Vestibular Nuclei and Cerebellum Put Visual Gravitational Motion in Context

Abstract

Animal survival in the forest, and human success on the sports field, often depend on the ability to seize a target on the fly. All bodies fall at the same rate in the gravitational field, but the corresponding retinal motion varies with apparent viewing distance. How then does the brain predict time-to-collision under gravity? A perspective context from natural or pictorial settings might afford accurate predictions of gravity's effects via the recovery of an environmental reference from the scene structure. We report that embedding motion in a pictorial scene facilitates interception of gravitational acceleration over unnatural acceleration, whereas a blank scene eliminates such bias. Functional magnetic resonance imaging (fMRI) revealed blood-oxygen-level-dependent correlates of these visual context effects on gravitational motion processing in the vestibular nuclei and posterior cerebellar vermis. Our results suggest an early stage of integration of high-level visual analysis with gravity-related motion information, which may represent the substrate for perceptual constancy of ubiquitous gravitational motion.

Anticipating the effects of visual gravity during simulated self-motion: estimates of time-to-passage along vertical and horizontal paths

“…As a consequence, this classical model predicts that the duration of constant speed motions should be estimated correctly while it should be overestimated for accelerated and underestimated for decelerated motions. Previous studies were consistent in finding underestimation of decelerated motion indicating the use of first-order (velocity) information for this motion law (self-motion: Capelli et al 2010;Kaiser and Hecht 1995;object motion: Maffei et al 2010;Miller et al 2008;Schlack et al 2008;Indovina et al 2005;Port et al 1997). On the contrary, anticipated responses during accelerated motions and delayed responses during decelerated motions found in the current study suggest that participants used second-order information in the Visible protocol.…”

“…This time shift indicates an influence of the orientation relative to visual gravity on response timing that could be attributed to the anticipation of the effects of visual gravity on self-motion along the vertical, but not the horizontal orientation. Finally, precision in TTP estimates was higher during vertical fall than when traveling at constant speed along the vertical orientation, consistent 1 3 network of areas including the posterior-insula and the temporo-parietal junction (Indovina et al 2013, Maffei et al 2010Miller et al 2008;Bosco et al 2008).…”

“…On the other hand, studies on interception of moving objects and on estimates of time intervals showed that a priori knowledge about gravitational acceleration, combined with realistic cues about the orientation and size of the visual scene, can influence response timing (Moscatelli and Lacquaniti 2011;Zago et al 2009;Miller et al 2008;Bosco et al 2008;Senot et al 2005;McIntyre et al 2001). This a priori knowledge is thought to be stored in a visual-vestibular Abstract By simulating self-motion on a virtual rollercoaster, we investigated whether acceleration cued by the optic flow affected the estimate of time-to-passage (TTP) to a target.…”

Contributions of the Human Temporoparietal Junction and MT/V5+ to the Timing of Interception Revealed by Transcranial Magnetic Stimulation

“…fMRI studies showed activation of hMT/V5ϩ during buttonpress interception of targets accelerated downward by gravity or decelerated downward by reversed gravity (Indovina et al, 2005;Miller et al, 2008). Instead, TPJ regions were activated preferentially by downward accelerating targets, suggesting a specialization for visual gravitational motion.…”

“…In primates, several brain regions contribute the necessary visual and motor information (Merchant et al, 2004;Indovina et al, 2005;Miller et al, 2008;Senot et al, 2008). Recordings in monkey motor cortex and area 7a showed firing patterns timed to either the target or the hand movement (Port et al, 2001;Merchant et al, 2004).…”