Assessing misperception of rotation in benign paroxysmal positional vertigo with static and dynamic visual images.

BACKGROUND: Perception of self-motion is difficult for patients to describe. In addition, the relationship between perceived rotation and eye movements is poorly understood, because most studies of patients have investigated only static orientation. OBJECTIVE: First, to determine whether patients with benign paroxysmal positional vertigo (BPPV) can use visual images to report perceived rotation elicited by the Dix-Hallpike maneuver. Second, to determine if the direction of patients' perceptions align with data on classical nystagmus direction. METHODS: After the Dix-Hallpike maneuver, BPPV patients viewed images - sketches or video animations - representing possible perceived motions. They selected one or more images representing perception. RESULTS: All subjects could select images. The directions of the videos were most often backward pitch and/ or ipsilateral roll and yaw relative to body orientation in the supine Dix-Hallpike position, generally consistent with the canal stimulus. Perceived direction of rotation was statistically significantly different from the direction of eye movements as published previously, suggesting a difference in mechanisms for perception and eye movements. CONCLUSION: Patients can easily learn to use a video language to describe their experiences. Perception is generally aligned with canal stimulus and nystagmus, but not exactly.

Asymmetries and three-dimensional features of vestibular cross-coupled stimuli illuminated through modeling.

Head movements during sustained rotation can cause angular cross-coupling which leads to tumbling illusions. Even though angular vectors predict equal magnitude illusions for head movements in opposite directions, the magnitudes of the illusions are often surprisingly asymmetric, such as during leftward versus rightward yaw while horizontal in a centrifuge. This paper presents a comprehensive investigation of the angular-linear stimulus combinations from eight different published papers in which asymmetries were found. Interactions between all angular and linear vectors, including gravity, are taken into account to model the three-dimensional consequences of the stimuli. Three main results followed. First, for every pair of head yaw movements, an asymmetry was found in the stimulus itself when considered in a fully three-dimensional manner, and the direction of the asymmetry matched the subjectively reported magnitude asymmetry. Second, for pitch and roll head movements for which motion sickness was measured, the stimulus was found symmetric in every case except one, and motion sickness generally aligned with other factors such as the existence of a head rest. Third, three-dimensional modeling predicted subjective inconsistency in the direction of perceived rotation when linear and angular components were oppositely-directed, and predicted surplus illusory rotation in the direction of head movement.

Sensory conflict compared in microgravity, artificial gravity, motion sickness, and vestibular disorders.

UNLABELLED: Perceptual disturbances and motion sickness are often attributed to sensory conflict. We investigated several conditions: head movements in microgravity, periodic motions in 1-g, and locomotion with vestibular disorders. In every case, linear vectors such as linear and gravitational acceleration are crucial factors, as previously found for head movements in artificial gravity, and thus the importance of measuring linear vectors emerges as a common theme. By modeling the sensory conflict between the vestibular and somatosensory systems, we computed a measure of linear conflict known as the "Stretch Factor". We hypothesized that the motions with the greatest Stretch Factor would be the most provocative motions. RESULTS: For head movements in microgravity, the Stretch Factor can explain why fast movements are more provocative than slow movements, and why pitch movements are more provocative than yaw movements. For off-vertical-axis rotation (OVAR) in 1-g, the Stretch Factor predicts that the most provocative frequency is higher than that for vertical linear oscillation (VLO). For example, the same sensor dynamics can predict a most provocative frequency around 0.2 Hz for VLO but 0.3 Hz for OVAR, solving a mystery of this experimentally observed discrepancy. Finally, we determined that certain sensory conflict perceptions reported by vestibular patients could be explained via mathematical simulation.

Differences between perception and eye movements during complex motions.

