Vestibular damage affects the precision and accuracy of navigation in a virtual visual environment.

Vestibular information is available to the brain during navigation, as are the other self-generated (idiothetic) and external (allothetic) sensorimotor cues that contribute to central estimates of position and motion. Rodent studies provide strong evidence that vestibular information contributes to navigation but human studies have been less conclusive. Furthermore, sex-based differences have been described in human navigation studies performed with the head stationary, a situation where dynamic vestibular (and other idiothetic) information is absent, but sex differences in the utilization of vestibular information have not been described. Here, we studied men and women with severe bilateral vestibular damage as they navigated through a visually barren virtual reality environment and compared their performance to normal men and women. Two navigation protocols were employed, which either activated dynamic idiothetic cues ('dynamic task', navigate by turning, walking in place) or eliminated them ('static task', navigate with key presses, head stationary). For both protocols, we employed a standard 'triangle completion task' in which subjects moved to two visual targets in series and then were required to return to their perceived starting position without localizing visual information. The angular and linear 'accuracy' (derived from response error) and 'precision' (derived from response variability) were calculated. Comparing performance 'within tasks', navigation on the dynamic paradigm was worse in male vestibular-deficient patients than in normal men but vestibular-deficient and normal women were equivalent; on the static paradigm, vestibular-deficient men (but not women) performed better than normal subjects. Comparing performance 'between tasks', normal men performed better on the dynamic than the static paradigm while vestibular-deficient men and both normal and vestibular-deficient women were equivalent on both tasks. Statistical analysis demonstrated that for the angular precision metric, sex had a significant effect on the interaction between vestibular status and the test paradigm. These results provide evidence that humans use vestibular information when they navigate in a virtual visual environment and that men and women may utilize vestibular (and visual) information differently. On our navigation paradigm, men used vestibular information to improve navigation performance, and in the presence of severe vestibular damage, they utilized visual information more effectively. In contrast, we did not find evidence that women used vestibular information while navigating on our virtual task, nor did we find evidence that they improved their utilization of visual information in the presence of severe vestibular damage.

Variation between individuals in sensorimotor feedback control of standing balance.

We examined intersubject variation in human balance, focusing on sensorimotor feedback. Our central hypothesis was that intersubject variation in balance characteristics arises from differences in central sensorimotor processing. Our second hypothesis was that similar sensorimotor feedback mechanisms are used for sagittal and frontal balance. Twenty-one adults stood on a continuously rotating platform with their eyes closed in the sagittal or frontal plane. Plant dynamics (mass, height, and inertia) and feedback control were included in a model of sensory weight, neural time delays, and sensory-to-motor scaling (stiffness, damping, and integral gains). Sway metrics [root-mean-square (RMS) sway and velocity] were moderately correlated between planes of motion (RMS: R = 0.66-0.69 and RMS velocity: R = 0.53-0.58). Sensory weight and integral gain exhibited the highest correlations between the plane of motion (R = 0.59 for sensory weight and R = 0.75 for integral gain during large stimuli). Compared with other subjects, people who adopted a high vestibular weight or large integral gain in one condition did so across all tests. Intersubject variation in sensory weight, stiffness, and integral gain were significantly associated with intersubject variation in RMS sway whereas sensory weight and time delay were the strongest significant predictors of RMS velocity. Multiple linear regression showed that intersubject variation in sway metrics was predicted better by intersubject variation in central feedback mechanisms vs. plant dynamics. Together, results supported the first hypothesis and partially supported the second hypothesis because only a subset of feedback processes was moderately or strongly correlated (mostly during large surface tilts) between planes of motion.NEW & NOTEWORTHY This study details naturally occurring intersubject variation in healthy adults' balance control. Experimental surface tilts evoked postural sway and sensorimotor modeling defined feedback control parameters. We determined the relation between intersubject variation in feedback control (vestibular and proprioceptive reliance, neural time delay, sensory-to-motor scaling) and intersubject variation in postural sway between planes of motion and between stimulus amplitudes.

Vestibular dysfunction in neurofibromatosis type 2-related schwannomatosis.

