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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-12-01
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| Series: | Frontiers in Integrative Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnint.2021.793634/full |
| _version_ | 1818422890855399424 |
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| author | Sergio Delle Monache Sergio Delle Monache Iole Indovina Iole Indovina Myrka Zago Myrka Zago Myrka Zago Elena Daprati Elena Daprati Elena Daprati Francesco Lacquaniti Francesco Lacquaniti Francesco Lacquaniti Gianfranco Bosco Gianfranco Bosco Gianfranco Bosco |
| author_facet | Sergio Delle Monache Sergio Delle Monache Iole Indovina Iole Indovina Myrka Zago Myrka Zago Myrka Zago Elena Daprati Elena Daprati Elena Daprati Francesco Lacquaniti Francesco Lacquaniti Francesco Lacquaniti Gianfranco Bosco Gianfranco Bosco Gianfranco Bosco |
| author_sort | Sergio Delle Monache |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T13:33:27Z |
| format | Article |
| id | doaj.art-9339787282a54b2fa11109987b75c99b |
| institution | Directory Open Access Journal |
| issn | 1662-5145 |
| language | English |
| last_indexed | 2024-12-14T13:33:27Z |
| publishDate | 2021-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Integrative Neuroscience |
| spelling | doaj.art-9339787282a54b2fa11109987b75c99b2022-12-21T22:59:38ZengFrontiers Media S.A.Frontiers in Integrative Neuroscience1662-51452021-12-011510.3389/fnint.2021.793634793634Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” GravitySergio Delle Monache0Sergio Delle Monache1Iole Indovina2Iole Indovina3Myrka Zago4Myrka Zago5Myrka Zago6Elena Daprati7Elena Daprati8Elena Daprati9Francesco Lacquaniti10Francesco Lacquaniti11Francesco Lacquaniti12Gianfranco Bosco13Gianfranco Bosco14Gianfranco Bosco15UniCamillus—Saint Camillus International University of Health Sciences, Rome, ItalyLaboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyLaboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyDepartment of Biomedical and Dental Sciences and Morphofunctional Imaging, University of Messina, Messina, ItalyLaboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyCenter for Space Biomedicine, University of Rome “Tor Vergata”, Rome, ItalyDepartment of Civil and Computer Engineering, University of Rome “Tor Vergata”, Rome, ItalyLaboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyCenter for Space Biomedicine, University of Rome “Tor Vergata”, Rome, ItalyDepartment of Systems Medicine, University of Rome “Tor Vergata”, Rome, ItalyLaboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyCenter for Space Biomedicine, University of Rome “Tor Vergata”, Rome, ItalyDepartment of Systems Medicine, University of Rome “Tor Vergata”, Rome, ItalyLaboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyCenter for Space Biomedicine, University of Rome “Tor Vergata”, Rome, ItalyDepartment of Systems Medicine, University of Rome “Tor Vergata”, Rome, ItalyGravity 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.https://www.frontiersin.org/articles/10.3389/fnint.2021.793634/fullinternal modelvestibular networkneuroimagingTMSconnectomicspsychophysics |
| spellingShingle | Sergio Delle Monache Sergio Delle Monache Iole Indovina Iole Indovina Myrka Zago Myrka Zago Myrka Zago Elena Daprati Elena Daprati Elena Daprati Francesco Lacquaniti Francesco Lacquaniti Francesco Lacquaniti Gianfranco Bosco Gianfranco Bosco Gianfranco Bosco Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of “Visual” Gravity Frontiers in Integrative Neuroscience internal model vestibular network neuroimaging TMS connectomics psychophysics |
| 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 | internal model vestibular network neuroimaging TMS connectomics psychophysics |
| url | https://www.frontiersin.org/articles/10.3389/fnint.2021.793634/full |
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