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Merfeld, D. M.

Publications and source records attributed to Merfeld, D. M..

Exhibition of Stochastic Resonance in Vestibular Perception

Astronauts experience sensorimotor changes during spaceflight, particularly during G-transitions. Post flight sensorimotor changes include spatial disorientation, along with postural and gait instability that may degrade operational capabilities of the astronauts and endanger the crew. A sensorimotor countermeasure that mitigates these effects would improve crewmember safety and decrease risk. The goal of this research is to investigate the potential use of stochastic vestibular stimulation (SVS) as a technology to improve sensorimotor function. We hypothesize that low levels of SVS will improve sensorimotor perception through the phenomenon of stochastic resonance (SR), when the response of a nonlinear system to a weak input signal is enhanced by the application of a particular nonzero level of noise. This study aims to advance the development of SVS as a potential countermeasure by 1) demonstrating the exhibition of stochastic resonance in vestibular perception, a vital component of sensorimotor function, 2) investigating the repeatability of SR exhibition, and 3) determining the relative contribution of the semicircular canals (SCC) and otolith (OTO) organs to vestibular perceptual SR. A constant current stimulator was used to deliver bilateral bipolar SVS via electrodes placed on each of the mastoid processes, as previously done. Vestibular perceptual motion recognition thresholds were measured using a 6-degree of freedom MOOG platform and a 150 trial 3-down/1-up staircase procedure. In the first test session, we measured vestibular perceptual thresholds in upright roll-tilt at 0.2 Hz (SCC+OTO) with SVS ranging from 0-700 μA. In a second test session a week later, we re-measured roll-tilt thresholds with 0, optimal (from test session 1), and 1500 μA SVS levels. A subset of these subjects, plus naive subjects, participated in two additional test sessions in which we measured thresholds in supine roll-rotation at 0.2 Hz (SCC) and upright y-translation at 1 Hz (OTO) with SVS up to 700 μA. A sinusoidal galvanic vestibular stimulation (GVS) perceptual threshold was also measured on each test day and used to normalize the SVS levels across subjects. In roll-tilt thresholds with SVS, the characteristic SR curve was qualitatively exhibited in 10 of 12 subjects, and the improvement in motion threshold was significant in 6 subjects, indicating that optimal SVS improved passive body motion perception in a way that is consistent with classical SR theory. A probabilistic comparison to numeric simulations further validated these experimental results. On the second test session, 4 out of the 10 SR exhibitors showed repeated improvement with SVS compared to the no SVS condition. Data collection is ongoing for the last two test sessions in which SCC and OTO only perceptual motion recognition thresholds are being measured with SVS. The final results of these test sessions will give insight into whether vestibular perceptual SR can occur when only one type of vestibular sensor is sensing motion or if it is more evident when sensory integration between the SCC and OTO is occurring during the motion. The overall purpose of this research is to further quantify the effects of SVS on various sensorimotor tasks and to gain a more fundamental understanding of how SVS causes SR in the vestibular system. In the context of human space flight, results from this research will help in understanding how SVS may be practically implemented in the future as a component of a comprehensive countermeasure plan for G-transition adaptation.

Galvan-Garza, R. C.

Improving Sensorimotor Function and Adaptation using Stochastic Vestibular Stimulation

