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Sensorimotor aspects of high-speed artificial gravity: III. Sensorimotor adaptation

As a countermeasure to the debilitating physiological effects of weightlessness, astronauts could live continuously in an artificial gravity environment created by slow rotation of an entire spacecraft or be exposed to brief daily "doses" in a short radius centrifuge housed within a non-rotating spacecraft. A potential drawback to both approaches is that head movements made during rotation may be disorienting and nauseogenic. These side effects are more severe at higher rotation rates, especially upon first exposure. Head movements during rotation generate aberrant vestibular stimulation and Coriolis force perturbations of the head-neck motor system. This article reviews our progress toward distinguishing vestibular and motor factors in side effects of rotation, and presents new data concerning the rates of rotation up to which adaptation is possible. We have studied subjects pointing to targets during constant velocity rotation, because these movements generate Coriolis motor perturbations of the arm but do not involve unusual vestibular stimulation. Initially, reaching paths and endpoints are deviated in the direction of the transient lateral Coriolis forces generated. With practice, subjects soon move in straighter paths and land on target once more. If sight of the arm is permitted, adaptation is more rapid than in darkness. Initial arm movement trajectory and endpoint deviations are proportional to Coriolis force magnitude over a range of rotation speeds from 5 to 20 rpm, and there is rapid, complete motor adaptation at all speeds. These new results indicate that motor adaptation to high rotation rates is possible. Coriolis force perturbations of head movements also occur in a rotating environment but adaptation gradually develops over the course of many head movements.

Non-NASA Center

Sensorimotor aspects of high-speed artificial gravity: I. Sensory conflict in vestibular adaptation

Short-radius centrifugation offers a promising and affordable countermeasure to the adverse effects of prolonged weightlessness. However, head movements made in a fast rotating environment elicit Coriolis effects, which seriously compromise sensory and motor processes. We found that participants can adapt to these Coriolis effects when exposed intermittently to high rotation rates and, at the same time, can maintain their perceptual-motor coordination in stationary environments. In this paper, we explore the role of inter-sensory conflict in this adaptation process. Different measures (vertical nystagmus, illusory body tilt, motion sickness) react differently to visual-vestibular conflict and adapt differently. In particular, proprioceptive-vestibular conflict sufficed to adapt subjective parameters and the time constant of nystagmus decay, while retinal slip was required for VOR gain adaptation. A simple correlation between the strength of intersensory conflict and the efficacy of adaptation fails to explain the data. Implications of these findings, which differ from existing data for low rotation rates, are discussed.

Non-NASA Center

Sensorimotor integration in human postural control

It is generally accepted that human bipedal upright stance is achieved by feedback mechanisms that generate an appropriate corrective torque based on body-sway motion detected primarily by visual, vestibular, and proprioceptive sensory systems. Because orientation information from the various senses is not always available (eyes closed) or accurate (compliant support surface), the postural control system must somehow adjust to maintain stance in a wide variety of environmental conditions. This is the sensorimotor integration problem that we investigated by evoking anterior-posterior (AP) body sway using pseudorandom rotation of the visual surround and/or support surface (amplitudes 0.5-8 degrees ) in both normal subjects and subjects with severe bilateral vestibular loss (VL). AP rotation of body center-of-mass (COM) was measured in response to six conditions offering different combinations of available sensory information. Stimulus-response data were analyzed using spectral analysis to compute transfer functions and coherence functions over a frequency range from 0.017 to 2.23 Hz. Stimulus-response data were quite linear for any given condition and amplitude. However, overall behavior in normal subjects was nonlinear because gain decreased and phase functions sometimes changed with increasing stimulus amplitude. "Sensory channel reweighting" could account for this nonlinear behavior with subjects showing increasing reliance on vestibular cues as stimulus amplitudes increased. VL subjects could not perform this reweighting, and their stimulus-response behavior remained quite linear. Transfer function curve fits based on a simple feedback control model provided estimates of postural stiffness, damping, and feedback time delay. There were only small changes in these parameters with increasing visual stimulus amplitude. However, stiffness increased as much as 60% with increasing support surface amplitude. To maintain postural stability and avoid resonant behavior, an increase in stiffness should be accompanied by a corresponding increase in damping. Increased damping was achieved primarily by decreasing the apparent time delay of feedback control rather than by changing the damping coefficient (i.e., corrective torque related to body-sway velocity). In normal subjects, stiffness and damping were highly correlated with body mass and moment of inertia, with stiffness always about 1/3 larger than necessary to resist the destabilizing torque due to gravity. The stiffness parameter in some VL subjects was larger compared with normal subjects, suggesting that they may use increased stiffness to help compensate for their loss. Overall results show that the simple act of standing quietly depends on a remarkably complex sensorimotor control system.

