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Vestibular information is necessary for maintaining metric properties of representational space: Evidence from mental imagery
► Mental imagery deficits depend on the extent (bilateral vs. unilateral) of vestibular loss. ► Mental rotation of 3D objects is also impaired. ► Vestibular loss disrupts mental scanning in unfamiliar and in familiar environments. ► Mental imagery deficits decrease with vestibular compensation. ► Ne...
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Published in: | Neuropsychologia 2011-09, Vol.49 (11), p.3136-3144 |
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description | ► Mental imagery deficits depend on the extent (bilateral vs. unilateral) of vestibular loss. ► Mental rotation of 3D objects is also impaired. ► Vestibular loss disrupts mental scanning in unfamiliar and in familiar environments. ► Mental imagery deficits decrease with vestibular compensation. ► Neural networks common to vestibular processing and mental imagery are disorganized.
The vestibular system contributes to a wide range of functions, from postural and oculomotor reflexes to spatial representation and cognition. Vestibular signals are important to maintain an internal, updated representation of the body position and movement in space. However, it is not clear to what extent they are also necessary to mentally simulate movement in situations that do not involve displacements of the body, as in mental imagery. The present study assessed how vestibular loss can affect object-based mental transformations (OMTs), i.e., imagined rotations or translations of objects relative to the environment. Participants performed one task of mental rotation of 3D-objects and two mental scanning tasks dealing with the ability to build and manipulate mental images that have metric properties. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (1 week and 1 month). They were compared to healthy participants tested at similar time intervals and to bilateral vestibular-defective patients tested after the recovery period. Vestibular loss impaired all mental imagery tasks. Performance varied according to the extent of vestibular loss (bilateral patients were frequently the most impaired) and according to the time elapsed after unilateral vestibular neurotomy (deficits were stronger at the early stage after neurotomy and then gradually compensated). These findings indicate that vestibular signals are necessary to perform OMTs and provide the first demonstration of the critical role of vestibular signals in processing metric properties of mental representations. They suggest that vestibular loss disorganizes brain structures commonly involved in mental imagery, and more generally in mental representation. |
doi_str_mv | 10.1016/j.neuropsychologia.2011.07.026 |
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The vestibular system contributes to a wide range of functions, from postural and oculomotor reflexes to spatial representation and cognition. Vestibular signals are important to maintain an internal, updated representation of the body position and movement in space. However, it is not clear to what extent they are also necessary to mentally simulate movement in situations that do not involve displacements of the body, as in mental imagery. The present study assessed how vestibular loss can affect object-based mental transformations (OMTs), i.e., imagined rotations or translations of objects relative to the environment. Participants performed one task of mental rotation of 3D-objects and two mental scanning tasks dealing with the ability to build and manipulate mental images that have metric properties. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (1 week and 1 month). They were compared to healthy participants tested at similar time intervals and to bilateral vestibular-defective patients tested after the recovery period. Vestibular loss impaired all mental imagery tasks. Performance varied according to the extent of vestibular loss (bilateral patients were frequently the most impaired) and according to the time elapsed after unilateral vestibular neurotomy (deficits were stronger at the early stage after neurotomy and then gradually compensated). These findings indicate that vestibular signals are necessary to perform OMTs and provide the first demonstration of the critical role of vestibular signals in processing metric properties of mental representations. They suggest that vestibular loss disorganizes brain structures commonly involved in mental imagery, and more generally in mental representation.</description><identifier>ISSN: 0028-3932</identifier><identifier>EISSN: 1873-3514</identifier><identifier>DOI: 10.1016/j.neuropsychologia.2011.07.026</identifier><identifier>PMID: 21820000</identifier><identifier>CODEN: NUPSA6</identifier><language>eng</language><publisher>Kidlington: Elsevier Ltd</publisher><subject>Adult ; Adult and adolescent clinical studies ; Aged ; Biological and medical sciences ; Ear, auditive nerve, cochleovestibular tract, facial nerve: diseases, semeiology ; Female ; Humans ; Imagination - physiology ; Life Sciences ; Male ; Medical sciences ; Meniere Disease - physiopathology ; Menière's disease ; Mental imagery ; Middle Aged ; Neurons and Cognition ; Non tumoral diseases ; Object-based mental transformations ; Organic mental disorders. Neuropsychology ; Otorhinolaryngology. Stomatology ; Psychology. Psychoanalysis. Psychiatry ; Psychomotor Performance - physiology ; Psychopathology. Psychiatry ; Rotation ; Space Perception - physiology ; Spatial ability ; Vestibular compensation ; Vestibular Diseases - physiopathology ; Vestibule, Labyrinth - physiology ; Visual Perception - physiology</subject><ispartof>Neuropsychologia, 2011-09, Vol.49 (11), p.3136-3144</ispartof><rights>2011 Elsevier Ltd</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2011 Elsevier Ltd. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c487t-9711d947a1fc6edaa1f0ffd8e5919f32e37b7ef4ee085c206a56e0f524c996c43</citedby><cites>FETCH-LOGICAL-c487t-9711d947a1fc6edaa1f0ffd8e5919f32e37b7ef4ee085c206a56e0f524c996c43</cites><orcidid>0000-0002-3211-3523</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24492638$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21820000$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01449861$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Péruch, Patrick</creatorcontrib><creatorcontrib>Lopez, Christophe</creatorcontrib><creatorcontrib>Redon-Zouiteni, Christine</creatorcontrib><creatorcontrib>Escoffier, Guy</creatorcontrib><creatorcontrib>Zeitoun, Alain</creatorcontrib><creatorcontrib>Sanjuan, Mélanie</creatorcontrib><creatorcontrib>Devèze, Arnaud</creatorcontrib><creatorcontrib>Magnan, Jacques</creatorcontrib><creatorcontrib>Borel, Liliane</creatorcontrib><title>Vestibular information is necessary for maintaining metric properties of representational space: Evidence from mental imagery</title><title>Neuropsychologia</title><addtitle>Neuropsychologia</addtitle><description>► Mental imagery deficits depend on the extent (bilateral vs. unilateral) of vestibular loss. ► Mental rotation of 3D objects is also impaired. ► Vestibular loss disrupts mental scanning in unfamiliar and in familiar environments. ► Mental imagery deficits decrease with vestibular compensation. ► Neural networks common to vestibular processing and mental imagery are disorganized.
