Perception of angular displacement without landmarks: evidence for Bayesian fusion of vestibular, optokinetic, podokinesthetic, and cognitive information.
The perception of angular displacement during self turning is generally based on a combination of redundant signals from different sources. For example, during active turning in a visually structured environment devoid of landmarks, podokinesthetic, vestibular, and optokinetic velocity signals are fused and integrated over time to yield a unitary percept of the ongoing change in angular position ('podokinesthetic' refers to proprioceptive and corollary signals related to leg and foot movement). Previously we have shown that the fusion of two of these afferents improves perceptual accuracy and reliability in comparison to when only one is available. For example, with only a single modality available, slow rotations are perceived to be significantly larger than fast ones, whereas the combination of two modalities greatly reduces this difference. These observations spurred the hypothesis that displacement perception results from a weighted average of bottom-up (sensory) signals and top-down signals (a priori knowledge or expectation), with the weight of the latter decreasing the more sensory information is available. We now ask (1) whether the accuracy of angular displacement estimation can be further improved if it can draw on all three sensory modalities instead of only two, and (2) whether bottom-up sensory and top-down a priori information is combined for displacement estimation in a statistically optimal way. To this end 12 healthy subjects (Ss) standing on a turning platform surrounded by a rotatable optokinetic pattern were exposed to 6 different sensory conditions: pure podokinesthetic (P), vestibular (V), or optokinetic (O) stimulation, and combined podokinesthetic-vestibular (PV), vestibular-optokinetic (VO), or podokinesthetic-vestibular-optokinetic (PVO) stimulation. Stimuli had constant angular velocities of either 15, 30, or 60 degrees /s. Subjects were to press a signal button when they felt that angular displacement had reached a previously instructed magnitude (150-900 degrees ). In agreement with earlier observations, the combination of two sensory signals improved the accuracy of displacement perception by reducing both the variance of subjects' displacement estimates and their dependence on turning velocity. Adding a third sensory signal (condition PVO) led to a further reduction of variance and almost eliminated the effect of velocity. We show that these experimental results are compatible with a probabilistic fusion mechanism based on Bayes' law. This mechanism would operate on logarithmic representations of turning velocity and proceed in two stages. A first stage fuses all available bottom-up information to create a unitary representation of the velocity signalled by the different sensory modalities. A second stage then fuses this sensory information with top-down a priori information; the latter creates a bias in favour of a 'default velocity' that grows as the uncertainty of the sensory information increases. Our experimental data agree with the relation between (1) the variance of displacement estimates and (2) their modulation by velocity predicted by this scheme.
Jürgens
Reinhart
R
Sektion Neurophysiologie, Universität Ulm, Albert-Einstein-Allee 47, 89081 Ulm, Germany.
Becker
Wolfgang
W
D000293:Adolescent; D000328:Adult; D000704:Analysis of Variance; D001499:Bayes Theorem; D003071:Cognition / Q000502:physiology*; D005260:Female; D006801:Humans; D008297:Male; D010465:Perception / Q000502:physiology*; D004856:Postural Balance / Q000502:physiology*; D011434:Proprioception / Q000502:physiology*; D011597:Psychomotor Performance / Q000502:physiology; D012027:Reflex, Vestibulo-Ocular / Q000502:physiology*; D012399:Rotation; D014724:Vestibular Function Tests; D014722:Vestibule, Labyrinth / Q000502:physiology