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NASA NTRS1997

Response properties of pigeon otolith afferents to linear acceleration

In the present study, the sensitivity to sinusoidal linear accelerations in the plane of the utricular macula was tested in afferents. The head orientation relative to the translation axis was varied in order to determine the head position that elicited the maximal and minimal responses for each afferent. The response gain and phase values obtained to 0.5-Hz and 2-Hz linear acceleration stimuli were then plotted as a function of head orientation and a modified cosine function was fit to the data. From the best-fit cosine function, the predicted head orientations that would produce the maximal and minimal response gains were estimated. The estimated maximum response gains to linear acceleration in the utricular plane for the afferents varied between 75 and 1420 spikes s-1 g-1. The mean maximal gains for all afferents to 0.5-Hz and 2-Hz sinusoidal linear acceleration stimuli were 282 and 367 spikes s-1 g-1, respectively. The minimal response gains were essentially zero for most units. The response phases always led linear acceleration and remained constant for each afferent, regardless of head orientation. These response characteristics indicate that otolith afferents are cosine tuned and behave as one-dimensional linear accelerometers. The directions of maximal sensitivity to linear acceleration for the afferents varied throughout the plane of the utricle; however, most vectors were directed out of the opposite ear near the interaural axis. The response dynamics of the afferents were tested using stimulus frequencies ranging between 0.25 Hz and 10 Hz (0.1 g peak acceleration). Across stimulus frequencies, most afferents had increasing gains and constant phase values. These dynamic properties for individual afferents were fit with a simple transfer function that included three parameters: a mechanical time constant, a gain constant, and a fractional order distributed adaptation operator.

Non-NASA Center↗

NASA NTRS1997

Microgravity vestibular investigations: perception of self-orientation and self-motion

Four astronauts experienced passive whole-body rotation in a number of test sessions during a 7-day orbital mission. Pitch (Y-axis) and roll (X-axis) rotation required subject orientations on the rotator in which the otolith system was at radius of 0.5 m. Thus subjects experienced a constant -0.22 Gz stimulus to the otoliths during the 60 s constant-velocity segments of "pitch" and "roll" ramp profiles. The Gz stimulus, a radius-dependent vector ranging from -0.22 Gz at the otoliths to +0.36 Gz at the feet, generated sensory information that was not interpreted as inversion in any of the 16 tests carried out in flight (12 in pitch and 4 in roll orientation). None of the subjects was rotated with head off-center during the first 33 h of the mission. In the state of orbital adaptation of these subjects, a -0.22 Gz otolith stimulus did not provide a vertical reference in the presence of a gradient of +Gz stimuli to the trunk and legs.

NASA Experiment Number 284058↗

NASA NTRS1996

Spatial orientation perception and reflexive eye movements--a perspective, an overview, and some clinical implications

When head motion includes a linear velocity component, eye velocity required to track an earth-fixed target depends upon: a) angular and linear head velocity, b) target distance, and c) direction of gaze relative to the motion trajectory. Recent research indicates that eye movements (LVOR), presumably otolith-mediated, partially compensate for linear velocity in small head excursions on small devices. Canal-mediated eye velocity (AVOR), otolith-mediated eye velocity (LVOR), and Ocular Torsion (OT) can be measured, one by one, on small devices. However, response dynamics that depend upon the ratio of linear to angular velocity in the motion trajectory and on subject orientation relative to the trajectory are present in a centrifuge paradigm. With this paradigm, two 3-min runs yields measures of: LVOR differentially modulated by different subject orientations in the two runs; OT dynamics in four conditions; two directions of "steady-state" OT, and two directions of AVOR. Efficient assessment of the dynamics (and of the underlying central integrative processes) may require a centrifuge radius of 1.0 meters or more. Clinical assessment of the spatial orientation system should include evaluation of central integrative processes that determine the dynamics of these responses.