Astronauts experience sensorimotor changes during adaption to G-transitions that occur when entering and exiting microgravity. Post space flight, these sensorimotor disturbances can include postural and gait instability, visual performance changes, manual control disruptions, spatial disorientation, and motion sickness, all of which can hinder the operational capabilities of the astronauts. Crewmember safety would be significantly increased if sensorimotor changes brought on by gravitational changes could be mitigated and adaptation could be facilitated. The goal of this research is to investigate and develop the use of electrical stochastic vestibular stimulation (SVS) as a countermeasure to augment sensorimotor function and facilitate adaptation. For this project, SVS will be applied via electrodes on the mastoid processes at imperceptible amplitude levels. We hypothesize that SVS will improve sensorimotor performance through the phenomena of stochastic resonance, which occurs when the response of a nonlinear system to a weak input signal is optimized by the application of a particular nonzero level of noise. In line with the theory of stochastic resonance, a specific optimal level of SVS will be found and tested for each subject [1]. Three experiments are planned to investigate the use of SVS in sensory-dependent tasks and performance. The first experiment will aim to demonstrate stochastic resonance in the vestibular system through perception based motion recognition thresholds obtained using a 6-degree of freedom Stewart platform in the Jenks Vestibular Laboratory at Massachusetts Eye and Ear Infirmary. A range of SVS amplitudes will be applied to each subject and the subjectspecific optimal SVS level will be identified as that which results in the lowest motion recognition threshold, through previously established, well developed methods [2,3,4]. The second experiment will investigate the use of optimal SVS in facilitating sensorimotor adaptation to system disturbances. Subjects will adapt to wearing minifying glasses, resulting in decreased vestibular ocular reflex (VOR) gain. The VOR gain will then be intermittently measured while the subject readapts to normal vision, with and without optimal SVS. We expect that optimal SVS will cause a steepening of the adaptation curve. The third experiment will test the use of optimal SVS in an operationally relevant aerospace task, using the tilt translation sled at NASA Johnson Space Center, a test platform capable of recreating the tilt-gain and tilt-translation illusions associated with landing of a spacecraft post-space flight. In this experiment, a perception based manual control measure will be used to compare performance with and without optimal SVS. We expect performance to improve in this task when optimal SVS is applied. The ultimate goal of this work is to systematically investigate and further understand the potential benefits of stochastic vestibular stimulation in the context of human space flight so that it may be used in the future as a component of a comprehensive countermeasure plan for adaptation to G-transitions.

Galvan, R. C.

Improving Sensorimotor Function Using Stochastic Vestibular Stimulation

Astronauts experience sensorimotor changes during spaceflight, particularly during G-transition phases. Post flight sensorimotor changes may include postural and gait instability, spatial disorientation, and visual performance decrements, all of which can degrade operational capabilities of the astronauts and endanger the crew. Crewmember safety would be improved if these detrimental effects of spaceflight could be mitigated by a sensorimotor countermeasure and even further if adaptation to baseline could be facilitated. The goal of this research is to investigate the potential use of stochastic vestibular stimulation (SVS) as a technology to improve sensorimotor function. We hypothesize that low levels of SVS will improve sensorimotor performance through stochastic resonance (SR). The SR phenomenon occurs when the response of a nonlinear system to a weak input signal is optimized by the application of a particular nonzero level of noise. Two studies have been initiated to investigate the beneficial effects and potential practical usage of SVS. In both studies, electrical vestibular stimulation is applied via electrodes on the mastoid processes using a constant current stimulator. The first study aims to determine the repeatability of the effect of vestibular stimulation on sensorimotor performance and perception in order to better understand the practical use of SVS. The beneficial effect of low levels of SVS on balance performance has been shown in the past. This research uses the same balance task repeated multiple times within a day and across days to study the repeatability of the stimulation effects. The balance test consists of 50 sec trials in which the subject stands with his or her feet together, arms crossed, and eyes closed on compliant foam. Varying levels of SVS, ranging from 0-700 micro A, are applied across different trials. The subject-specific optimal SVS level is that which results in the best balance performance as measured by inertial measurement units placed on the upper and lower torso of the subjects. Additionally, each individual’s threshold for illusory motion perception of suprasensory electrical vestibular stimulation is measured multiple times within and across days to better understand how multiple SVS test methods compare. The second study aims to demonstrate stochastic resonance in the vestibular system using a perception based motion recognition task. This task measures an individual’s velocity threshold of motion recognition using a 6-degree of freedom Stewart platform and a 3-down/1-up staircase procedure. For this study, thresholds are determined using 150 trials in the upright, head-centered roll tilt motion direction at a 0.2 Hz frequency. We aim to demonstrate the characteristic bell shaped curve associated with stochastic resonance with each subject’s motion recognition thresholds at varying SVS levels ranging from 0 to 1500 micro A. The curve includes the individual’s baseline threshold with no SVS, optimal or minimal threshold at some mid-level of SVS, and finally degraded or increased threshold at a high SVS level. An additional aim is to formally retest each subject at his or her individual optimal SVS level on a different day than the original testing for additional validity. The overall purpose of this research is to further quantify the effects of SVS on various sensorimotor tasks and investigate the practical implications of its use in the context of human space flight so that it may be implemented in the future as a component of a comprehensive countermeasure plan for adaptation to G-transitions.

