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

Sergio Delle Monache,Francesco Lacquaniti,Iole Indovina,Myrka Zago,Elena Daprati,Gianfranco Bosco

doi:10.3389/fnint.2021.793634

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.

Highlights

Gravity represents a physical invariant of the Earth environment to which all species, including ours, have adapted through evolution
A clear exemplification of such adaptation is represented by the lack of conscious effort with which gravity effects are taken into account when controlling most motor behaviors, ranging from the seemingly simple task of maintaining balance during gait to the complex motor skills performed by professional athletes, acrobats, and ballet dancers
It is worth noting that this result has been obtained by collapsing data for the direction of motion regardless of the kinematics, more controlled studies are needed to disentangle whether this decrease in the activity of the right insula shown by PPPD patients is related to the internal representation of gravity, for example by combining neuroimaging and psychophysical approaches in these patients in order to measure both interception and fMRI responses to visual motion either coherent or incoherent with gravity effects

Summary

INTRODUCTION

Gravity represents a physical invariant of the Earth environment to which all species, including ours, have adapted through evolution. Practice with the task led to the incorporation of information about head and body orientation relative to gravity for response timing Such information could have been extracted by combining signals from at least two sources: (1) the background activity and dynamic sensitivity of otolith regular afferents, which are related to the component of the gravitational shear force acting in the plane of the maculae, changed by the static head tilt; and (2) signals from somatosensory (cutaneous, muscle, and tendon) and visceral receptors (in the kidneys, vena cava), which monitor contact forces between the body and the environment, thereby contributing a sense of body orientation. Vestibular stimulation resulting from increases of the gravito-inertial force (up to 1.4 g) with a short-radius centrifuge disrupts the time course of representational gravity, that is, the phenomenon in which the remembered vanishing location of a moving target is displaced downward in the direction of gravity, and more so with increasing retention intervals (De Sá Teixeira et al, 2017)

A NEURAL REPRESENTATION OF “VISUAL” GRAVITY IN THE VESTIBULAR CORTEX

CONCLUDING REMARKS