Review, Tutorial↗

NASA NTRS1995

Vestibular plasticity following orbital spaceflight: recovery from postflight postural instability

Results of previous studies suggested that the vestibular mediated postural instability observed in astronauts upon return to earth from orbital spaceflight may be exacerbated by an increased weighting of visual inputs for spatial orientation and control of movement. This study was performed to better understand the roles of visual and somatosensory contributions to recovery of normal sensori-motor postural control in returning astronauts. Preflight and postflight, 23 astronaut volunteers were presented randomly with three trials of six sensory organization test (SOT) conditions in the EquiTest system test battery. Sagittal plane center-of-gravity (COG) excursions computed from ground reaction forces were significantly higher on landing day than preflight for those test conditions presenting sway-referenced visual and/or somatosensory orientation cues. The ratio of summed peak-to-peak COG sway amplitudes on the two sway-referenced vision tests (SOTs 3 + 6) compared to the two eyes closed tests (SOTs 2 + 5) was increased on landing day, indicating an increased reliance on visual orientation cues for postural control. The ratio of peak-to-peak COG excursions on sway-referenced surfaces (SOTs 4, 5 & 6) to an earth fixed support surfaces (SOTs 1, 2 & 3) increased even more after landing suggesting primary reliance on somatosensory orientation cues for recovery of postflight postural stability. Readaptation to sway-referenced support surfaces took longer than readaptation to sway-referenced vision. The increased reliance on visual and somatosensory inputs disappeared in all astronauts 4-8 days following return to earth.

NASA Program Space Physiology and Countermeasures↗

NASA NTRS1995

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↗

NASA NTRS1995

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↗

NASA NTRS1995

Retinal, attentional, and causal aspects of illusory-motion directionality

Extended objects presented instantaneously appeared to propagate or grow into their final shape. A strong bias was found toward perceiving straight lines to grow away from the observer's point of fixation. If attention and fixation were not directed to the same point of the visual field, both influenced illusory motion directionality, and if another small object was present on the screen at a location that was neither fixated nor attended to, the object that was instantaneously presented seemed to grow away from this point. Thus, three factors are involved in illusory-motion directionality: biases toward perceiving objects spreading away from the fixation point, away from an attended area, and away from preexisting objects. The experiments indicate that a satisfactory explanation of the illusion has to include bottom-up and top-down processes. They also challenge existing theories of motion detection.

Pattern Recognition, Visual/physiology↗

NASA NTRS1994

Comparative transduction mechanisms of hair cells in the bullfrog utriculus. II. Sensitivity and response dynamics to hair bundle displacement

1. Hair cells in whole-mount in vitro preparations of the utricular macula of the bullfrog (Rana catesbeiana) were selected according to their macular location and hair bundle morphology. The sensitivity and response dynamics of selected hair cells to natural stimulation were examined by recording their voltage responses to step and sinusoidal hair bundle displacements applied to their longest stereocilia. 2. The voltage responses of 31 hair cells to sinusoidal hair bundle displacements were characterized by their gains and phases, taken with respect to peak hair bundle displacement. The gains of Type B and Type C cells at both 0.5 and 5.0 Hz were markedly lower than those of Type F and Type E cells. Phases, with the exception of Type C cells, lagged hair bundle displacement at 0.5 Hz. Type C cells had phase leads of 25-40 degrees. At 5.0 Hz, response phases in all cells were phase lagged with respect to those at 0.5 Hz. Type C cells had larger gains and smaller phase leads at 5.0 Hz than at 0.5 Hz, suggesting the presence of low-frequency adaptation. 3. Displacement-response curves, derived from the voltage responses to 5.0-Hz sinusoids, were sigmoidal in shape and asymmetrical, with the depolarizing response having a greater magnitude and saturating less abruptly than the hyperpolarizing response. When normalized to their largest displacement the linear ranges of these curves varied from < 0.5 to 1.25 microns and were largest in Type B and smallest in Type F and Type E cells. Sensitivity, defined as the slope of the normalized displacement-response curve, was inversely correlated with linear range. 4. The contribution of geometric factors associated with the hair bundle to linear range and sensitivity were predicted from realistic models of utricular hair bundles created using morphological data obtained from light and electron microscopy. Three factors, including 1) the inverse ratio of the lengths of the kinocilium and longest stereocilia, representing the lever arm between kinociliary and stereociliary displacement; 2) tip link extension/linear displacement, largely a function of stereociliary height and separation; and 3) stereociliary number, an estimate of the number of transduction channels, were considered in this analysis. The first of these factors was quantitatively more important than the latter two factors and their total contribution was largest in Type B and Type C cells. Theoretical models were also used to calculate the relation between rotary and linear displacement.(ABSTRACT TRUNCATED AT 400 WORDS).

