Ward Bryan K, Bockisch Christopher J, Caramia Nicoletta, Bertolini Giovanni, Tarnutzer Alexander Andrea
Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins School of Medicine, Baltimore, Maryland.
Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland.
J Neurophysiol. 2017 May 1;117(5):1948-1958. doi: 10.1152/jn.00303.2016. Epub 2017 Feb 1.
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°, = 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° ( < 0.005). Offsets grew from 3.9 ± 1.8° (upright) to 22.1 ± 11.8° (±120° roll tilt, < 0.001). Trial-to-trial variability increased with roll angle, demonstrating a nonsignificant increase when providing optokinetic stimulation. Variability and optokinetic bias were correlated ( = 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. 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.
准确精确地估计重力方向对于空间定向至关重要。根据贝叶斯理论，多感觉前庭、视觉和本体感觉输入会基于各组成感觉信号的可靠性以加权方式在中枢进行整合。对于耳石输入，随着侧倾角度增加，信噪比呈下降趋势。我们假设前庭（耳石）和前庭外（视觉/本体感觉）传感器的权重依赖于侧倾角度，并预测随着侧倾角度增加，前庭外线索的权重会增加，这可能符合贝叶斯假设。为了探究这一概念，在不同侧倾位置（≤±120°，步长 = 30°， = 10）下，在有/无呈现视动刺激（速度 = ±60°/秒）的情况下评估主观视觉垂直线（SVV）。视动刺激使侧倾角度≥±30°时的SVV偏向刺激旋转方向（<0.005）。偏移量从直立时的3.9±1.8°增加到±120°侧倾倾斜时的22.1±11.8°（<0.001）。逐次试验的变异性随侧倾角度增加，在提供视动刺激时显示出不显著的增加。变异性和视动偏差具有相关性（ = 0.71，斜率 = 0.71，95%置信区间 = 0.57 - 0.86）。一个将视动偏差与前庭输入相结合的最优观察者模型能紧密再现测量误差。这些发现支持了在通过视动刺激估计重力方向时进行加权多感觉整合的假设。当前庭输入变得不太可靠时，即侧倾倾斜角度较大时，视觉输入的权重更大。然而，根据贝叶斯理论，组合线索的变异性总是低于每个源线索的变异性。如果观察到的变异性增加（尽管不显著）是真实的，那么要么它必须依赖于SVV计算后添加的额外变异性来源，要么就会与贝叶斯假设相冲突。在记录不同全身侧倾角度下的主观视觉垂直线时应用旋转视动刺激，我们注意到视动诱导的偏差与侧倾角度相关。这些发现支持这样一种假设，即根据单感觉线索的可靠性来估计重力方向时所确立的最优加权可以扩展到由视觉自我运动刺激引起的偏差。
