Effect of head roll‐tilt on the subjective visual vertical in healthy participants: Towards better clinical measurement of gravity perception

Accurate and precise estimates of direction of gravity are essential for spatial orientation. According to Bayesian theory, multisensory vestibular, visual, and proprioceptive input is centrally integrated in a weighted fashion based on the reliability of the component sensory signals. For otolithic input, a decreasing signal-to-noise ratio was demonstrated with increasing roll angle. We hypothesized that the weights of vestibular (otolithic) and extravestibular (visual/proprioceptive) sensors are roll-angle dependent and predicted an increased weight of extravestibular cues with increasing roll angle, potentially following the Bayesian hypothesis. To probe this concept, the subjective visual vertical (SVV) was assessed in different roll positions (≤ ± 120°, steps = 30°, n = 10) with/without presenting an optokinetic stimulus (velocity = ± 60°/s). The optokinetic stimulus biased the SVV toward the direction of stimulus rotation for roll angles ≥ ± 30° ( P < 0.005). Offsets grew from 3.9 ± 1.8° (upright) to 22.1 ± 11.8° (±120° roll tilt, P < 0.001). Trial-to-trial variability increased with roll angle, demonstrating a nonsignificant increase when providing optokinetic stimulation. Variability and optokinetic bias were correlated ( R2 = 0.71, slope = 0.71, 95% confidence interval = 0.57–0.86). An optimal-observer model combining an optokinetic bias with vestibular input reproduced measured errors closely. These findings support the hypothesis of a weighted multisensory integration when estimating direction of gravity with optokinetic stimulation. Visual input was weighted more when vestibular input became less reliable, i.e., at larger roll-tilt angles. However, according to Bayesian theory, the variability of combined cues is always lower than the variability of each source cue. If the observed increase in variability, although nonsignificant, is true, either it must depend on an additional source of variability, added after SVV computation, or it would conflict with the Bayesian hypothesis. NEW & NOTEWORTHY Applying a rotating optokinetic stimulus while recording the subjective visual vertical in different whole body roll angles, we noted the optokinetic-induced bias to correlate with the roll angle. These findings allow the hypothesis that the established optimal weighting of single-sensory cues depending on their reliability to estimate direction of gravity could be extended to a bias caused by visual self-motion stimuli.

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Development of a Clinical Examination to Evaluate Gravity Perception during Static Head Roll Tilt

Nippon Jibiinkoka Gakkai Kaiho ◽

10.3950/jibiinkoka.119.1201 ◽

2016 ◽

Vol 119 (9) ◽

pp. 1201-1209

Author(s):

Yoshiro Wada ◽

Toshiaki Yamanaka ◽

Tadashi Kitahara ◽

Junichi Kurata

Keyword(s):

Clinical Examination ◽

Gravity Perception ◽

Head Roll ◽

Static Head ◽

Roll Tilt

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Body-Tilt and Visual Verticality Perception During Multiple Cycles of Roll Rotation

Journal of Neurophysiology ◽

10.1152/jn.00704.2007 ◽

2008 ◽

Vol 99 (5) ◽

pp. 2264-2280 ◽

Cited By ~ 23

Author(s):

R.A.A. Vingerhoets ◽

W. P. Medendorp ◽

J.A.M. Van Gisbergen

Keyword(s):

Constant Velocity ◽

Interaction Model ◽

The Body ◽

Body Tilt ◽

Subjective Visual Vertical ◽

Egocentric Bias ◽

Leaky Integrator ◽

Visual Vertical ◽

Multiple Cycles ◽

Roll Tilt

To assess the effects of degrading canal cues for dynamic spatial orientation in human observers, we tested how judgments about visual-line orientation in space (subjective visual vertical task, SVV) and estimates of instantaneous body tilt (subjective body-tilt task, SBT) develop in the course of three cycles of constant-velocity roll rotation. These abilities were tested across the entire tilt range in separate experiments. For comparison, we also obtained SVV data during static roll tilt. We found that as tilt increased, dynamic SVV responses became strongly biased toward the head pole of the body axis (A-effect), as if body tilt was underestimated. However, on entering the range of near-inverse tilts, SVV responses adopted a bimodal pattern, alternating between A-effects (biased toward head-pole) and E-effects (biased toward feet-pole). Apart from an onset effect, this tilt-dependent pattern of systematic SVV errors repeated itself in subsequent rotation cycles with little sign of worsening performance. Static SVV responses were qualitatively similar and consistent with previous reports but showed smaller A-effects. By contrast, dynamic SBT errors were small and unimodal, indicating that errors in visual-verticality estimates were not caused by errors in body-tilt estimation. We discuss these results in terms of predictions from a canal-otolith interaction model extended with a leaky integrator and an egocentric bias mechanism. We conclude that the egocentric-bias mechanism becomes more manifest during constant velocity roll-rotation and that perceptual errors due to incorrect disambiguation of the otolith signal are small despite the decay of canal signals.