The vestibular system contributes to a wide range of functions, from postural and oculomotor reflexes to spatial representation and cognition. Vestibular signals are important to maintain an internal, updated representation of the body position and movement in space. However, it is not clear to what extent they are also necessary to mentally simulate movement in situations that do not involve displacements of the body, as in mental imagery. The present study assessed how vestibular loss can affect object-based mental transformations (OMTs), i.e., imagined rotations or translations of objects relative to the environment. Participants performed one task of mental rotation of 3D-objects and two mental scanning tasks dealing with the ability to build and manipulate mental images that have metric properties. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (1 week and 1 month). They were compared to healthy participants tested at similar time intervals and to bilateral vestibular-defective patients tested after the recovery period. Vestibular loss impaired all mental imagery tasks. Performance varied according to the extent of vestibular loss (bilateral patients were frequently the most impaired) and according to the time elapsed after unilateral vestibular neurotomy (deficits were stronger at the early stage after neurotomy and then gradually compensated). These findings indicate that vestibular signals are necessary to perform OMTs and provide the first demonstration of the critical role of vestibular signals in processing metric properties of mental representations. 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Psychiatry</subject><subject>Rotation</subject><subject>Space Perception - physiology</subject><subject>Spatial ability</subject><subject>Vestibular compensation</subject><subject>Vestibular Diseases - physiopathology</subject><subject>Vestibule, Labyrinth - physiology</subject><subject>Visual Perception - physiology</subject><issn>0028-3932</issn><issn>1873-3514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqNkc-L1DAUx4Mo7rj6L0guKh46JmnaJh6EZVkdYcCLeg2Z9GU2Q9vUpB2Yg_-7r8y4ghclPB55fN7PLyGvOVtzxut3h_UAc4pjPrn72MV9sGvBOF-zZs1E_YisuGrKoqy4fExWjAlVlLoUV-RZzgfGmKyEekquBFcCf2xFfn6HPIXd3NlEw-Bj6u0U4kBDpgM4yNmmE8Uw7W0YJrQw7GkPUwqOjjgHpClAptHTBGOCDAgtBWxH82gdvKd3x9DC4ID6FHtMRaCjobd7SKfn5Im3XYYXF39Nvn28-3q7KbZfPn2-vdkWTqpmKnTDeatlY7l3NbQWPfO-VVBprn0poGx2DXgJwFTlBKttVQPzlZBO69rJ8pq8Pde9t50ZE3ZPJxNtMJubrVlijEupVc2PHNk3ZxbX-zHjdUwfsoOuswPEORvNWYNW6X-SSkl8QtdIfjiTLsWcE_iHITgzi67mYP7W1Sy6GtYY1BULvLy0mnc9tA_pv4VE4NUFsNnZzic7uJD_cLgellHIbc4c4LmPAZLJLizytCGBm0wbw__O9Avhac5t</recordid><startdate>20110901</startdate><enddate>20110901</enddate><creator>Péruch, Patrick</creator><creator>Lopez, Christophe</creator><creator>Redon-Zouiteni, Christine</creator><creator>Escoffier, Guy</creator><creator>Zeitoun, Alain</creator><creator>Sanjuan, Mélanie</creator><creator>Devèze, Arnaud</creator><creator>Magnan, Jacques</creator><creator>Borel, Liliane</creator><general>Elsevier Ltd</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7TK</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-3211-3523</orcidid></search><sort><creationdate>20110901</creationdate><title>Vestibular information is necessary for maintaining metric properties of representational space: Evidence from mental imagery</title><author>Péruch, Patrick ; Lopez, Christophe ; Redon-Zouiteni, Christine ; Escoffier, Guy ; Zeitoun, Alain ; Sanjuan, Mélanie ; Devèze, Arnaud ; Magnan, Jacques ; Borel, Liliane</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c487t-9711d947a1fc6edaa1f0ffd8e5919f32e37b7ef4ee085c206a56e0f524c996c43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Adult</topic><topic>Adult and adolescent clinical studies</topic><topic>Aged</topic><topic>Biological and medical sciences</topic><topic>Ear, auditive nerve, cochleovestibular tract, facial nerve: diseases, semeiology</topic><topic>Female</topic><topic>Humans</topic><topic>Imagination - physiology</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Meniere Disease - physiopathology</topic><topic>Menière's disease</topic><topic>Mental imagery</topic><topic>Middle Aged</topic><topic>Neurons and Cognition</topic><topic>Non tumoral diseases</topic><topic>Object-based mental transformations</topic><topic>Organic mental disorders. Neuropsychology</topic><topic>Otorhinolaryngology. Stomatology</topic><topic>Psychology. Psychoanalysis. Psychiatry</topic><topic>Psychomotor Performance - physiology</topic><topic>Psychopathology. Psychiatry</topic><topic>Rotation</topic><topic>Space Perception - physiology</topic><topic>Spatial