Galvan, R. C.

Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt

Sensory systems often provide ambiguous information. Integration of various sensory cues is required for the CNS to resolve sensory ambiguity and elicit appropriate responses. The vestibular system includes two types of sensors: the semicircular canals, which measure head rotation, and the otolith organs, which measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. According to Einstein's equivalence principle, gravitational force is indistinguishable from inertial force due to linear acceleration. As a consequence, otolith measurements must be supplemented with other sensory information for the CNS to distinguish tilt from translation. The GIF resolution hypothesis states that the CNS estimates gravity and linear acceleration, so that the difference between estimates of gravity and linear acceleration matches the measured GIF. Both otolith and semicircular canal cues influence this estimation of gravity and linear acceleration. The GIF resolution hypothesis predicts that inaccurate estimates of both gravity and linear acceleration can occur due to central interactions of sensory cues. The existence of specific patterns of vestibuloocular reflexes (VOR) related to these inaccurate estimates can be used to test the GIF resolution hypothesis. To investigate this hypothesis, we measured eye movements during two different protocols. In one experiment, eight subjects were rotated at a constant velocity about an earth-vertical axis and then tilted 90 degrees in darkness to one of eight different evenly spaced final orientations, a so-called "dumping" protocol. Three speeds (200, 100, and 50 degrees /s) and two directions, clockwise (CW) and counterclockwise (CCW), of rotation were tested. In another experiment, four subjects were rotated at a constant velocity (200 degrees /s, CW and CCW) about an earth-horizontal axis and stopped in two different final orientations (nose-up and nose-down), a so-called "barbecue" protocol. The GIF resolution hypothesis predicts that post-rotatory horizontal VOR eye movements for both protocols should include an "induced" VOR component, compensatory to an interaural estimate of linear acceleration, even though no true interaural linear acceleration is present. The GIF resolution hypothesis accurately predicted VOR and induced VOR dependence on rotation direction, rotation speed, and head orientation. Alternative hypotheses stating that frequency segregation may discriminate tilt from translation or that the post-rotatory VOR time constant is dependent on head orientation with respect to the GIF direction did not predict the observed VOR for either experimental protocol.

Non-NASA Center

Low-frequency otolith and semicircular canal interactions after canal inactivation

During sustained constant velocity and low-frequency off-vertical axis rotations (OVAR), otolith signals contribute significantly to slow-phase eye velocity. The adaptive plasticity of these responses was investigated here after semicircular canal plugging. Inactivation of semicircular canals results in a highly compromised and deficient vestibulo-ocular reflex (VOR). Based on the VOR enhancement hypothesis, one could expect an adaptive increase of otolith-borne angular velocity signals due to combined otolith/canal inputs after inactivation of the semicircular canals. Contrary to expectations, however, the steady-state slow-phase velocity during constant velocity OVAR decreased in amplitude over time. A similar progressive decrease in VOR gain was also observed during low-frequency off-vertical axis oscillations. This response deterioration was present in animals with either lateral or vertical semicircular canals inactivated and was limited to the plane(s) of the plugged canals. The results are consistent with the idea that the low-frequency otolith signals do not simply enhance VOR responses. Rather, the nervous system appears to correlate vestibular sensory information from the otoliths and the semicircular canals to generate an integral response to head motion.