During passive whole-body motion in the dark, the motion perceived by subjects may or may not be veridical. Either way, reflexive eye movements are typically compensatory for the perceived motion. However, studies are discovering that for certain motions, the perceived motion and eye movements are incompatible. The incompatibility has not been explained by basic differences in gain or time constants of decay. This paper uses three-dimensional modeling to investigate gondola centrifugation (with a tilting carriage) and off-vertical axis rotation. The first goal was to determine whether known differences between perceived motions and eye movements are true differences when all three-dimensional combinations of angular and linear components are considered. The second goal was to identify the likely areas of processing in which perceived motions match or differ from eye movements, whether in angular components, linear components and/or dynamics. The results were that perceived motions are more compatible with eye movements in three dimensions than the one-dimensional components indicate, and that they differ more in their linear than their angular components. In addition, while eye movements are consistent with linear filtering processes, perceived motion has dynamics that cannot be explained by basic differences in time constants, filtering, or standard GIF-resolution processes.

Phase-linking and the perceived motion during off-vertical axis rotation.

Human off-vertical axis rotation (OVAR) in the dark typically produces perceived motion about a cone, the amplitude of which changes as a function of frequency. This perception is commonly attributed to the fact that both the OVAR and the conical motion have a gravity vector that rotates about the subject. Little-known, however, is that this rotating-gravity explanation for perceived conical motion is inconsistent with basic observations about self-motion perception: (a) that the perceived vertical moves toward alignment with the gravito-inertial acceleration (GIA) and (b) that perceived translation arises from perceived linear acceleration, as derived from the portion of the GIA not associated with gravity. Mathematically proved in this article is the fact that during OVAR these properties imply mismatched phase of perceived tilt and translation, in contrast to the common perception of matched phases which correspond to conical motion with pivot at the bottom. This result demonstrates that an additional perceptual rule is required to explain perception in OVAR. This study investigates, both analytically and computationally, the phase relationship between tilt and translation at different stimulus rates-slow (45 degrees /s) and fast (180 degrees /s), and the three-dimensional shape of predicted perceived motion, under different sets of hypotheses about self-motion perception. We propose that for human motion perception, there is a phase-linking of tilt and translation movements to construct a perception of one's overall motion path. Alternative hypotheses to achieve the phase match were tested with three-dimensional computational models, comparing the output with published experimental reports. The best fit with experimental data was the hypothesis that the phase of perceived translation was linked to perceived tilt, while the perceived tilt was determined by the GIA. This hypothesis successfully predicted the bottom-pivot cone commonly reported and a reduced sense of tilt during fast OVAR. Similar considerations apply to the hilltop illusion often reported during horizontal linear oscillation. Known response properties of central neurons are consistent with this ability to phase-link translation with tilt. In addition, the competing "standard" model was mathematically proved to be unable to predict the bottom-pivot cone regardless of the values used for parameters in the model.

Spatial disorientation in gondola centrifuges predicted by the form of motion as a whole in 3-D.

INTRODUCTION: During a coordinated turn, subjects can misperceive tilts. Subjects accelerating in tilting-gondola centrifuges without external visual reference underestimate the roll angle, and underestimate more when backward-facing than when forward-facing. In addition, during centrifuge deceleration, the perception of pitch can include tumble while paradoxically maintaining a fixed perceived pitch angle. The goal of the present research was to test two competing hypotheses: 1) that components of motion are perceived relatively independently and then combined to form a three-dimensional (3-D) perception; and 2) that perception is governed by familiarity of motions as a whole in three dimensions, with components depending more strongly on the overall shape of the motion. METHODS: Published experimental data from existing tilting-gondola centrifuge studies were used. The two hypotheses were implemented formally in computer models, and centrifuge acceleration and deceleration were simulated. RESULTS: The second, whole-motion oriented hypothesis better predicted subjects' perceptions, including the forward-backward asymmetry and the paradoxical tumble upon deceleration. The predominant stimulus at the beginning of the motion and the familiarity of centripetal acceleration were important factors. CONCLUSION: Three-dimensional perception is better predicted by taking into account familiarity with the form of 3-D motion.

Constructive perception of self-motion.

