Influence of multisensory graviceptive information on the apparent zenith.

We studied the contribution of vestibular and somatosensory/proprioceptive stimulation to the perception of the apparent zenith (AZ). Experiment 1 involved rotation on a centrifuge and settings of the AZ. Subjects were supine on the centrifuge, and their body position was varied in relation to the rotation axis so that the gravitoinertial resultant force at the otoliths was 1 or 1.2 g with the otolith organs positioned 50 or 100 cm from the axis of rotation. Their legs were also positioned in different configurations, flexed and elevated or extended, to create different distributions of blood and lymph. Experiment 2 involved (a) settings of the AZ for subjects positioned supine with legs fully extended or legs flexed and elevated to create a torsoward shift of blood and (b) settings of the subjective visual vertical for subjects horizontally positioned on their sides with legs extended or bent. Experiment 3 had subjects in the same body configurations as in Experiment 2 indicate when they were horizontal as they were rotated in pitch or roll about an inter-aural or naso-occipital axis. The experimental results for all three experiments demonstrated that both visual localization and apparent body horizontal are jointly determined by multimodal combinations of otolithic and somatosensory/proprioceptive stimulation. No evidence was found for non-overlapping or exclusive mechanisms determining one or the other. The subjective postural horizontal and AZ were affected in similar ways by comparable manipulations.

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.

Parabolic flight: loss of sense of orientation.

On the earth, or in level flight, a blindfolded subject being rotated at constant velocity about his recumbent long body axis experiences illusory orbital motion of his body in the opposite direction. By contrast, during comparable rotation in the free-fall phase of parabolic flight, no body motion is perceived and all sense of external orientation may be lost; when touch and pressure stimulation is applied to the body surface, a sense of orientation is reestablished immediately. The increased gravitoinertial force period of a parabola produces an exaggeration of the orbital motion experienced in level flight. These observations reveal an important influence of touch, pressure, and kinesthetic information on spatial orientation and provide a basis for understanding many of the postural illusions reported by astronauts in space flight.

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.

Alterations in speech shadowing ability after cerebral injury in man.

Patients with penetrating wounds of the left cerebral hemisphere are inferior to normal control subjects and patients with right hemisphere lesions in their ability to shadow language stimuli presented at various rates. Their performance deteriorates rapidly at higher rates of stimulus presentation. Patients with bilateral cerebral penetration show similar patterns of deficits. The deficits on the shadowing task are especially prominent in patients who were dysphasic or dysarthric during the immediate postinjury period.

Use of promethazine to hasten adaptation to provocative motion.

In an earlier study, the authors found that severely motion sick individuals could be greatly relieved of their symptoms by intramuscular injections of promethazine (50 mg) or scopolamine (.5 mg). Comparable 50-mg injections of promethazine also have been found effective in alleviating symptoms of space motion sickness. The concern has risen, however, that such drugs may delay or retard the acquisition of adaptation to stressful environments. In the current study, we controlled arousal using a mental arithmetic task and precisely equated the exposure history (number of head movements during rotation) of a placebo, control group and an experimental group who had received promethazine. No differences in total adaptation or in rates of adaptation were present between the two groups. Another experimental group also received promethazine and was allowed to make as many head movements as they could, before reaching nausea, up to 800. This group showed a greater level of adaptation than the placebo group. These results suggest a strategy for dealing with space motion sickness that is described.

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.

Smooth pursuit eye movements elicited by somatosensory stimulation.

Smooth pursuit eye movements approaching the qualitative and quantitative characteristics of those elicited by a moving visual target were obtained in complete darkness with a moving tactile stimulus. Pursuit eye movements in response to tactile stimulation have longer latencies to onset and to offset of pursuit, are more often interrupted by saccades, and provide less accurate stimulus localization than those in response to moving visual stimuli. The evocation of pursuit eye movements by a somatosensory input suggests that within the appropriate velocity domain a spatially changing sensory input from any modality may be sufficient to elicit ocular pursuit.

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.

Influence of voluntary ocular deviation on vestibular nystagmus.

We examined the influence of voluntary gaze deviation on per-rotary vestibular nystagmus during trapezoidal velocity profiles. Gaze deviation in the direction of the fast-phase component of nystagmus significantly increased slow-phase amplitude, fast-phase amplitude and slow-phase velocity; gaze deviation in the direction of the slow phase marginally decreased these three properties. Schlagfeld deviation and beat frequency were unaffected by per-rotary ocular deviation in either direction. The observed changes in per-rotary eye movements are consistent with post-rotary observations first described by Alexander which later became known as "Alexander's Law".

Multimodal and motor influences on orientation: implications for adapting to weightless and virtual environments.

Human sensory-motor control and orientation involve the correlation of sensory information from many modalities with motor information about ongoing patterns of voluntary and reflexive activation of the body musculature. The vestibular system represents only one of the acceleration-sensitive receptor systems of the body conveying spatial information. Touch- and pressure-dependent receptors, somatosensory and interoceptive, as well as proprioceptive receptors contribute, along with visual and auditory signals specifying relative motion between self and surround. Control of body movement and orientation is dynamically adapted to the 1G force background of Earth. Exposure to non-1G environments such as in space travel produces a variety of sensory-motor disturbances, and often motion sickness, until adaptation is achieved. Exposure to virtual environments in which body movements are not accompanied by normal patterns of inertial and sensory feedback can also lead to control errors and elicit motion sickness.

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.

Stabilization of posture by precision contact of the index finger.

Postural sway during quiet stance increases if sight of the surroundings is denied. We studied how sensory-motor information about body displacement provided by contact of the index finger with a stationary bar can be used to stabilize balance in the absence of vision. Stabilization equivalent to the contribution conferred by vision was achieved at contact force levels less than 1 N. This value is much below that necessary to provide significant physical stabilization of the body. We interpret our findings in relation to tactile thresholds for motion detection, "precision grip," and proprioceptive and sensory-motor information about the configuration of the arm to the torso. In conditions allowing higher force levels at the fingertip (5-8 N), subjects assumed a passively stable state to stabilize their stance.

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.

Induction of illusory self-rotation and nystagmus by a rotating sound-field.

Subjects seated in darkness often experience illusory self-rotation when exposed to a rotating sound field. Compelling illusions of self-rotation are generally accompanied by nystagmoid movements of the eyes with the slow phase in the direction opposite that of the experienced self-rotation. These phenomena are related to the functioning of a spatial constancy mechanism by which a stable distinction is normally maintained between movements of self and movements of the environment. The appearance of nystagmus during illusory self-rotation indicates that apparent body orientation can influence oculomotor control.

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.