Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity

Abstract

Gravity is a physical constraint all terrestrial species have adapted to through evolution. Indeed, gravity effects are taken into account in many forms of interaction with the environment, from the seemingly simple task of maintaining balance to the complex motor skills performed by athletes and dancers. Graviceptors, primarily located in the vestibular otolith organs, feed the Central Nervous System with information related to the gravity acceleration vector. This information is integrated with signals from semicircular canals, vision, and proprioception in an ensemble of interconnected brain areas, including the vestibular nuclei, cerebellum, thalamus, insula, retroinsula, parietal operculum, and temporo-parietal junction, in the so-called vestibular network. Classical views consider this stage of multisensory integration as instrumental to sort out conflicting and/or ambiguous information from the incoming sensory signals. However, there is compelling evidence that it also contributes to an internal representation of gravity effects based on prior experience with the environment. This a priori knowledge could be engaged by various types of information, including sensory signals like the visual ones, which lack a direct correspondence with physical gravity. Indeed, the retinal accelerations elicited by gravitational motion in a visual scene are not invariant, but scale with viewing distance. Moreover, the “visual” gravity vector may not be aligned with physical gravity, as when we watch a scene on a tilted monitor or in weightlessness. This review will discuss experimental evidence from behavioral, neuroimaging (connectomics, fMRI, TMS), and patients’ studies, supporting the idea that the internal model estimating the effects of gravity on visual objects is constructed by transforming the vestibular estimates of physical gravity, which are computed in the brainstem and cerebellum, into internalized estimates of virtual gravity, stored in the vestibular cortex. The integration of the internal model of gravity with visual and non-visual signals would take place at multiple levels in the cortex and might involve recurrent connections between early visual areas engaged in the analysis of spatio-temporal features of the visual stimuli and higher visual areas in temporo-parietal-insular regions.

Rhythmic tapping to a moving beat: motion kinematics overrules motion naturalness

“…In addition, the degree of congruency between the visual motion and the motor response can influence rhythm synchronization, as tapping movements aligned with the direction of the visual motion accomplish better synchronization than when the tapping and visual motion direction are incongruent (Hove et al, 2010). These findings are in line with the notion that gravitational cues can facilitate some perceptual functions, like interpreting the causality and the naturalness of object motion or discriminating pendular motion (Pittenger, 1990; Kim and Spelke, 1992; Bingham et al, 1995; Twardy and Bingham, 2002), and can lead to an advantage in manual interceptions, by engaging an internal representation of gravity in the vestibular cortex (Indovina et al, 2005; Lacquaniti et al, 2013; Delle Monache et al, 2021). Interestingly, this internal representation of gravity can be engaged even by the mere object kinematics displayed on a computer screen, especially over a pictorial background providing scaling cues to real world metrics (Moscatelli and Lacquaniti, 2011; La Scaleia et al, 2015; Delle Monache et al, 2017, 2019; Ceccarelli et al, 2018).…”

“…The present study was designed to test whether physically realistic motion trajectories with downward-acceleration or upward-deceleration profiles induced better rhythm entraining in the SCT than the non-naturalistic upward-acceleration/downward-deceleration or accelerating/decelerating horizontal motion metronomes. In effect, a natural gravity gain on rhythmic timing might be expected based on the evidence that diving gannets use gravitational signals to compute the time-to-contact and fold their wings before entering the water (Lee and Reddish, 1981), and that humans can use an internal representation of gravity effects residing in the vestibular cortex to time accurately the interception of vertically falling objects (Lacquaniti and Maioli, 1989; Indovina et al, 2005; Lacquaniti et al, 2015; Delle Monache et al, 2021). However, our findings were not congruent with this expectation, since the timing accuracy, precision, and the correlation of consecutively produced intervals were not different between the natural and non-natural gravity vertical motion nor with horizontal motion.…”

The human posterior cingulate, retrosplenial, and medial parietal cortex effective connectome, and implications for memory and navigation

“…This Group 3 part of the PCC may also provide a route for vestibular and optic flow information useful in navigation to reach hippocampal whole body motion neurons, for it receives inputs from VIP and V6A in which optic flow is represented (Delle Monache et al, 2021 ; Duhamel et al, 1997 ; Sherrill et al, 2015 ).…”

Brain potential responses involved in decision-making in weightlessness

“…The fact that the cerebellar contribution to the P300 was mainly observed when the docking task was performed on Earth and not when the same task was realized in weightlessness might be explained by the major contribution of the cerebellum to the body control during the free-floating posture adopted by the astronaut during the realization of the docking task (Cebolla et al 5 ). On Earth, the cerebellum integrates the semicircular and otolith signals, providing a neural representation of the head orientation relative to gravity 38 – 40 . Because the decision to dock necessitates perceptual stability, the dynamic prediction of the sensory consequences of gravity realized by the internal model of the cerebellum is crucial.…”