Neurofibromatosis type 2-related schwannomatosis is a genetic disorder characterized by neurologic tumours, most typically vestibular schwannomas that originate on the vestibulo-cochlear nerve(s). Although vestibular symptoms can be disabling, vestibular function has never been carefully analysed in neurofibromatosis type 2-related schwannomatosis. Furthermore, chemotherapy (e.g. bevacizumab) can reduce tumour volume and improve hearing in neurofibromatosis type 2-related schwannomatosis, but nothing is known about its vestibular effects. In this report, we studied the three primary vestibular-mediated behaviours (eye movements, motion perception and balance), clinical vestibular disability (dizziness and ataxia), and imaging and hearing in eight untreated patients with neurofibromatosis type 2-related schwannomatosis and compared their results with normal subjects and patients with sporadic, unilateral vestibular schwannoma tumours. We also examined how bevacizumab affected two patients with neurofibromatosis type 2-related schwannomatosis. Vestibular schwannomas in neurofibromatosis type 2-related schwannomatosis degraded vestibular precision (inverse of variability, reflecting a reduced central signal-to-noise ratio) but not vestibular accuracy (amplitude relative to ideal amplitude, reflecting the central signal magnitude) and caused clinical disability. Bevacizumab improved vestibular precision and clinical disability in both patients with neurofibromatosis type 2-related schwannomatosis but did not affect vestibular accuracy. These results demonstrate that vestibular schwannoma tumours in our neurofibromatosis type 2-related schwannomatosis population degrade the central vestibular signal-to-noise ratio, while bevacizumab improves the signal-to-noise ratio, changes that can be explained mechanistically by the addition (schwannoma) and suppression (bevacizumab) of afferent neural noise.

Your Vestibular Thresholds May Be Lower Than You Think: Cognitive Biases in Vestibular Psychophysics.

PURPOSE: Recently, there has been a surge of interest in measuring vestibular perceptual thresholds, which quantify the smallest motion that a subject can reliably perceive, to study physiology and pathophysiology. These thresholds are sensitive to age, pathology, and postural performance. Threshold tasks require decisions to be made in the presence of uncertainty. Since humans often rely on past information when making decisions in the presence of uncertainty, we hypothesized that (a) perceptual responses are affected by their preceding trial; (b) perceptual responses tend to be biased opposite of the "preceding response" because of cognitive biases but are not biased by the "preceding stimulus"; and (c) when fits do not account for this cognitive bias, thresholds are overestimated. To our knowledge, these hypotheses are unaddressed in vestibular and direction-recognition tasks. CONCLUSIONS: Results in normal subjects supported each hypothesis. Subjects tended to respond opposite of their preceding response (not the preceding stimulus), indicating a cognitive bias, and this caused an overestimation of thresholds. Using an enhanced model (MATLAB code provided) that considered these effects, average thresholds were lower (5.5% for yaw, 7.1% for interaural). Since the results indicate that the magnitude of cognitive bias varies across subjects, this enhanced model can reduce measurement variability and potentially improve the efficiency of data collection.

How Peripheral Vestibular Damage Affects Velocity Storage: a Causative Explanation.

Velocity storage is a centrally-mediated mechanism that processes peripheral vestibular inputs. One prominent aspect of velocity storage is its effect on dynamic responses to yaw rotation. Specifically, when normal human subjects are accelerated to constant angular yaw velocity, horizontal eye movements and perceived angular velocity decay exponentially with a time constant circa 15-30 s, even though the input from the vestibular periphery decays much faster (~ 6 s). Peripheral vestibular damage causes a time constant reduction, which is useful for clinical diagnoses, but a mechanistic explanation for the relationship between vestibular damage and changes in these behavioral dynamics is lacking. It has been hypothesized that Bayesian optimization determines ideal velocity storage dynamics based on statistics of vestibular noise and experienced motion. Specifically, while a longer time constant would make the central estimate of angular head velocity closer to actual head motion, it may also result in the accumulation of neural noise which simultaneously degrades precision. Thus, the brain may balance these two effects by determining the time constant that optimizes behavior. We applied a Bayesian optimal Kalman filter to determine the ideal velocity storage time constant for unilateral damage. Predicted time constants were substantially lower than normal and similar to patients. Building on our past work showing that Bayesian optimization explains age-related changes in velocity storage, we also modeled interactions between age-related hair cell loss and peripheral damage. These results provide a plausible mechanistic explanation for changes in velocity storage after peripheral damage. Results also suggested that even after peripheral damage, noise originating in the periphery or early central processing may remain relevant in neurocomputations. Overall, our findings support the hypothesis that the brain optimizes velocity storage based on the vestibular signal-to-noise ratio.

