopite component of SMS persists. Reports of mal de barquement, the renewed symptoms of motion sickness after returning from spaceflight, tend to strengthen the analogy between SMS and terrestrial motion sickness. The incidence of symptoms is about 90 percent in cosmonauts returning from missions lasting several months.103 Movements of the head or of the head and body under weightless conditions are generally considered causal factors in evoking and exacerbating SMS.104 In fact, head movements made during exposure

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--> to altered g levels, both for decreases and increases relative to 1 g, are provocative.105 Their influence is compounded at 2 g, compared with 0-g force backgrounds. Off-axis head movements made during rotation generate unusual stimulation of the semicircular canals, known as Coriolis cross-coupling stimulation. Such stimulation occurs because as the head moves out of the plane of rotation, one set of canals also moves out of the plane of rotation and loses angular momentum and another set is brought toward the plane of rotation and gains angular momentum. This causes both sets of canals to signal rotation simultaneously but about different head axes, whereas the remaining pair of canals appropriately signals the tilting of the head. Such cross-coupling stimulation can cause profound nausea and is disorienting when head movements are made during high velocities of rotation on Earth. By contrast, head movements made at high velocities of rotation (20 to 25 rpm) after 6 days in spaceflight are not at all nausea-inducing or disorienting.106 Unfortunately, tests have not been carried out on earlier mission days. However, in parabolic flight, susceptibility to cross-coupling stimulation changes virtually immediately as a function of g level, with head movements during rotation being much less provocative in 0 g and much more so in 1.8 g than in straight-and-level flight.107 These force-dependent variations likely reflect factors related both to the altered sensorimotor control of the head and to the changes in otolith activity as a function of force level, given that input to the semicircular canals is kept constant in these studies.108 Subjective reports suggest that visual factors can also influence the development of SMS. For example, when astronauts are upside down in relation to the architectural ceiling of the spacecraft, or see other astronauts upside down in relation to themselves, they may develop symptoms.109 110 This is especially true for astronauts who are visually dependent, i.e., down is where the visual architectural floor is, as opposed to astronauts who tend to perceive the "down" direction as corresponding to where their feet are located.111 Biofeedback control of SMS has been suggested as a means of decreasing or preventing SMS as well as terrestrial motion sickness.112 Unfortunately, this approach has not proven successful in spaceflight. Terrestrial experiments reported to be successful in using biofeedback to control motion sickness have lacked appropriate controls for physiological changes associated with movement activity levels, initial susceptibility, and adaptation effects associated with repeated exposure conditions. The electro-gastrogram (EGG) has been suggested as a potential physiological index of the presence and severity of motion sickness, because tachygastria has been reported to be related to the onset of nausea.113 If this were consistently the case, monitoring the EGG could serve as an objective predictor of impending SMS. However, studies using controls for anxiety level that have attempted to relate symptom development and severity with changes in the EGG have failed to find a consistent correlation between EGG changes and the development of motion sickness. 114 Progress in understanding SMS is hampered by the lack of adequate understanding of the physiological bases of motion sickness115 116 117 118 and by the lack of adequate theories.119 120 121 Current sensory-conflict theories provide useful characterizations of the condition without offering new directions to pursue for its control. One factor that correlates with severity of motion sickness in parabolic flight is the magnitude of velocity storage, as assessed by the extent of suppression of postrotary nystagmus by head tilt.122 This is a potential link with physiological mechanisms known to be involved in eliciting motion sickness and that are altered in spaceflight, but this finding has not been pursued. SMS can be controlled operationally by intramuscular injections of promethazine at dose levels established from parabolic flight studies. 123 124 125 The extreme drowsiness generally associated with promethazine during ground-testing is generally not reported in either spaceflight or parabolic flight. This may be partially attributed to the excitement inherent in being in such situations.

