Multisensory Processing in Spatial Orientation: An Inverse Probabilistic Approach

Abstract

Most evidence that the brain uses Bayesian inference to integrate noisy sensory signals optimally has been obtained by showing that the noise levels in each modality separately can predict performance in combined conditions. Such a forward approach is difficult to implement when the various signals cannot be measured in isolation, as in spatial orientation, which involves the processing of visual, somatosensory, and vestibular cues. Instead, we applied an inverse probabilistic approach, based on optimal observer theory. Our goal was to investigate whether the perceptual differences found when probing two different states-body-in-space and head-in-space orientation-can be reconciled by a shared scheme using all available sensory signals. Using a psychometric approach, seven human subjects were tested on two orientation estimates at tilts Ͻ120°: perception of body tilt [subjective body tilt (SBT)] and perception of visual vertical [subjective visual vertical (SVV)]. In all subjects, the SBT was more accurate than the SVV, which showed substantial systematic errors for tilt angles beyond 60°. Variability increased with tilt angle in both tasks, but was consistently lower in the SVV. The sensory integration model fitted both datasets very nicely. A further experiment, in which supine subjects judged their head orientation relative to the body, independently confirmed the predicted head-on-body noise by the model. Model predictions based on the derived noise properties from the various modalities were also consistent with previously published deficits in vestibular and somatosensory patients. We conclude that Bayesian computations can account for the typical differences in spatial orientation judgments associated with different task requirements.

Vestibular benefits to task savings in motor adaptation

“…We cannot dissociate their contribution from the vestibular contribution to retention (Clemens et al 2011). In contrast, it is unlikely that proprioceptive signals have cued the opposing force environments.…”

Egocentric and allocentric alignment tasks are affected by otolith input

“…With increasing head roll, trial-to-trial SVV variability increases (De Vrijer et al 2008;Kaptein and Van Gisbergen 2005;Lechner-Steinleitner 1978;Mittelstaedt 1983;Schoene and Udo de Haes 1971;Tarnutzer et al 2009b;Udo de Haes 1970). This modulation of SVV variability was successfully reproduced using an otolith model estimating the gravitational vertical based on the characteristics (e.g., firing rate, orientation of polarization vectors) of a group of utricular and saccular otolith afferents and a prior biasing errors toward the body-longitudinal axis (Clemens et al 2011;De Vrijer et al 2009;MacNeilage et al 2007;Tarnutzer et al 2009b).…”

Visual and vestibular perceptual thresholds each demonstrate better precision at specific frequencies and also exhibit optimal integration

“…Bayesian integration for static roll orientation has been demonstrated (Clemens et al 2011;De Vrijer et al 2009), and perceptual visual-vestibular interaction has been studied in roll tilt (e.g., Dichgans et al 1972;Zacharias and Young 1981), but this is the first experimental study to examine optimal integration using thresholds determined with dynamic roll tilt stimuli.…”

“…Previous threshold studies have reported static Bayesian optimal cue integration for rotation (Jurgens and Becker 2006), translation (Butler et al 2010;Fetsch et al 2009Fetsch et al , 2010Fetsch et al , 2012Gu et al 2008), and static roll orientation (Clemens et al 2011;De Vrijer et al 2009) but visual-vestibular cue integration using thresholds and dynamic tilt has not been reported. Furthermore, unlike the earlier studies that degraded visual cues (Butler et al 2010;Fetsch et al 2009Fetsch et al , 2012Gu et al 2008) or put two sensory cues in conflict (Butler et al 2010;Fetsch et al 2009Fetsch et al , 2012; Jurgens and Becker 2006), we used natural cue combinations.…”