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

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 da...

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Autores principales: Delle Monache, Sergio, Indovina, Iole, Zago, Myrka, Daprati, Elena, Lacquaniti, Francesco, Bosco, Gianfranco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8671301/
https://www.ncbi.nlm.nih.gov/pubmed/34924968
http://dx.doi.org/10.3389/fnint.2021.793634
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author Delle Monache, Sergio
Indovina, Iole
Zago, Myrka
Daprati, Elena
Lacquaniti, Francesco
Bosco, Gianfranco
author_facet Delle Monache, Sergio
Indovina, Iole
Zago, Myrka
Daprati, Elena
Lacquaniti, Francesco
Bosco, Gianfranco
author_sort Delle Monache, Sergio
collection PubMed
description 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.
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spelling pubmed-86713012021-12-16 Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity Delle Monache, Sergio Indovina, Iole Zago, Myrka Daprati, Elena Lacquaniti, Francesco Bosco, Gianfranco Front Integr Neurosci Neuroscience 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. Frontiers Media S.A. 2021-12-01 /pmc/articles/PMC8671301/ /pubmed/34924968 http://dx.doi.org/10.3389/fnint.2021.793634 Text en Copyright © 2021 Delle Monache, Indovina, Zago, Daprati, Lacquaniti and Bosco. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Delle Monache, Sergio
Indovina, Iole
Zago, Myrka
Daprati, Elena
Lacquaniti, Francesco
Bosco, Gianfranco
Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity
title Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity
title_full Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity
title_fullStr Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity
title_full_unstemmed Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity
title_short Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity
title_sort watching the effects of gravity. vestibular cortex and the neural representation of “visual” gravity
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8671301/
https://www.ncbi.nlm.nih.gov/pubmed/34924968
http://dx.doi.org/10.3389/fnint.2021.793634
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