The predictive power of geographic health care utilization for unintentional fatal fall rates.

BACKGROUND: Falls are the leading cause of fatal and nonfatal injuries among adults over 65 years old. The increase in fall mortality rates is likely multifactorial. With a lack of key drivers identified to explain rising rates of death from falls, accurate predictive modelling can be challenging, hindering evidence-based health resource and policy efforts. The objective of this work is to examine the predictive power of geographic utilization and longitudinal trends in mortality from unintentional falls amongst different demographic and geographic strata. METHODS: This is a nationwide, retrospective cohort study using the United States Centers for Disease Control (CDC) Web-based Injury Statistics Query and Reporting System (WISQARS) database. The exposure was death from an unintentional fall as determined by the CDC. Outcomes included aggregate and trend crude and age-adjusted death rates. Health care utilization, reimbursement, and cost metrics were also compared. RESULTS: Over 2001 to 2018, 465,486 total deaths due to unintentional falls were recorded with crude and age-adjusted rates of 8.42 and 7.76 per 100,000 population respectively. Comparing age-adjusted rates, males had a significantly higher age-adjusted death rate (9.89 vs. 6.17; p <  0.00001), but both male and female annual age-adjusted mortality rates are expected to rise (Male: + 0.25 rate/year, R2= 0.98; Female: + 0.22 rate/year, R2= 0.99). There were significant increases in death rates commensurate with increasing age, with the adults aged 85 years or older having the highest aggregate (201.1 per 100,000) and trending death rates (+ 8.75 deaths per 100,000/year, R2= 0.99). Machine learning algorithms using health care utilization data were accurate in predicting geographic age-adjusted death rates. CONCLUSIONS: Machine learning models have high accuracy in predicting geographic age-adjusted mortality rates from health care utilization data. In the United States from 2001 through 2018, adults aged 85+ years carried the highest death rate from unintentional falls and this rate is forecasted to accelerate.

Imbalance and dizziness caused by unilateral vestibular schwannomas correlate with vestibulo-ocular reflex precision and bias.

Imbalance and dizziness are disabling symptoms for many patients with vestibular schwannomas (VS) but symptom severity typically does not correlate with the vestibulo-ocular reflex (VOR) amplitude-based metrics used to assess peripheral vestibular damage. In this study, we tested the hypothesis that imbalance and dizziness in patients with VS relate to VOR metrics that are not based on response amplitude. Twenty-four patients with unilateral, sporadic VS tumors were studied, and objective (balance) and subjective (dizziness) vestibular dysfunction was quantified. The VOR was tested using two yaw-axis motion stimuli, low-frequency en-bloc sinusoidal, and high-frequency head-on-body impulsive rotations. Imbalance correlated with VOR precision (the inverse of the trial-to-trial variability) and with low-frequency VOR dynamics (quantified with the time constant), and these two metrics were also strongly correlated. Dizziness correlated with the VOR bias caused by an imbalance in static central vestibular tone, but not with dynamic VOR metrics. VOR accuracy (mean response amplitude relative to the ideal response) was not correlated with the severity of imbalance or dizziness or with measures of VOR precision or time constant. Imbalance in patients with VS, therefore, scales with VOR precision and time constant, both of which appear to reflect the central vestibular signal-to-noise ratio, but not with VOR slow-phase accuracy, which is based on the magnitude of the central vestibular signals. Dizziness was related to the presence of a static central tone imbalance but not to any VOR metrics, suggesting that abnormal perception in VS may be affected by factors that are not captured by yaw-axis VOR measurements.NEW & NOTEWORTHY The severity of symptoms associated with unilateral vestibular schwannomas (VS) is poorly correlated with standard yaw-axis vestibulo-ocular reflex (VOR) metrics that are based on response amplitude. In this study, we show that the balance and perceptual dysfunction experienced by patients with VS scales with VOR metrics that capture information about the central signal-to-noise ratio (balance) and central static tone (dizziness), but are not correlated with the VOR gain, which reflects central signal amplitude.