Non-NASA Center↗

NASA NTRS1994

Orientation of human optokinetic nystagmus to gravity: a model-based approach

Optokinetic nystagmus (OKN) was induced by having subjects watch a moving display in a binocular, head-fixed apparatus. The display was composed of 3.3 degrees stripes moving at 35 degrees/s for 45 s. It subtended 88 degrees horizontally by 72 degrees vertically of the central visual field and could be oriented to rotate about axes that were upright or tilted 45 degrees or 90 degrees. The head was held upright or was tilted 45 degrees left or right on the body during stimulation. Head-horizontal (yaw axis) and head-vertical (pitch axis) components of OKN were recorded with electro-oculography (EOG). Slow phase velocity vectors were determined and compared with the axis of stimulation and the spatial vertical (gravity axis). With the head upright, the axis of eye rotation during yaw axis OKN was coincident with the stimulus axis and the spatial vertical. With the head tilted, a significant vertical component of eye velocity appeared during yaw axis stimulation. As a result the axis of eye rotation shifted from the stimulus axis toward the spatial vertical. Vertical components developed within 1-2 s of stimulus onset and persisted until the end of stimulation. In the six subjects there was a mean shift of the axis of eye rotation during yaw axis stimulation of approximately 18 degrees with the head tilted 45 degrees on the body. Oblique optokinetic stimulation with the head upright was associated with a mean shift of the axis of eye rotation toward the spatial vertical of 9.2 degrees. When the head was tilted and the same oblique stimulation was given, the axis of eye rotation rotated to the other side of the spatial vertical by 5.4 degrees. This counterrotation of the axis of eye rotation is similar to the "Muller (E) effect," in which the perception of the upright is counterrotated to the opposite side of the spatial vertical when subjects are tilted in darkness. The data were simulated by a model of OKN with a "direct" and "indirect" pathway. It was assumed that the direct visual pathway is oriented in a body, not a spatial frame of reference. Despite the short optokinetic after-nystagmus time constants, strong horizontal to vertical cross-coupling could be produced if the horizontal and vertical time constants were in proper ratio and there were no suppression of nystagmus in directions orthogonal to the stimulus direction. The model demonstrates that the spatial orientation of OKN can be achieved by restructuring the system matrix of velocity storage. We conclude that an important function of velocity storage is to orient slow-phase velocity toward the spatial vertical during movement in a terrestrial environment.

Non-NASA Center↗

NASA NTRS1993

Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration

1. Extracellular recordings were made in and around the medial vestibular nuclei in decerebrated rats. Neurons were functionally identified according to their semicircular canal input on the basis of their responses to angular head rotations around the yaw, pitch, and roll head axes. Those cells responding to angular acceleration were classified as either horizontal semicircular canal-related (HC) or vertical semicircular canal-related (VC) neurons. The HC neurons were further characterized as either type I or type II, depending on the direction of rotation producing excitation. Cells that lacked a response to angular head acceleration, but exhibited sensitivity to a change in head position, were classified as purely otolith organ-related (OTO) neurons. All vestibular neurons were then tested for their response to sinusoidal linear translation in the horizontal head plane. 2. Convergence of macular and canal inputs onto central vestibular nuclei neurons occurred in 73% of the type I HC, 79% of the type II HC, and 86% of the VC neurons. Out of the 223 neurons identified as receiving macular input, 94 neurons were further studied, and their spatiotemporal response properties to sinusoidal stimulation with pure linear acceleration were quantified. Data were obtained from 33 type I HC, 22 type II HC, 22 VC, and 17 OTO neurons. 3. For each neuron the angle of the translational stimulus vector was varied by 15, 30, or 45 degrees increments in the horizontal head plane. In all tested neurons, a direction of maximum sensitivity was identified. An interesting difference among neurons was their response to translation along the direction perpendicular to that that produced the maximum response ("null" direction). For the majority of neurons tested, it was possible to evoke a nonzero response during stimulation along the null direction always had response phases that varied as a function of stimulus direction. 4. These spatiotemporal response properties were quantified in two independent ways. First, the data were evaluated on the basis of the traditional one-dimensional principle governed by the "cosine gain rule" and constant response phase at different stimulus orientations. Second, the response gain and phase values that were empirically determined for each orientation of the applied linear stimulus vector were fitted on the basis of a newly developed formalism that treats neuronal responses as exhibiting two-dimensional spatial sensitivity. Thus two response vectors were determined for each neuron on the basis of its response gain and phase at different stimulus directions in the horizontal head plane.(ABSTRACT TRUNCATED AT 400 WORDS).