Non-NASA Center

Effects of static orientation upon human optokinetic afternystagmus

"Normal" human subjects were placed in a series of 5 static orientations with respect to gravity and were asked to view an optokinetic display moving at a constant angular velocity. The axis of rotation coincided with the subject's rostro-caudal axis and produced horizontal optokinetic nystagmus and afternystagmus. Wall (1) previously reported that these optokinetic afternystagmus responses were not well characterized by parametric fits to slow component velocity. The response for nose-up, however, was larger than for nose-down. This suggested that the horizontal eye movements measured during optokinetic stimulation might include an induced linear VOR component as presented in the body of this paper. To investigate this hypothesis, another analysis of these data has been made using cumulative slow component eye position. Some subjects' responses had reversals in afternystagmus direction. These reversals were "filled in" by a zero slow component velocity. This method of analysis gives a much more consistent result across subjects and shows that, on average, responses from the nose-down horizontal (prone) orientation are greatly reduced (p < 0.05) compared to other horizontal and vertical orientations. Average responses are compared to responses predicted by a model previously used to predict successfully the responses to post-rotatory nystagmus after earth horizontal axis rotation. Ten of 11 subjects had larger responses in their supine than their prone orientation. Application of horizontal axis optokinetic afternystagmus for clinical otolith function testing, and implications for altered gravity experiments are discussed.

Non-NASA Center

Clinical use of three-dimensional video measurements of eye movements

Noninvasive measurements of three-dimensional eye position can be accurately achieved with video methods. A case study showing the potential clinical benefit of these enhanced measurements is presented along with some thoughts about technological advances, essential for clinical application, that are likely to occur in the next several years.

Non-NASA Center

The dynamic contributions of the otolith organs to human ocular torsion

We measured human ocular torsion (OT) monocularly (using video) and binocularly (using search coils) while sinusoidally accelerating (0.7 g) five human subjects along an earth-horizontal axis at five frequencies (0.35, 0.4, 0.5, 0.75, and 1.0 Hz). The compensatory nature of OT was investigated by changing the relative orientation of the dynamic (linear acceleration) and static (gravitational) cues. Four subject orientations were investigated: (1) Y-upright-acceleration along the interaural (y) axis while upright; (2) Y-supine-acceleration along the y-axis while supine; (3) Z-RED-acceleration along the dorsoventral (z) axis with right ear down; (4) Z-supine-acceleration along the z-axis while supine. Linear acceleration in the Y-upright, Y-supine and Z-RED orientations elicited conjugate OT. The smaller response in the Z-supine orientation appeared disconjugate. The amplitude of the response decreased and the phase lag increased with increasing frequency for each orientation. This frequency dependence does not match the frequency response of the regular or irregular afferent otolith neurons; therefore the response dynamics cannot be explained by simple peripheral mechanisms. The Y-upright responses were larger than the Y-supine responses (P < 0.05). This difference indicates that OT must be more complicated than a simple low-pass filtered response to interaural shear force, since the dynamic shear force along the interaural axis was identical in these two orientations. The Y-supine responses were, in turn, larger than the Z-RED responses (P < 0.01). Interestingly, the vector sum of the Y-supine responses plus Z-RED responses was not significantly different (P = 0.99) from the Y-upright responses. This suggests that, in this frequency range, the conjugate OT response during Y-upright stimulation might be composed of two components: (1) a response to shear force along the y-axis (as in Y-supine stimulation), and (2) a response to roll tilt of gravitoinertial force (as in Z-RED stimulation).

NASA Discipline Neuroscience

Vestibulo-ocular reflex of the squirrel monkey during eccentric rotation with centripetal acceleration along the naso-occipital axis