Vestibular Precision at the Level of Perception, Eye Movements, Posture, and Neurons.

Precision and accuracy are two fundamental properties of any system, including the nervous system. Reduced precision (i.e., imprecision) results from the presence of neural noise at each level of sensory, motor, and perceptual processing. This review has three objectives: (1) to show the importance of studying vestibular precision, and specifically that studying accuracy without studying precision ignores fundamental aspects of the vestibular system; (2) to synthesize key hypotheses about precision in vestibular perception, the vestibulo-ocular reflex, posture, and neurons; and (3) to show that groups of studies that are thoughts to be distinct (e.g., perceptual thresholds, subjective visual vertical variability, neuronal variability) are actually "two sides of the same coin" - because the methods used allow results to be related to the standard deviation of a Gaussian distribution describing the underlying neural noise. Vestibular precision varies with age, stimulus amplitude, stimulus frequency, body orientation, motion direction, pathology, medication, and electrical/mechanical vestibular stimulation, but does not vary with sex. The brain optimizes precision during integration of vestibular cues with visual, auditory, and/or somatosensory cues. Since a common concern with precision metrics is time required for testing, we describe approaches to optimize data collection and provide evidence that fatigue and session effects are minimal. Finally, we summarize how precision is an individual trait that is correlated with clinical outcomes in patients as well as with performance in functional tasks like balance. These findings highlight the importance of studying vestibular precision and accuracy, and that knowledge gaps remain.

An Implanted Vestibular Prosthesis Improves Spatial Orientation in Animals with Severe Vestibular Damage.

Gravity is a pervasive environmental stimulus, and accurate graviception is required for optimal spatial orientation and postural stability. The primary graviceptors are the vestibular organs, which include angular velocity (semicircular canals) and linear acceleration (otolith organs) sensors. Graviception is degraded in patients with vestibular damage, resulting in spatial misperception and imbalance. Since minimal therapy is available for these patients, substantial effort has focused on developing a vestibular prosthesis or vestibular implant (VI) that reproduces information normally provided by the canals (since reproducing otolith function is very challenging technically). Prior studies demonstrated that angular eye velocity responses could be driven by canal VI-mediated angular head velocity information, but it remains unknown whether a canal VI could improve spatial perception and posture since these behaviors require accurate estimates of angular head position in space relative to gravity. Here, we tested the hypothesis that a canal VI that transduces angular head velocity and provides this information to the brain via motion-modulated electrical stimulation of canal afferent nerves could improve the perception of angular head position relative to gravity in monkeys with severe vestibular damage. Using a subjective visual vertical task, we found that normal female monkeys accurately sensed the orientation of the head relative to gravity during dynamic tilts, that this ability was degraded following bilateral vestibular damage, and improved when the canal VI was used. These results demonstrate that a canal VI can improve graviception in vestibulopathic animals, suggesting that it could reduce the disabling perceptual and postural deficits experienced by patients with severe vestibular damage.SIGNIFICANCE STATEMENT Patients with vestibular damage experience impaired vision, spatial perception, and balance, symptoms that could potentially respond to a vestibular implant (VI). Anatomic features facilitate semicircular canal (angular velocity) prosthetics but inhibit approaches with the otolith (linear acceleration) organs, and canal VIs that sense angular head velocity can generate compensatory eye velocity responses in vestibulopathic subjects. Can the brain use canal VI head velocity information to improve estimates of head orientation (e.g., head position relative to gravity), which is a prerequisite for accurate spatial perception and posture? Here we show that a canal VI can improve the perception of head orientation in vestibulopathic monkeys, results that are highly significant because they suggest that VIs mimicking canal function can improve spatial orientation and balance in vestibulopathic patients.