This review focusses attention on a ragged edge of our knowledge of self-motion perception, where understanding ends but there are experimental results to indicate that present approaches to analysis are inadequate. Although self-motion perception displays processes of "top-down" construction, it is typically analyzed as if it is nothing more than a deformation of the stimulus, using a "bottom-up" and input/output approach beginning with the transduction of the stimulus. Analysis often focusses on the extent to which passive transduction of the movement stimulus is accurate. Some perceptual processes that deform or transform the stimulus arise from the way known properties of sensory receptors contribute to perceptual accuracy or inaccuracy. However, further constructive processes in self-motion perception that involve discrete transformations are not well understood. We introduce constructive perception with a linguistic example which displays familiar discrete properties, then look closely at self-motion perception. Examples of self-motion perception begin with cases in which constructive processes transform particular properties of the stimulus. These transformations allow the nervous system to compose whole percepts of movement; that is, self-motion perception acts at a whole-movement level of analysis, rather than passively transducing individual cues. These whole-movement percepts may be paradoxical. In addition, a single stimulus may give rise to multiple perceptions. After reviewing self-motion perception studies, we discuss research methods for delineating principles of the constructed perception of self-motion. The habit of viewing self-motion illusions only as continuous deformations of the stimulus may be blinding the field to other perceptual phenomena, including those best characterized using the mathematics of discrete transformations or mathematical relationships relating sensory modalities in novel, sometimes discrete ways. Analysis of experiments such as these is required to mathematically formalize elements of self-motion perception, the transformations they may undergo, consistency principles, and logical structure underlying multiplicity of perceptions. Such analysis will lead to perceptual rules analogous to those recognized in visual perception.

Whole-motion model of perception during forward- and backward-facing centrifuge runs.

Illusory perceptions of motion and orientation arise during human centrifuge runs without vision. Asymmetries have been found between acceleration and deceleration, and between forward-facing and backward-facing runs. Perceived roll tilt has been studied extensively during upright fixed-carriage centrifuge runs, and other components have been studied to a lesser extent. Certain, but not all, perceptual asymmetries in acceleration-vs-deceleration and forward-vs-backward motion can be explained by existing analyses. The immediate acceleration-deceleration roll-tilt asymmetry can be explained by the three-dimensional physics of the external stimulus; in addition, longer-term data has been modeled in a standard way using physiological time constants. However, the standard modeling approach is shown in the present research to predict forward-vs-backward-facing symmetry in perceived roll tilt, contradicting experimental data, and to predict perceived sideways motion, rather than forward or backward motion, around a curve. The present work develops a different whole-motion-based model taking into account the three-dimensional form of perceived motion and orientation. This model predicts perceived forward or backward motion around a curve, and predicts additional asymmetries such as the forward-backward difference in roll tilt. This model is based upon many of the same principles as the standard model, but includes an additional concept of familiarity of motions as a whole.

Effect of radius versus rotation speed in artificial gravity.

Artificial gravity by centrifugation can lead to perceptual disturbances in the form of motion sickness and/or misperception of motion during head movements, but the degree of perceptual disturbance during centrifugation in 0-g has not been thoroughly investigated. It is known that during whole-body on-axis yaw rotation in 0-g, head movements in pitch and roll cause very little disturbance, despite significant disturbance in 1-g. Therefore, 1-g experimental results do not apply directly to 0-g without further analysis. A modeling approach was used here to predict disorienting effects in 0-g and 1-g environments, with different rotation speeds, centrifuge radii, and directions of head movement. The results were based upon investigation of the stimulus itself, in the form of angular and linear accelerations, and their consequences due to linear-angular interactions in three dimensions. The results explain known differences in 0-g and 1-g, for head turns toward and away from the direction of motion, and for head movements on- and off-axis. Additional predictions include an increase in perceptual disturbance with the magnitude of the gravito-inertial acceleration (GIA), therefore an increase off-axis, but a decrease in 0-g. Also predicted is that head-movement direction makes a difference, with rotation outward relative to the centrifuge axis causing the least disturbance.