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Pupil responses associated with the perception of gravitational vertical under directional optic flows

Scientific Reports ◽

10.1038/s41598-021-00346-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Joo Hyun Park ◽

Sung Ik Cho ◽

June Choi ◽

JungHyun Han ◽

Yoon Chan Rah

Keyword(s):

Fine Tuning ◽

Gravity Perception ◽

Cognitive Demands ◽

Head Mounted Display ◽

Rotational Flows ◽

Visual Vertical ◽

Optic Flows ◽

The Difference ◽

Gravitational Vertical ◽

Healthy Participants

AbstractThis study assessed the pupil responses in the sensory integration of various directional optic flows during the perception of gravitational vertical. A total of 30 healthy participants were enrolled with normal responses to conventional subjective visual vertical (SVV) which was determined by measuring the difference (error angles) between the luminous line adjusted by the participants and the true vertical. SVV was performed under various types of rotational (5°/s, 10°/s, and 50°/s) and straight (5°/s and 10°/s) optic flows presented via a head-mounted display. Error angles (°) of the SVV and changes in pupil diameters (mm) were measured to evaluate the changes in the visually assessed subjective verticality and related cognitive demands. Significantly larger error angles were measured under rotational optic flows than under straight flows (p < 0.001). The error angles also significantly increased as the velocity of the rotational optic flow increased. The pupil diameter increased after starting the test, demonstrating the largest diameter during the final fine-tuning around the vertical. Significantly larger pupil changes were identified under rotational flows than in straight flows. Pupil changes were significantly correlated with error angles and the visual analog scale representing subjective difficulties during each test. These results suggest increased pupil changes for integrating more challenging visual sensory inputs in the process of gravity perception.

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Gravity Dependence of Subjective Visual Vertical Variability

Journal of Neurophysiology ◽

10.1152/jn.00007.2008 ◽

2009 ◽

Vol 102 (3) ◽

pp. 1657-1671 ◽

Cited By ~ 68

Author(s):

A. A. Tarnutzer ◽

C. Bockisch ◽

D. Straumann ◽

I. Olasagasti

Keyword(s):

Inertial Force ◽

Semicircular Canals ◽

The Body ◽

Otolith Organs ◽

Subjective Visual Vertical ◽

Visual Vertical ◽

Head Roll ◽

Static Head ◽

Experimental Findings ◽

Vertical Variability

The brain integrates sensory input from the otolith organs, the semicircular canals, and the somatosensory and visual systems to determine self-orientation relative to gravity. Only the otoliths directly sense the gravito-inertial force vector and therefore provide the major input for perceiving static head-roll relative to gravity, as measured by the subjective visual vertical (SVV). Intraindividual SVV variability increases with head roll, which suggests that the effectiveness of the otolith signal is roll-angle dependent. We asked whether SVV variability reflects the spatial distribution of the otolithic sensors and the otolith-derived acceleration estimate. Subjects were placed in different roll orientations (0–360°, 15° steps) and asked to align an arrow with perceived vertical. Variability was minimal in upright, increased with head-roll peaking around 120–135°, and decreased to intermediate values at 180°. Otolith-dependent variability was modeled by taking into consideration the nonuniform distribution of the otolith afferents and their nonlinear firing rate. The otolith-derived estimate was combined with an internal bias shifting the estimated gravity-vector toward the body-longitudinal. Assuming an efficient otolith estimator at all roll angles, peak variability of the model matched our data; however, modeled variability in upside-down and upright positions was very similar, which is at odds with our findings. By decreasing the effectiveness of the otolith estimator with increasing roll, simulated variability matched our experimental findings better. We suggest that modulations of SVV precision in the roll plane are related to the properties of the otolith sensors and to central computational mechanisms that are not optimally tuned for roll-angles distant from upright.

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Static roll-tilt over 5 minutes locally distorts the internal estimate of direction of gravity

Journal of Neurophysiology ◽

10.1152/jn.00540.2014 ◽

2014 ◽

Vol 112 (11) ◽

pp. 2672-2679 ◽

Cited By ~ 6

Author(s):

A. A. Tarnutzer ◽

C. J. Bockisch ◽

D. Straumann ◽

S. Marti ◽

G. Bertolini

Keyword(s):

Human Subjects ◽

Healthy Human ◽

Healthy Human Subjects ◽

Short Term Adaptation ◽

Body Roll ◽

Visual Vertical ◽

Head Roll ◽

Global Bias ◽

Mixture Of Gaussian ◽

Roll Tilt

The subjective visual vertical (SVV) indicates perceived direction of gravity. Even in healthy human subjects, roll angle-dependent misestimations, roll overcompensation (A-effect, head-roll > 60° and <135°) and undercompensation (E-effect, head-roll < 60°), occur. Previously, we demonstrated that, after prolonged roll-tilt, SVV estimates when upright are biased toward the preceding roll position, which indicates that perceived vertical (PV) is shifted by the prior tilt (Tarnutzer AA, Bertolini G, Bockisch CJ, Straumann D, Marti S. PLoS One 8: e78079, 2013). Hypothetically, PV in any roll position could be biased toward the previous roll position. We asked whether such a “global” bias occurs or whether the bias is “local”. The SVV of healthy human subjects ( N = 9) was measured in nine roll positions (−120° to +120°, steps = 30°) after 5 min of roll-tilt in one of two adaptation positions (±90°) and compared with control trials without adaptation. After adapting, adjustments were shifted significantly ( P < 0.05) toward the previous adaptation position for nearby roll-tilted positions (±30°, ±60°) and upright only. We computationally simulated errors based on the sum of a monotonically increasing function (producing roll undercompensation) and a mixture of Gaussian functions (representing roll overcompensation centered around PV). In combination, the pattern of A- and E-effects could be generated. By shifting the function representing local overcompensation toward the adaptation position, the experimental postadaptation data could be fitted successfully. We conclude that prolonged roll-tilt locally distorts PV rather than globally shifting it. Short-term adaptation of roll overcompensation may explain these shifts and could reflect the brain's strategy to optimize SVV estimates around recent roll positions. Thus postural stability can be improved by visually-mediated compensatory responses at any sustained body-roll orientation.

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