The role of vestibular cues in postural sway.

Controlling posture requires continuous sensory feedback about body motion and orientation, including from the vestibular organs. Little is known about the role of tilt vs. translation vs. rotation vestibular cues. We examined whether intersubject differences in vestibular function were correlated with intersubject differences in postural control. Vestibular function was assayed using vestibular direction-recognition perceptual thresholds, which determine the smallest motion that can be reliably perceived by a subject seated on a motorized platform in the dark. In study A, we measured thresholds for lateral translation, vertical translation, yaw rotation, and head-centered roll tilts. In study B, we measured thresholds for roll, pitch, and left anterior-right posterior and right anterior-left posterior tilts. Center-of-pressure (CoP) sway was measured in sensory organization tests (study A) and Romberg tests (study B). We found a strong positive relationship between CoP sway and lateral translation thresholds but not CoP sway and other thresholds. This finding suggests that the vestibular encoding of lateral translation may contribute substantially to balance control. Since thresholds assay sensory noise, our results support the hypothesis that vestibular noise contributes to spontaneous postural sway. Specifically, we found that lateral translation thresholds explained more of the variation in postural sway in postural test conditions with altered proprioceptive cues (vs. a solid surface), consistent with postural sway being more dependent on vestibular noise when the vestibular contribution to balance is higher. These results have potential implications for vestibular implants, balance prostheses, and physical therapy exercises.NEW & NOTEWORTHY Vestibular feedback is important for postural control, but little is known about the role of tilt cues vs. translation cues vs. rotation cues. We studied healthy human subjects with no known vestibular pathology or symptoms. Our findings showed that vestibular encoding of lateral translation correlated with medial-lateral postural sway, consistent with lateral translation cues contributing to balance control. This adds support to the hypothesis that vestibular noise contributes to spontaneous postural sway.

Corrigendum: Multivariate Analyses of Balance Test Performance, Vestibular Thresholds, and Age.

[This corrects the article DOI: 10.3389/fneur.2017.00578.].

The influence of target distance on perceptual self-motion thresholds and the vestibulo-ocular reflex during interaural translation.

An elegant and influential mathematical model of eye movements is the geometric compensation required for visual fixation location in the translational vestibulo-ocular reflex (VOR). Compensatory eye velocity scales with the inverse of fixation distance during head translation because larger angular eye movements are required to minimize retinal slip during head translation when targets are closer. This model has been extensively verified in experiments. Since the VOR and vestibular perception have shared anatomic pathways, we asked whether the same scaling may affect motion perception. Since perception does not require the linear-to-angular transformation required for the translational VOR, we hypothesized that perception would not scale with target distance. Subjects were tested with a motion direction-recognition threshold task in which they reported their perception of small translations of their body. Thresholds were measured in three conditions: (1) with a near target (0.20m) that extinguished just before each motion; (2) with a far target (0.47m); 3) with no target. The subject was always in darkness during motion. Thresholds were 0.59, 0.61 and 0.61cm/s, respectively. Translational VOR sensitivity (eye angular velocity divided by head translation velocity) was also measured and modulated with target distance. The scaling ratio of responses for the near vs. far target was 0.97 for perceptual thresholds, which was significantly different from the compensatory ratio (2.35; P<0.001) and the translational VOR scaling ratio (1.59; P=0.007) but not from no compensation (1.00; P=0.93). Thus, we conclude that despite shared anatomy for the VOR and perception, the brain processes signals according to the geometric functional constraints of each task.

Vestibular roll tilt thresholds partially mediate age-related effects on balance.