NASA Discipline Neuroscience

Adaptation to Coriolis force perturbation of movement trajectory; role of proprioceptive and cutaneous somatosensory feedback

Subjects exposed to constant velocity rotation in a large fully-enclosed room that rotates initially make large reaching errors in pointing to targets. The paths and endpoints of their reaches are deviated in the direction of the transient lateral Coriolis forces generated by the forward velocity of their reaches. With additional reaches, subjects soon reach in straighter paths and become more accurate at landing on target even in the absence of visual feedback about their movements. Two factors contribute to this adaptation: first, muscle spindle and golgi tendon organ feedback interpreted in relation to efferent commands provide information about movement trajectory, and second, somatosensory stimulation of the fingertip at the completion of a reach provides information about the location of the fingertip relative to the torso.

Non-NASA Center

Development of sensory systems in zebrafish (Danio rerio)

Zebrafish possess all of the classic sensory modalities: taste, tactile, smell, balance, vision, and hearing. For each sensory system, this article provides a brief overview of the system in the adult zebrafish followed by a more detailed overview of the development of the system. By far the majority of studies performed in each of the sensory systems of the zebrafish have involved some aspect of molecular biology or genetics. Although molecular biology and genetics are not major foci of the paper, brief discussions of some of the mutant strains of zebrafish that have developmental defects in each specific sensory system are included. The development of the sensory systems is only a small sampling of the work being done using zebrafish and provides a mere glimpse of the potential of this model for the study of vertebrate development, physiology, and human disease.

Non-NASA Center

Invited review: gravitational biology of the neuromotor systems: a perspective to the next era

Earth's gravity has had a significant impact on the designs of the neuromotor systems that have evolved. Early indications are that gravity also plays a key role in the ontogenesis of some of these design features. The purpose of the present review is not to assess and interpret a body of knowledge in the usual sense of a review but to look ahead, given some of the general concepts that have evolved and observations made to date, which can guide our future approach to gravitational biology. We are now approaching an era in gravitational biology during which well-controlled experiments can be conducted for sustained periods in a microgravity environment. Thus it is now possible to study in greater detail the role of gravity in phylogenesis and ontogenesis. Experiments can range from those conducted on the simplest levels of organization of the components that comprise the neuromotor system to those conducted on the whole organism. Generally, the impact of Earth's gravitational environment on living systems becomes more complex as the level of integration of the biological phenomenon of interest increases. Studies of the effects of gravitational vectors on neuromotor systems have and should continue to provide unique insight into these mechanisms that control and maintain neural control systems designed to function in Earth's gravitational environment. A number of examples are given of how a gravitational biology perspective can lead to a clearer understanding of neuromotor disorders. Furthermore, the technologies developed for spaceflight studies have contributed and should continue to contribute to studies of motor dysfunctions, such as spinal cord injury and stroke. Disorders associated with energy support and delivery systems and how these functions are altered by sedentary life styles at 1 G and by space travel in a microgravity environment are also discussed.

Review, Tutorial

Time-dependent influence of sensorimotor set on automatic responses in perturbed stance