NASA Discipline Neuroscience↗

NASA NTRS1993

Space vestibulo-neuroscience in the new century

In the new century there will probably be more long spaceflights and fewer short spaceflights. There will probably be several flights to Mars, flights that (if chemical rockets are used) will involve one year to get there, a second year on Mars, and a third year to return. The three-year Mars scenario will probably include rotation of the spacecraft to provide artificial gravity. If nuclear thermal rockets are used, a manned exploration of Mars could be accomplished in less than one year. Vestibular research will be directed towards ensuring that astronauts, upon landing on Mars, will be able to walk with confidence and without delay. Research will be required to investigate vestibular adaptation in spaceflight, motion sickness, and the vestibular effects of rotation in spaceflight.

NASA Discipline Neuroscience↗

NASA NTRS1993

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↗

NASA NTRS1991

Modeling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies

1. A generalized three-dimensional state space model of visual vestibular interaction was developed. Matrix and dynamical system operators associated with inputs from the semicircular canals, otolith velocity estimator, and the visual system have been incorporated into the model, which focus on their relationship to the velocity storage integrator. 2. A relationship was postulated between the eigenvalues and the direction of the eigenvectors of the system matrix and the orientation of the spatial vertical. It was assumed that the system matrix for a tilted position was a composition of two linear transformations of the system matrix for the upright position. One transformation modifies the eigenvalues of the system matrix, whereas another rotates the eigenvectors of the system matrix. The pitch and roll eigenvectors rotate with the head, whereas the yaw axis eigenvector remains approximately spatially invariant. 3. Based on the three-dimensional model, a computational procedure was formulated to identify the eigenvalues and eigenvectors of the system matrix with the use of a modification of the marquardt algorithm. With the use of data obtained from a monkey, it was shown that the three-dimensional behavior of velocity storage cannot be predicted solely in terms of its time constants, i.e., the inverse of its eigenvalues. With the use of the same eigenvalues the data could either be fit or not fit, depending on the eigenvector directions. Therefore, it is necessary to specify eigenvector directions when characterizing velocity storage in three dimensions. 4. Parameters found with the use of the Marquardt algorithm were incorporated into the model. Diagonal matrices in a head coordinate frame were introduced for coupling the visual system to the integrator and to the direct optokinetic pathway. Simulations of optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN) were run. The model predicted the behavior of yaw and pitch OKN and OKAN when the animal is upright. It also predicted the cross-coupling in the side down position. The trajectories in velocity space were also accurately simulated. 5. One of the predictions of the model is that when the stimulus direction is along an eigenvector, the trajectory in velocity space is a straight line. Using the "spectral width" of the residuals from a straight line sequence during OKAN, we developed a methodology to estimate how close the OKAN decay was to an eigenvector trajectory. 6. Thus we have developed a model-based approach for studying and interpreting the response characteristics of velocity storage in three dimensions.(ABSTRACT TRUNCATED AT 400 WORDS).

Non-NASA Center↗

NASA NTRS1986

M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 2. Visual vestibular tilt interaction in weightlessness

Adaptation to weightlessness includes the substitution of other sensory signals for the no longer appropriate graviceptor information concerning static spatial orientation. Visual-vestibular interaction producing roll circularvection was studied in weightlessness to assess the influence of otolith cues on spatial orientation. Preliminary results from four subjects tested on Spacelab-1 indicate that visual orientation effects were stronger in weightlessness than pre-flight. The rod and frame test of visual field dependence showed a weak post-flight increase in visual influence. Localized tactile cues applied to the feet in space reduced subjective vection strength.