BACKGROUND: It has been well-established that both vestibular function and balance degrade with age and that balance degradation contributes to falls. While multiple causes contribute to balance declines, there have been few empirical investigations of the specific sensory contributors to balance that mediate (i.e., explain a significant fraction of) the effect of age on balance. OBJECTIVE: To determine if vestibular function significantly mediates the effect of age on balance, and to quantify the fraction of any such statistically significant age-effect on balance using previously published vestibular threshold and balance data. METHODS: Balance was quantified as complete/incomplete on a standard Romberg 4-condition foam balance test. Vestibular thresholds were determined using standard methods with motion provided by a Moog 6DOF motion platform. Standard mediation analyses were performed to determine if any of the five vestibular thresholds measured (0.2Hz roll tilt and 1Hz roll tilt, yaw rotation, y-translation, and z-translation) significantly mediated the previously reported age-effect on balance. RESULTS: 0.2Hz roll tilt thresholds were found to significantly mediate the relationship between age and balance, whether we considered all subjects or just the subjects above the age of 40 (above which vestibular thresholds increase with age). Depending on the exact age cut-off implemented between 37 and 42 years of age, 0.2Hz roll tilt thresholds explained (mediated) between 33% and 55% of the total age-effect on balance. CONCLUSION: Vestibular function may mediate approximately 50% of the widely-reported age-effect on balance. If confirmed by future studies, this may provide an opportunity to improve balance (and presumably reduce fall risk) via specific therapies tailored to improve vestibular function.

The velocity storage time constant: Balancing between accuracy and precision.

The velocity storage mechanism is often described in terms of the exponential decay in eye velocity in an upright subject who experiences a constant velocity yaw rotation after a rapid acceleration. The velocity storage time constant for this decay is roughly 6-30s, which means that for low-frequency head rotations, eye velocity and perceptions have large errors compared to actual motion. One may wonder if there would be benefits to having a longer time constant, which would improve accuracy. In this paper, simulations are used to highlight that improved accuracy may come at the cost of increased noise-i.e., reduced precision. Specifically, since the velocity storage mechanism extends the 5.7s time constant of the semicircular canal, it must be performing an integration process over a certain frequency range. In fact, all mathematical models of velocity storage include an integration. This integration would also integrate neural noise. Thus, increasing the velocity storage time constant would lead to integration over a wider range of frequencies, resulting in more noise in the brain's estimate of motion. Simulation results show this accuracy-precision tradeoff. Recent evidence is also reviewed supporting the hypothesis that the brain optimizes the velocity storage time constant to resolve this accuracy-precision tradeoff during aging and with variations in stimulus amplitude.

Mathematical models for dynamic, multisensory spatial orientation perception.

Mathematical models have been proposed for how the brain interprets sensory information to produce estimates of self-orientation and self-motion. This process, spatial orientation perception, requires dynamically integrating multiple sensory modalities, including visual, vestibular, and somatosensory cues. Here, we review the progress in mathematical modeling of spatial orientation perception, focusing on dynamic multisensory models, and the experimental paradigms in which they have been validated. These models are primarily "black box" or "as if" models for how the brain processes spatial orientation cues. Yet, they have been effective scientifically, in making quantitative hypotheses that can be empirically assessed, and operationally, in investigating aircraft pilot disorientation, for example. The primary family of models considered, the observer model, implements estimation theory approaches, hypothesizing that internal models (i.e., neural systems replicating the behavior/dynamics of physical systems) are used to produce expected sensory measurements. Expected signals are then compared to actual sensory afference, yielding sensory conflict, which is weighted to drive central perceptions of gravity, angular velocity, and translation. This approach effectively predicts a wide range of experimental scenarios using a small set of fixed free parameters. We conclude with limitations and applications of existing mathematical models and important areas of future work.

Human manual control precision depends on vestibular sensory precision and gravitational magnitude.