These experiments tested the hypothesis that the ability to change sensorimotor set quickly for automatic responses depends on the time interval between successive surface perturbations. Sensorimotor set refers to the influence of prior experience or context on the state of the sensorimotor system. Sensorimotor set for postural responses was influenced by first giving subjects a block of identical backward translations of the support surface, causing forward sway and automatic gastrocnemius responses. The ability to change set quickly was inferred by measuring the suppression of the stretched antagonist gastrocnemius responses to toes-up rotations causing backward sway, following the translations. Responses were examined under short (10-14 s) and long (19-24 s) inter-trial intervals in young healthy subjects. The results showed that subjects in the long-interval group changed set immediately by suppressing gastrocnemius to 51% of translation responses within the first rotation and continued to suppress them over succeeding rotations. In contrast, subjects in the short-interval group did not change set immediately, but required two or more rotations to suppress gastrocnemius responses. By the last rotation, the short-interval group suppressed gastrocnemius responses to 33%, similar to the long-interval group of 29%. Associated surface plantarflexor torque resulting from these responses showed similar results. When rotation and translation perturbations alternated, however, the short-interval group was not able to suppress gastrocnemius responses to rotations as much as the long-interval group, although they did suppress more than in the first rotation trial after a series of translations. Set for automatic responses appears to linger, from one trial to the next. Specifically, sensorimotor set is more difficult to change when surface perturbations are given in close succession, making it appear as if set has become progressively stronger. A strong set does not mean that responses become larger over consecutive trials. Rather, it is inferred by the extent of difficulty in changing a response when it is appropriate to do so. These results suggest that the ability to change sensorimotor set quickly is sensitive to whether the change is required after a long or a short series of a prior different response, which in turn depends on the time interval between successive trials. Different rate of gastrocnemius suppression to toes-up rotation of the support surface have been reported in previous studies. This may be partially explained by different inter-trial time intervals demonstrated in this study.

NASA Discipline Neuroscience

Effect of altered sensory conditions on multivariate descriptors of human postural sway

Multivariate descriptors of sway were used to test whether altered sensory conditions result not only in changes in amount of sway but also in postural coordination. Eigenvalues and directions of eigenvectors of the covariance of shnk and hip angles were used as a set of multivariate descriptors. These quantities were measured in 14 healthy adult subjects performing the Sensory Organization test, which disrupts visual and somatosensory information used for spatial orientation. Multivariate analysis of variance and discriminant analysis showed that resulting sway changes were at least bivariate in character, with visual and somatosensory conditions producing distinct changes in postural coordination. The most significant changes were found when somatosensory information was disrupted by sway-referencing of the support surface (P = 3.2 x 10(-10)). The resulting covariance measurements showed that subjects not only swayed more but also used increased hip motion analogous to the hip strategy. Disruption of vision, by either closing the eyes or sway-referencing the visual surround, also resulted in altered sway (P = 1.7 x 10(-10)), with proportionately more motion of the center of mass than with platform sway-referencing. As shown by discriminant analysis, an optimal univariate measure could explain at most 90% of the behavior due to altered sensory conditions. The remaining 10%, while smaller, are highly significant changes in posture control that depend on sensory conditions. The results imply that normal postural coordination of the trunk and legs requires both somatosensory and visual information and that each sensory modality makes a unique contribution to posture control. Descending postural commands are multivariate in nature, and the motion at each joint is affected uniquely by input from multiple sensors.

NASA Discipline Neuroscience

Mechanism of thirst attenuation during head-out water immersion in men

The purpose was to determine whether extracellular volume or osmolality was the major contributing factor for reduction of thirst in air and head-out water immersion in hypohydrated subjects. Eight males (19-25 yr) were subjected to thermoneutral immersion and thermoneutral air under two hydration conditions without further drinking: euhydration in water (Eu-H2O) and euhydration in air, and hypohydration in water (Hypo-H2O) and hypohydration in air (3.7% wt loss after exercise in heat). The increased thirst sensation with Hypo-H2O decreased (P < 0.05) within 10 min of immersion and continued thereafter. Mean plasma osmolality (288 +/- 1 mosmol/kgH2O) and sodium (140 +/- 1 meq/l) remained elevated, and plasma volume increased by 4.2 +/- 1.0% (P < 0.05) throughout Hypo-H2O. A sustained increase (P < 0.05) in stroke volume accompanied the prompt and sustained decrease in plasma renin activity and sustained increase (P < 0.05) in plasma atrial natriuretic peptide during Eu-H2O and Hypo-H2O. Plasma vasopressin decreased from 5.3 +/- 0.7 to 2.9 +/- 0.5 pg/ml (P < 0.05) during Hypo-H2O but was unchanged in Eu-H2O. These findings suggest a sustained stimulation of the atrial baroreceptors and reduction of a dipsogenic stimulus without major alterations of extracellular osmolality in Hypo-H2O. Thus it appears that vascular volume-induced stimuli of cardiopulmonary baroreceptors play a more important role than extracellular osmolality in reducing thirst sensations during immersion in hypohydrated subjects.

