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Gravity dependence of the effect of optokinetic stimulation on the subject visual vertical


Ward, Bryan K; Bockisch, Christopher J; Caramia, Nicoletta; Bertolini, Giovanni; Tarnutzer, Alexander Andrea (2017). Gravity dependence of the effect of optokinetic stimulation on the subject visual vertical. Journal of Neurophysiology:jn.00303.2016.

Abstract

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 extra-vestibular (visual/proprioceptive) sensors are roll-angle dependent and predicted an increased weight of extra-vestibular 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 towards 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 non-significant increase when providing optokinetic stimulation. Variability and optokinetic bias were correlated (R(2)=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 non-significant- is true, either it must depend on an additional source of variability, added after SVV-computation, or it would conflict with the Bayesian hypothesis.

Abstract

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 extra-vestibular (visual/proprioceptive) sensors are roll-angle dependent and predicted an increased weight of extra-vestibular 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 towards 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 non-significant increase when providing optokinetic stimulation. Variability and optokinetic bias were correlated (R(2)=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 non-significant- is true, either it must depend on an additional source of variability, added after SVV-computation, or it would conflict with the Bayesian hypothesis.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > University Hospital Zurich > Ophthalmology Clinic
04 Faculty of Medicine > University Hospital Zurich > Clinic for Neurology
04 Faculty of Medicine > University Hospital Zurich > Clinic for Otorhinolaryngology
Dewey Decimal Classification:610 Medicine & health
Scopus Subject Areas:Life Sciences > General Neuroscience
Life Sciences > Physiology
Language:English
Date:1 February 2017
Deposited On:02 Mar 2017 13:33
Last Modified:26 Jan 2022 12:36
Publisher:American Physiological Society
ISSN:0022-3077
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1152/jn.00303.2016
PubMed ID:28148642
  • Content: Accepted Version