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--> Summary and Recommendations Space motion sickness is usually an operational problem for the first 72 hours of flight and can be controlled with intramuscular drug injections. Nevertheless, it is hazardous for the initial transition between different gravitational force environments. An understanding of its etiology is also important for determining human adaptability to novel environments. Moreover, the Sopite syndrome component of SMS may be a factor in generating interpersonal friction in the restrictive and stressful space environment. The use of virtual environments in space to augment training in long-duration missions and for extravehicular activities (EVAs) or for experimental purposes will likely exacerbate motion sickness. Mal de barquement may also occur in transitions between background force levels and is a potential operational problem for entry or reentry after long-duration missions. The relationship of motion sickness to altered sensorimotor control of the head and body as a function of altered force background and effective body weight should be assessed. The possibility of maintaining dual adaptations to more than one force background simultaneously—allowing transitions between them without performance decrements—should be explored. Combined physiological and morphological studies using animal models should be performed to investigate the interaction between the vestibular system and autonomic function, including cardiovascular regulation. The time course of the Sopite syndrome component of space motion sickness should be definitively established. Testable models should be developed that integrate current knowledge of terrestrial and space motion sickness. Central Nervous System Reorganization There is compelling evidence that cortical maps of both sensory and motor functions are highly plastic and subject to rapid reorganization. 126 Such plasticity occurs at many relay stations in the central nervous system, not just the cortex. The functional implications and consequences of such reorganizations are not understood fully under terrestrial conditions, let alone in spaceflight. Extended spaceflight must produce sensorimotor remappings. Preliminary studies should be undertaken to evaluate their implications and significance for both in-flight and postflight performance. Recommendations Pre- and postflight fMRI studies should be conducted with astronauts to determine the effects of microgravity on cortical maps. Bed-rest studies may also serve as useful models for inducing sensory-motor reorganizations. Test strategies should be developed to determine the sensorimotor and cognitive consequences of central nervous system reorganizations resulting from exposure to microgravity and their implications for reentry disturbances. Teleoperation And Telepresence Virtual environment technology has made it possible to create compelling artificial situations for training and operational purposes.127 Many relevant aspects of real environments can be reproduced,

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--> creating important possibilities for teleoperation, teleexploration, and learning the layout of real environments from virtual ones. Telepresence is the sense of being physically present in a remote environment removed from an actual location. It can be induced using virtual environment technology. Virtual environments will probably be used increasingly often in preflight training and in-flight rehearsal and training for mission tasks, including familiarization with equipment and environment. Recommendation The extent to which telepresence is helpful in controlling equipment and robots in a remote environment should be determined. General Strategic Issues NASA Life Science has been following a strategy of focusing on key problem areas using coordinated series of studies, such as in the Spacelab and Neurolab missions. This is an important approach and should be continued. The following recommendations will enhance the progress already made. Recommendations Systematic baseline data on key aspects of sensorimotor function need to be collected, preflight as well as in-flight and postflight as a function of time. Data related to other changes that would affect the interpretation of sensorimotor results need to be interrelated with them (e.g., sleep cycles, hormonal and immune changes, alterations in muscle physiology, use of drugs to combat motion sickness, and so on). Sample sizes are needed that are large enough so that the range and characterization of individual differences in performance can be identified and potential age relatedness determined. The efficacy of different countermeasures against space motion sickness and postflight reentry disturbances should be validated. Those not validated should be discontinued. Identical equipment and procedures should be used as much as possible for ground-based and flight data collection in a given experiment. Neurophysiological and related experiments conducted on the International Space Station are best carried out by physiologists serving as payload specialists. Relevant animal models should be developed for exploring the physiological and morphological bases for postflight reentry disturbances. References 1. Space Science Board, National Research Council. 1987. A Strategy for Space Biology and Medical Sciences for the 1980s and 1990s. National Academy Press, Washington, D.C. 2. Lackner, J.R., and DiZio, P. 1993. Multisensory, cognitive, and motor influences on human spatial orientation in weightlessness. J. Vest. Res. 3(3): 361-372. 3. Lackner, J.R., and DiZio, P. 1997. The role of reafference in recalibration of limb movement control and locomotion. J. Vest. Res. 7(2/3): 1-8. 4. Young, L.R., and Shelhamer, M. 1990. Microgravity enhances the relative contribution of visually-induced motion sensation. Aviat. Space Environ. Med. 61: 525-530. 5. Young, L.R., Oman, C.M., Merfled, D., Watt, D.G.D., Roy, S., Deluca, C., Balkwill, D., Christie, J., Groleau, N., Jackson, D.K., Law, G., Modestino, S., and Mayer, W. 1993. Spatial orinetation and posture during and following weightlessness: Human experiments on Spacelab-Life Sciences-1. J. Vestib. Res. 3: 231-240.