Non-NASA Center↗

NASA NTRS1993

Perceived self-orientation and self-motion in microgravity, after landing and during preflight adaptation training

The research described in this paper is intended to support development and evaluation of preflight adaptation training (PAT) apparatus and procedures. Successful training depends on appropriate manipulation of visual and inertial stimuli that control perception of self-motion and self-orientation. For one part of this process, astronauts are trained to report their self-motion and self-orientation experiences. Before their space mission, they are exposed to the altered sensory environments produced by the PAT trainers. During and after the mission, they report their motion and orientation experiences. Subsequently, they are again exposed to the PAT trainers and are asked to describe relationships between their experiences in microgravity and following entry and their experiences in the trainers.

Space Flight↗

NASA NTRS2005

Expansion of direction space around the cardinal axes revealed by smooth pursuit eye movements

It is well established that perceptual direction discrimination shows an oblique effect; thresholds are higher for motion along diagonal directions than for motion along cardinal directions. Here, we compare simultaneous direction judgments and pursuit responses for the same motion stimuli and find that both pursuit and perceptual thresholds show similar anisotropies. The pursuit oblique effect is robust under a wide range of experimental manipulations, being largely resistant to changes in trajectory (radial versus tangential motion), speed (10 versus 25 deg/s), directional uncertainty (blocked versus randomly interleaved), and cognitive state (tracking alone versus concurrent tracking and perceptual tasks). Our data show that the pursuit oblique effect is caused by an effective expansion of direction space surrounding the cardinal directions and the requisite compression of space for other directions. This expansion suggests that the directions around the cardinal directions are in some way overrepresented in the visual cortical pathways that drive both smooth pursuit and perception.

Visual Pathways/physiology↗

NASA NTRS2005

Properties of cerebellar fastigial neurons during translation, rotation, and eye movements

The most medial of the deep cerebellar nuclei, the fastigial nucleus (FN), receives sensory vestibular information and direct inhibition from the cerebellar vermis. We investigated the signal processing in the primate FN by recording single-unit activities during translational motion, rotational motion, and eye movements. Firing rate modulation during horizontal plane translation in the absence of eye movements was observed in all non-eye-movement-sensitive cells and 26% of the pursuit eye-movement-sensitive neurons in the caudal FN. Many non-eye-movement-sensitive cells recorded in the rostral FN of three fascicularis monkeys exhibited convergence of signals from both the otolith organs and the semicircular canals. At low frequencies of translation, the majority of these rostral FN cells changed their firing rates in phase with head velocity rather than linear acceleration. As frequency increased, FN vestibular neurons exhibited a wide range of response dynamics with most cells being characterized by increasing phase leads as a function of frequency. Unlike cells in the vestibular nuclei, none of the rostral FN cells responded to rotational motion alone, without simultaneously exhibiting sensitivity to translational motion. Modulation during earth-horizontal axis rotation was observed in more than half (77%) of the neurons, although with smaller gains than during translation. In contrast, only 47% of the cells changed their firing rates during earth-vertical axis rotations in the absence of a dynamic linear acceleration stimulus. These response properties suggest that the rostral FN represents a main processing center of otolith-driven information for inertial motion detection and spatial orientation.

Non-NASA Center↗

NASA NTRS2004

Path perception during rotation: influence of instructions, depth range, and dot density

How do observers perceive their direction of self-motion when traveling on a straight path while their eyes are rotating? Our previous findings suggest that information from retinal flow and extra-retinal information about eye movements are each sufficient to solve this problem for both perception and active control of self-motion [Vision Res. 40 (2000) 3873; Psych. Sci. 13 (2002) 485]. In this paper, using displays depicting translation with simulated eye rotation, we investigated how task variables such as instructions, depth range, and dot density influenced the visual system's reliance on retinal vs. extra-retinal information for path perception during rotation. We found that path errors were small when observers expected to travel on a straight path or with neutral instructions, but errors increased markedly when observers expected to travel on a curved path. Increasing depth range or dot density did not improve path judgments. We conclude that the expectation of the shape of an upcoming path can influence the interpretation of the ambiguous retinal flow. A large depth range and dense motion parallax are not essential for accurate path perception during rotation, but reference objects and a large field of view appear to improve path judgments.

Space Perception/physiology↗