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

Bryan K. Ward, Christopher J. Bockisch, Nicoletta Caramia, Giovanni Bertolini, Alexander Andrea Tarnutzer

Research output: Contribution to journalArticlepeer-review

Abstract

Ac-curate 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/proprio-ceptive) 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.

Original languageEnglish (US)
Pages (from-to)1948-1958
Number of pages11
JournalJournal of neurophysiology
Volume117
Issue number5
DOIs
StatePublished - May 2017

Keywords

  • Bayesian hypothesis
  • Multisensory integration
  • Optokinetic
  • Perception
  • Subjective visual vertical

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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