The vestibulo-ocular reflexes (VOR) are determined not only by angular acceleration, but also by the presence of gravity and linear acceleration. This phenomenon was studied by measuring three-dimensional nystagmic eye movements, with implanted search coils, in four male squirrel monkeys. Monkeys were rotated in the dark at 200 degrees/s, centrally or 79 cm off-axis, with the axis of rotation always aligned with gravity and the spinal axis of the upright monkeys. The monkey's position relative to the centripetal acceleration (facing center or back to center) had a dramatic influence on the VOR. These studies show that a torsional response was always elicited that acted to shift the axis of eye rotation toward alignment with gravito-inertial force. On the other hand, a slow phase downward vertical response usually existed, which shifted the axis of eye rotation away from the gravito-inertial force. These findings were consistent across all monkeys. In another set of tests, the same monkeys were rapidly tilted about their interaural (pitch) axis. Tilt orientations of 45 degrees and 90 degrees were maintained for 1 min. Other than a compensatory angular VOR during the rotation, no consistent eye velocity response was ever observed during or following the tilt. The absence of any response following tilt proves that the observed torsional and vertical responses were not a positional nystagmus. Model simulations qualitatively predict all components of these eccentric rotation and tilt responses. These simulations support the conclusion that the VOR during eccentric rotation may consist of two components: a linear VOR and a rotational VOR. The model predicts a slow phase downward, vertical, linear VOR during eccentric rotation even though there was never a change in the force aligned with monkey's spinal (Z) axis. The model also predicts the torsional components of the response that shift the rotation axis of the angular VOR toward alignment with gravito-inertial force.

NASA Center JSC

Modeling human vestibular responses during eccentric rotation and off vertical axis rotation

A mathematical model has been developed to help explain human multi-sensory interactions. The most important constituent of the model is the hypothesis that the nervous system incorporates knowledge of sensory dynamics into an "internal model" of these dynamics. This internal model allows the nervous system to integrate the sensory information from many different sensors into a coherent estimate of self-motion. The essence of the model is unchanged from a previously published model of monkey eye movement responses; only a few variables have been adjusted to yield the prediction of human responses. During eccentric rotation, the model predicts that the axis of eye rotation shifts slightly toward alignment with gravito-inertial force. The model also predicts that the time course of the perception of tilt following the acceleration phase of eccentric rotation is much slower than that during deceleration. During off vertical axis rotation (OVAR) the model predicts a small horizontal bias along with small horizontal, vertical, and torsional oscillations. Following OVAR stimulation, when stopped right- or left-side down, a small vertical component is predicted that decays with the horizontal post-rotatory response. All of the predictions are consistent with measurements of human responses.

NASA Discipline Neuroscience

Effect of vergence on the gain of the linear vestibulo-ocular reflex

We measured the linear vestibulo-ocular reflex (LVOR) and vergence, using binocular search coils, in 3 humans. The subjects were accelerated sinusoidally at 0.5 Hz and 0.2 g peak acceleration, in complete darkness, while performing three different tasks: i) mental arithmetic; ii) tracking a remembered target at either 0.34 m or 0.14 m distance; and iii) maintaining vergence at either of these distances by means of audio biofeedback based on vergence. Subjects could control vergence using the audio feedback; there was greater convergence with the near audio target. However, there was no significant difference in vergence between the near and far remembered target conditions. With audio feedback, the amplitude of smooth tracking was not consistently different for the near and the far conditions. However, the amplitude of tracking (saccades and smooth component) in the remembered target conditions was greater for near than for far targets. These results suggest that linear VOR amplitude is not determined by vergence alone.