Head tilt-translation combinations distinguished at the level of neurons.

Angular and linear accelerations of the head occur throughout everyday life, whether from external forces such as in a vehicle or from volitional head movements. The relative timing of the angular and linear components of motion differs depending on the movement. The inner ear detects the angular and linear components with its semicircular canals and otolith organs, respectively, and secondary neurons in the vestibular nuclei receive input from these vestibular organs. Many secondary neurons receive both angular and linear input. Linear information alone does not distinguish between translational linear acceleration and angular tilt, with its gravity-induced change in the linear acceleration vector. Instead, motions are thought to be distinguished by use of both angular and linear information. However, for combined motions, composed of angular tilt and linear translation, the infinite range of possible relative timing of the angular and linear components gives an infinite set of motions among which to distinguish the various types of movement. The present research focuses on motions consisting of angular tilt and horizontal translation, both sinusoidal, where the relative timing, i.e. phase, of the tilt and translation can take any value in the range -180 degrees to 180 degrees . The results show how hypothetical neurons receiving convergent input can distinguish tilt from translation, and that each of these neurons has a preferred combined motion, to which the neuron responds maximally. Also shown are the values of angular and linear response amplitudes and phases that can cause a neuron to be tilt-only or translation-only. Such neurons turn out to be sufficient for distinguishing between combined motions, with all of the possible relative angular-linear phases. Combinations of other neurons, as well, are shown to distinguish motions. Relative response phases and in-phase firing-rate modulation are the key to identifying specific motions from within this infinite set of combined motions.

Vestibular coriolis effect differences modeled with three-dimensional linear-angular interactions.

The vestibular coriolis (or "cross-coupling") effect is traditionally explained by cross-coupled angular vectors, which, however, do not explain the differences in perceptual disturbance under different acceleration conditions. For example, during head roll tilt in a rotating chair, the magnitude of perceptual disturbance is affected by a number of factors, including acceleration or deceleration of the chair rotation or a zero-g environment. Therefore, it has been suggested that linear-angular interactions play a role. The present research investigated whether these perceptual differences and others involving linear coriolis accelerations could be explained under one common framework: the laws of motion in three dimensions, which include all linear-angular interactions among all six components of motion (three angular and three linear). The results show that the three-dimensional laws of motion predict the differences in perceptual disturbance. No special properties of the vestibular system or nervous system are required. In addition, simulations were performed with angular, linear, and tilt time constants inserted into the model, giving the same predictions. Three-dimensional graphics were used to highlight the manner in which linear-angular interaction causes perceptual disturbance, and a crucial component is the Stretch Factor, which measures the "unexpected" linear component.

Perceptual disturbances predicted in zero-g through three-dimensional modeling.

Perceptual disturbances in zero-g and 1-g differ. For example, the vestibular coriolis (or "cross-coupled") effect is weaker in zero-g. In 1-g, blindfolded subjects rotating on-axis experience perceptual disturbances upon head tilt, but the effects diminish in zero-g. Head tilts during centrifugation in zero-g and 1-g are investigated here by means of three-dimensional modeling, using a model that was previously used to explain the zero-g reduction of the on-axis vestibular coriolis effect. The model's foundation comprises the laws of physics, including linear-angular interactions in three dimensions. Addressed is the question: In zero-g, will the vestibular coriolis effect be as weak during centrifugation as during on-axis rotation? Centrifugation in 1-g was simulated first, with the subject supine, head toward center. The most noticeable result concerned direction of head yaw. For clockwise centrifuge rotation, greater perceptual effects arose in simulations during yaw counterclockwise (as viewed from the top of the head) than for yaw clockwise. Centrifugation in zero-g was then simulated with the same "supine" orientation. The result: In zero-g the simulated vestibular coriolis effect was greater during centrifugation than during on-axis rotation. In addition, clockwise-counterclockwise differences did not appear in zero-g, in contrast to the differences that appear in 1-g.