Precise motion control is critical to human survival on Earth and in space. Motion sensation is inherently imprecise, and the functional implications of this imprecision are not well understood. We studied a "vestibular" manual control task in which subjects attempted to keep themselves upright with a rotational hand controller (i.e., joystick) to null out pseudorandom, roll-tilt motion disturbances of their chair in the dark. Our first objective was to study the relationship between intersubject differences in manual control performance and sensory precision, determined by measuring vestibular perceptual thresholds. Our second objective was to examine the influence of altered gravity on manual control performance. Subjects performed the manual control task while supine during short-radius centrifugation, with roll tilts occurring relative to centripetal accelerations of 0.5, 1.0, and 1.33 GC (1 GC = 9.81 m/s2). Roll-tilt vestibular precision was quantified with roll-tilt vestibular direction-recognition perceptual thresholds, the minimum movement that one can reliably distinguish as leftward vs. rightward. A significant intersubject correlation was found between manual control performance (defined as the standard deviation of chair tilt) and thresholds, consistent with sensory imprecision negatively affecting functional precision. Furthermore, compared with 1.0 GC manual control was more precise in 1.33 GC (-18.3%, P = 0.005) and less precise in 0.5 GC (+39.6%, P < 0.001). The decrement in manual control performance observed in 0.5 GC and in subjects with high thresholds suggests potential risk factors for piloting and locomotion, both on Earth and during human exploration missions to the moon (0.16 G) and Mars (0.38 G). NEW & NOTEWORTHY The functional implications of imprecise motion sensation are not well understood. We found a significant correlation between subjects' vestibular perceptual thresholds and performance in a manual control task (using a joystick to keep their chair upright), consistent with sensory imprecision negatively affecting functional precision. Furthermore, using an altered-gravity centrifuge configuration, we found that manual control precision was improved in "hypergravity" and degraded in "hypogravity." These results have potential relevance for postural control, aviation, and spaceflight.

Human perception of whole body roll-tilt orientation in a hypogravity analog: underestimation and adaptation.

Overestimation of roll tilt in hypergravity ("G-excess" illusion) has been demonstrated, but corresponding sustained hypogravic conditions are impossible to create in ground laboratories. In this article we describe the first systematic experimental evidence that in a hypogravity analog, humans underestimate roll tilt. We studied perception of self-roll tilt in nine subjects, who were supine while spun on a centrifuge to create a hypogravity analog. By varying the centrifuge rotation rate, we modulated the centripetal acceleration (GC) at the subject's head location (0.5 or 1 GC) along the body axis. We measured orientation perception using a subjective visual vertical task in which subjects aligned an illuminated bar with their perceived centripetal acceleration direction during tilts (±11.5-28.5°). As hypothesized, based on the reduced utricular otolith shearing, subjects initially underestimated roll tilts in the 0.5 GC condition compared with the 1 GC condition (mean perceptual gain change = -0.27, P = 0.01). When visual feedback was given after each trial in 0.5 GC, subjects' perceptual gain increased in approximately exponential fashion over time (time constant = 16 tilts or 13 min), and after 45 min, the perceptual gain was not significantly different from the 1 GC baseline (mean gain difference between 1 GC initial and 0.5 GC final = 0.16, P = 0.3). Thus humans modified their interpretation of sensory cues to more correctly report orientation during this hypogravity analog. Quantifying the acute orientation perceptual learning in such an altered gravity environment may have implications for human space exploration on the moon or Mars. NEW & NOTEWORTHY Humans systematically overestimate roll tilt in hypergravity. However, human perception of orientation in hypogravity has not been quantified across a range of tilt angles. Using a centrifuge to create a hypogravity centripetal acceleration environment, we found initial underestimation of roll tilt. Providing static visual feedback, perceptual learning reduced underestimation during the hypogravity analog. These altered gravity orientation perceptual errors and adaptation may have implications for astronauts.

Variability in the Vestibulo-Ocular Reflex and Vestibular Perception.