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--> 6. Young, L.R., and Shelhamer, M. 1990. Microgravity enhances the relative contribution of visually-induced motion sensation. Aviat. Space Environ. Med. 61: 525-530. 7. Graybiel, A., and Kellogg, R.S. 1967. The inversion illusion and its probable dependence on otolith function. Aerospace Med. 38: 1099-1103. 8. Lackner, J.R., and DiZio, P. 1993. Multisensory, cognitive andmotor influences on human spatial orientation in weightlessness . J. Vestib. Res. 3: 361-372. 9. Oman, C.M. 1988. The role of static visual orientation cues in the etiology of space motion sickness. Pp. 25-38 in Proceedings of the Symposium on Vestibular Organs and Altered Force Environment (M. Igarashi and K.G. Nute, eds). National Aeronautics and Space Administration, Space Biomedical Institute and Universities Space Research Association, Division of Space Biomedicine, Houston, Tex. 10. Mittelstaedt, H. 1989. The role of the pitched-up orientation of the otoliths in two recent models of the subjective vertical. Biol. Cybern. 61: 405-416. 11. Mittlestaedt, H., and Glasauer, S. 1993a. Illusions of verticality in weightlessness. Clin. Invest. 71: 732-739. 12. Mittlestaedt, H., and Glasauer, S. 1993b. Crucial effects of weightlessness on human orientation. J. Vestib. Res. 3: 307-314. 13. Lackner, J.R. 1992. Spatial orientation in weightless environments. Perception 21: 803-812. 14. Young, L.R., Oman, C.M., Watt, D.G.D., Money, K.E., Lichtenberg, B.K., Kenyon, R.V., and Arrott, A.P. 1986. M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 1. Sensory adaptation to weightlessness and readaptation to one-g: An overview. Exp. Brain Res. 64: 291-298. 15. Benson, A.J., Von Baumgarten, R., Berthoz, A., Brandt, T., Brand, U., Bruzek, W., Dichgans, J., Kass, J., Probst, T., Scherer, H., Viéville, T., Vogel, H., and Wetzig, J. 1986. Some results of the European vestibular experiments in the Spacelab-1 mission. Advisory Group for Aerosp. Res. Dev. (AGARD) Proc. 377: 1B3-1B14. 16. Arrott, A.P., and Young, L.R. 1986. M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 6. Vestibular reactions to lateral acceleration following ten days of weightlessness. Exp. Brain Res. 64: 347-357. 17. Arrott, A.P., Young, L.R., and Merfeld, D.P. 1990. Perceptionof linear acceleration in weightlessness . Aviat. Space Environ. Med. 61: 319-326. 18. Fisk, J., Lackner, J.R., and DiZio. P. 1993. Gravitoinertial force level influences arm movement control. J. Neurophysiol. 69(2): 504-511. 19. Young, L.R., Oman, C.M., Watt, D.G.D., Money, K.E., and Lichtenberg, B.K. 1984. Spatial orientation in weightlessness and readaptation to Earth's gravity. Science 225: 205-208. 20. Lackner, J.R., and DiZio, P. 1992. Gravitoinertial force level affects the appreciation of limb position during muscle vibration. Brain Res. 592: 175-180. 21. Lackner, J.R., DiZio, P., and Fisk, J.D. 1992. Tonic vibration reflexes and background force level. Acta Astronautica 26(2): 133-136. 22. Fisk, J., Lackner, J.R., and DiZio. P. 1993. Gravitoinertial force level influences arm movement control. J. Neurophysiol. 69(2): 504-511. 23. Schmitt, H.H., and Reid, D.J. 1985. Anecdotal information on space adaptation syndrome. National Aeronautics and Space Administration, Johnson Space Center, Houston, Tex. 24. Roll, J.P., Popov, K., Gurfinkel, V., Lipshits, M., André-Deshays, C., Gilhodes, J.C., and Quoniam, C. 1993. Sensorimotor and perceptual function of muscle proprioception in microgravity. J. Vestib. Res. 3: 259-274. 25. Ross, H.E., Brodie, E.E., and Benson, A.J. 1984. Mass discrimination during prolonged weightlessness. Science 225: 219-221. 26. Ross, H.E., Brodie, E.E., and Benson, A.J. 1986. Mass discrimination in weightlessness and readaptation to Earth's gravity. Exp. Brain Res. 64: 358-366. 27. Ross, H.E., Schwartz, E., and Emmerson, P. 1986. Mass discriminationin weightlessness improves with arm movements of higher acceleration . Naturwissenschaften 73: 453-454. 28. Clément, G., Gurfinkel, V.S., Lestienne, F., Lipshits, M.I., and Popov, K.E. 1984. Adaptation of posture control to weightlessness. Exp. Brain Res. 57: 61-72. 29. Clément, G., Gurfinkel, V.S., Lestienne, F., Lipshits, M.I., and Popov, K.E. 1985. Changes of posture during transient perturbations in microgravity. Aviat. Space Environ. Med. 56: 666-671. 30. Massion, J. 1992. Movement, posture and equilibrium: Interaction and coordination. Prog. Neurobiol. 38: 35-56. 31. Massion, J., Gurfinkel, V., Lipshits, M., Obadia, A., and Popov, K. 1993. Axial synergies under microgravity conditions. J. Vestib. Res. 3: 275-288.

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