NASA Program Space Physiology and Countermeasures

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

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

NASA Discipline Neuroscience

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

The vestibulo-ocular reflexes (VOR) are determined not only by angular acceleration, but also by the presence of gravity and linear acceleration. This phenomenon was studied by measuring three-dimensional nystagmic eye movements, with implanted search coils, in six male squirrel monkeys during eccentric rotation. Monkeys were rotated in the dark at a constant velocity of 200 degrees/s (centrally or 79 cm off axis) with the axis of rotation always aligned with gravity and the spinal axis of the upright monkeys. The monkey's orientation (facing-motion or back-to-motion) had a dramatic influence on the VOR. These experiments show that: (a) the axis of eye rotation always shifted toward alignment with gravito-inertial force; (b) the peak value of horizontal slow phase eye velocity was greater with the monkey facing-motion than with back-to-motion; and (c) the time constant of horizontal eye movement decay was smaller with the monkey facing-motion than with back-to-motion. All of these findings were statistically significant and consistent across monkeys. In another set of tests, the same monkeys were rapidly tilted about their naso-occipital (roll) axis. Tilted orientations of 45 degrees and 90 degrees were maintained for 1 min. Other than a compensatory angular VOR during the angular rotation, no consistent eye velocity response was observed during or following the tilt for any of the six monkeys. The absence of any eye movement response following tilt weighs against the possibility that translational linear VOR responses are due to simple high-pass filtering of the otolith signals. The VOR response during eccentric rotation was divided into the more familiar angular VOR and linear VOR components. The angular component is known to depend upon semicircular canal dynamics and central influences. The linear component of the response decays rapidly with a mean duration of only 6.6 s, while the axis of eye rotation rapidly aligns (< 10 s) with gravito-inertial force. These results are consistent with the hypothesis that the measurement of gravito-inertial force by the otolith organs is resolved into central estimates of linear acceleration and gravity, such that the central estimate of gravitational force minus the central estimate of linear acceleration approximately equals the otolith measurement of gravito-inertial force.

NASA Discipline Neuroscience

A multidimensional model of the effect of gravity on the spatial orientation of the monkey

A "sensory conflict" model of spatial orientation was developed. This mathematical model was based on concepts derived from observer theory, optimal observer theory, and the mathematical properties of coordinate rotations. The primary hypothesis is that the central nervous system of the squirrel monkey incorporates information about body dynamics and sensory dynamics to develop an internal model. The output of this central model (expected sensory afference) is compared to the actual sensory afference, with the difference defined as "sensory conflict." The sensory conflict information is, in turn, used to drive central estimates of angular velocity ("velocity storage"), gravity ("gravity storage"), and linear acceleration ("acceleration storage") toward more accurate values. The model successfully predicts "velocity storage" during rotation about an earth-vertical axis. The model also successfully predicts that the time constant of the horizontal vestibulo-ocular reflex is reduced and that the axis of eye rotation shifts toward alignment with gravity following postrotatory tilt. Finally, the model predicts the bias, modulation, and decay components that have been observed during off-vertical axis rotations (OVAR).

NASA Discipline Neuroscience

Three dimensional eye movements of squirrel monkeys following postrotatory tilt

Three-dimensional squirrel monkey eye movements were recorded during and immediately following rotation around an earth-vertical yaw axis (160 degrees/s steady state, 100 degrees/s2 acceleration and deceleration). To study interactions between the horizontal angular vestibulo-ocular reflex (VOR) and head orientation, postrotatory VOR alignment was changed relative to gravity by tilting the head out of the horizontal plane (pitch or roll tilt between 15 degrees and 90 degrees) immediately after cessation of motion. Results showed that in addition to post rotatory horizontal nystagmus, vertical nystagmus followed tilts to the left or right (roll), and torsional nystagmus followed forward or backward (pitch) tilts. When the time course and spatial orientation of eye velocity were considered in three dimensions, the axis of eye rotation always shifted toward alignment with gravity, and the postrotatory horizontal VOR decay was accelerated by the tilts. These phenomena may reflect a neural process that resolves the sensory conflict induced by this postrotatory tilt paradigm.

NASA Program Space Physiology and Countermeasures

Perception of linear acceleration in weightlessness

Tests of the perception and use of linear acceleration sensory information were performed on the science crews of the Spacelab 1 (SL-1) and D-1 missions using linear "sleds" in-flight (D-1) and pre-post flight. The time delay between the acceleration step stimulus and the subjective response was consistently reduced during weightlessness, but was neither statistically significant nor of functional importance. Increased variability of responses when going from one environment to the other was apparent from measurements on the first day of the mission and in the first days post-flight. Subjective reports of perceived motion during sinusoidal oscillation in weightlessness were qualitatively similar to reports on earth. In a closed-loop motion nulling task, enhanced performance was observed post-flight in all crewmembers tested in the Y or Z axes.

NASA Discipline Number 16-10