NASA Center ARC

Horizontal angular VOR, nystagmus dumping, and sensation duration in spacelab SLS-1 crewmembers

In 1G, the apparent time constant (Td) of postrotatory SPV decay with the head tilted face down is 55% of that with head erect (Te). This phenomenon is called "nystagmus dumping" and has been attributed to G effects on VOR velocity storage. Similarly, postrotatory sensation duration with head tilted (Dd) is 32% of that when head erect (De). In parabolic flight, Te and De are 70% of 1-G values, but a pitch back dumping movement produces no further change. Te, Td, and Dd have not previously been measured in orbital flight. VOR and sensation duration was tested in 4 crewmembers in 4 preflight, 1 inflight (days 4 or 5) and 4 post flight sessions. Bitemporal EOG was recorded with eyes open in darkness. Instructions were to "gaze straight ahead," and indicate when "rotation sensation disappears or becomes ambiguous". Subjects were rotated CW and CCW head erect for 1 min at 120 degrees/s, stopped, and EOG was recorded for another 1 min. This procedure was then used to study dumping, except that immediately after chair stop, subjects pitched their head forward 90 degrees. SPV was calculated using order statistic filtering, and dropouts removed using an iterative model fitting method. Te and Td were determined by logarithmic linear regression of mean SPV for each subject. In orbit, 90 degrees pitch movement produced rapid subjective dumping, but not nystagmus dumping. Dd was noticeably shorter ("almost instantaneous") compared to preflight Dd. Te and Td in orbit were similar to preflight Te for 3/4 subjects (rather than to preflight Td as expected). No consistent VOR gain changes were seen in orbit. Although Te is known to decrease acutely in parabolic flight, a longer time constant was measured in 3/4 subjects after 4-5 days adaptation to weightlessness, suggesting a return of angular velocity storage.

NASA Experiment Number 178072 1/2

Geometrical approach to neural net control of movements and posture

In one approach to modeling brain function, sensorimotor integration is described as geometrical mapping among coordinates of non-orthogonal frames that are intrinsic to the system; in such a case sensors represent (covariant) afferents and motor effectors represent (contravariant) motor efferents. The neuronal networks that perform such a function are viewed as general tensor transformations among different expressions and metric tensors determining the geometry of neural functional spaces. Although the non-orthogonality of a coordinate system does not impose a specific geometry on the space, this "Tensor Network Theory of brain function" allows for the possibility that the geometry is non-Euclidean. It is suggested that investigation of the non-Euclidean nature of the geometry is the key to understanding brain function and to interpreting neuronal network function. This paper outlines three contemporary applications of such a theoretical modeling approach. The first is the analysis and interpretation of multi-electrode recordings. The internal geometries of neural networks controlling external behavior of the skeletomuscle system is experimentally determinable using such multi-unit recordings. The second application of this geometrical approach to brain theory is modeling the control of posture and movement. A preliminary simulation study has been conducted with the aim of understanding the control of balance in a standing human. The model appears to unify postural control strategies that have previously been considered to be independent of each other. Third, this paper emphasizes the importance of the geometrical approach for the design and fabrication of neurocomputers that could be used in functional neuromuscular stimulation (FNS) for replacing lost motor control.

Review

Sensorimotor recovery following spaceflight may be due to frequent square-wave saccadic intrusions

Square-wave jerks (SWJs) are small, involuntary saccades that disrupt steady fixation. We report the case of an astronaut (approximately 140 d on orbit) who showed frequent SWJs, especially postflight, but who showed no impairment of vision or decrement of postflight performance. These data support the view that SWJs do not impair vision because they are paired movements, consisting of a small saccade away from the fixation position followed, within 200 ms, by a corrective saccade that brings the eye back on target. Since many returning astronauts show a decrement of dynamic visual function during postflight locomotion, it seems possible that frequent SWJs improved this astronaut's visual function by providing postsaccadic enhancement of visual fixation, which aided postflight performance. Certainly, frequent SWJs did not impair performance in this astronaut, who had no other neurological disorder.

Case Reports