The vestibular system enables humans to estimate self-motion, stabilize gaze and maintain posture, but these behaviors are impacted by neural noise at all levels of processing (e.g., sensory, central, motor). Despite its essential importance, the behavioral impact of noise in human vestibular pathways is not completely understood. Here, we characterize the vestibular imprecision that results from neural noise by measuring trial-to-trial vestibulo-ocular reflex (VOR) variability and perceptual just-noticeable differences (JNDs) in the same human subjects as a function of stimulus intensity. We used head-centered yaw rotations about an Earth-vertical axis over a broad range of motion velocities (0-65°/s for VOR variability and 3-90°/s peak velocity for JNDs). We found that VOR variability increased from approximately 0.6°/s at a chair velocity of 1°/s to approximately 3°/s at 65°/s; it exhibited a stimulus-independent range below roughly 1°/s. Perceptual imprecision ("sigma") increased from 0.76°/s at 3°/s to 4.7°/s at 90°/s. Using stimuli that manipulated the relationship between velocity, displacement and acceleration, we found that velocity was the salient cue for VOR variability for our motion stimuli. VOR and perceptual imprecision both increased with stimulus intensity and were broadly similar over a range of stimulus velocities, consistent with a common noise source that affects motor and perceptual pathways. This contrasts with differing perceptual and motor stimulus-dependent imprecision in visual studies. Either stimulus-dependent noise or non-linear signal processing could explain our results, but we argue that afferent non-linearities alone are unlikely to be the source of the observed behavioral stimulus-dependent imprecision.

Perception of threshold-level whole-body motion during mechanical mastoid vibration.

BACKGROUND: Vibration applied on the mastoid has been shown to be an excitatory stimulus to the vestibular receptors, but its effect on vestibular perception is unknown. OBJECTIVE: Determine whether mastoid vibration affects yaw rotation perception using a self-motion perceptual direction-recognition task. METHODS: We used continuous, bilateral, mechanical mastoid vibration using a stimulus with frequency content between 1 and 500 Hz. Vestibular perception of 10 healthy adults (M±S.D. = 34.3±12 years old) was tested with and without vibration. Subjects repeatedly reported the perceived direction of threshold-level yaw rotations administered at 1 Hz by a motorized platform. A cumulative Gaussian distribution function was fit to subjects' responses, which was described by two parameters: bias and threshold. Bias was defined as the mean of the Gaussian distribution, and equal to the motion perceived on average when exposed to null stimuli. Threshold was defined as the standard deviation of the distribution and corresponded to the stimulus the subject could reliably perceive. RESULTS: The results show that mastoid vibration may reduce bias, although two statistical tests yield different conclusions. There was no evidence that yaw rotation thresholds were affected. CONCLUSIONS: Bilateral mastoid vibration may reduce left-right asymmetry in motion perception.

Bayesian optimal adaptation explains age-related human sensorimotor changes.

The brain uses information from different sensory systems to guide motor behavior, and aging is associated with simultaneous decline in the quality of sensory information provided to the brain and deterioration in motor control. Correlations between age-dependent decline in sensory anatomical structures and behavior have been demonstrated in many sensorimotor systems, and it has recently been suggested that a Bayesian framework could explain these relationships. Here we show that age-dependent changes in a human sensorimotor reflex, the vestibuloocular reflex, are explained by a Bayesian optimal adaptation in the brain occurring in response to death of motion-sensing hair cells. Specifically, we found that the temporal dynamics of the reflex as a function of age emerge from ( r = 0.93, P < 0.001) a Kalman filter model that determines the optimal behavioral output when the sensory signal-to-noise characteristics are degraded by death of the transducers. These findings demonstrate that the aging brain is capable of generating the ideal and statistically optimal behavioral response when provided with deteriorating sensory information. While the Bayesian framework has been shown to be a general neural principle for multimodal sensory integration and dynamic sensory estimation, these findings provide evidence of longitudinal Bayesian processing over the human life span. These results illuminate how the aging brain strives to optimize motor behavior when faced with deterioration in the peripheral and central nervous systems and have implications in the field of vestibular and balance disorders, as they will likely provide guidance for physical therapy and for prosthetic aids that aim to reduce falls in the elderly. NEW & NOTEWORTHY We showed that age-dependent changes in the vestibuloocular reflex are explained by a Bayesian optimal adaptation in the brain that occurs in response to age-dependent sensory anatomical changes. This demonstrates that the brain can longitudinally respond to age-related sensory loss in an ideal and statistically optimal way. This has implications for understanding and treating vestibular disorders caused by aging and provides insight into the structure-function relationship during aging.