ability</topic><topic>Vestibular compensation</topic><topic>Vestibular Diseases - physiopathology</topic><topic>Vestibule, Labyrinth - physiology</topic><topic>Visual Perception - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Péruch, Patrick</creatorcontrib><creatorcontrib>Lopez, Christophe</creatorcontrib><creatorcontrib>Redon-Zouiteni, Christine</creatorcontrib><creatorcontrib>Escoffier, Guy</creatorcontrib><creatorcontrib>Zeitoun, Alain</creatorcontrib><creatorcontrib>Sanjuan, Mélanie</creatorcontrib><creatorcontrib>Devèze, Arnaud</creatorcontrib><creatorcontrib>Magnan, Jacques</creatorcontrib><creatorcontrib>Borel, Liliane</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Neuropsychologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Péruch, Patrick</au><au>Lopez, Christophe</au><au>Redon-Zouiteni, Christine</au><au>Escoffier, Guy</au><au>Zeitoun, Alain</au><au>Sanjuan, Mélanie</au><au>Devèze, Arnaud</au><au>Magnan, Jacques</au><au>Borel, Liliane</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vestibular information is necessary for maintaining metric properties of representational space: Evidence from mental imagery</atitle><jtitle>Neuropsychologia</jtitle><addtitle>Neuropsychologia</addtitle><date>2011-09-01</date><risdate>2011</risdate><volume>49</volume><issue>11</issue><spage>3136</spage><epage>3144</epage><pages>3136-3144</pages><issn>0028-3932</issn><eissn>1873-3514</eissn><coden>NUPSA6</coden><abstract>► Mental imagery deficits depend on the extent (bilateral vs. unilateral) of vestibular loss. ► Mental rotation of 3D objects is also impaired. ► Vestibular loss disrupts mental scanning in unfamiliar and in familiar environments. ► Mental imagery deficits decrease with vestibular compensation. ► Neural networks common to vestibular processing and mental imagery are disorganized.
The vestibular system contributes to a wide range of functions, from postural and oculomotor reflexes to spatial representation and cognition. Vestibular signals are important to maintain an internal, updated representation of the body position and movement in space. However, it is not clear to what extent they are also necessary to mentally simulate movement in situations that do not involve displacements of the body, as in mental imagery. The present study assessed how vestibular loss can affect object-based mental transformations (OMTs), i.e., imagined rotations or translations of objects relative to the environment. Participants performed one task of mental rotation of 3D-objects and two mental scanning tasks dealing with the ability to build and manipulate mental images that have metric properties. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (1 week and 1 month). They were compared to healthy participants tested at similar time intervals and to bilateral vestibular-defective patients tested after the recovery period. Vestibular loss impaired all mental imagery tasks. Performance varied according to the extent of vestibular loss (bilateral patients were frequently the most impaired) and according to the time elapsed after unilateral vestibular neurotomy (deficits were stronger at the early stage after neurotomy and then gradually compensated). These findings indicate that vestibular signals are necessary to perform OMTs and provide the first demonstration of the critical role of vestibular signals in processing metric properties of mental representations. They suggest that vestibular loss disorganizes brain structures commonly involved in mental imagery, and more generally in mental representation.</abstract><cop>Kidlington</cop><pub>Elsevier Ltd</pub><pmid>21820000</pmid><doi>10.1016/j.neuropsychologia.2011.07.026</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-3211-3523</orcidid></addata></record> |
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subjects | Adult Adult and adolescent clinical studies Aged Biological and medical sciences Ear, auditive nerve, cochleovestibular tract, facial nerve: diseases, semeiology Female Humans Imagination - physiology Life Sciences Male Medical sciences Meniere Disease - physiopathology Menière's disease Mental imagery Middle Aged Neurons and Cognition Non tumoral diseases Object-based mental transformations Organic mental disorders. Neuropsychology Otorhinolaryngology. Stomatology Psychology. Psychoanalysis. Psychiatry Psychomotor Performance - physiology Psychopathology. Psychiatry Rotation Space Perception - physiology Spatial ability Vestibular compensation Vestibular Diseases - physiopathology Vestibule, Labyrinth - physiology Visual Perception - physiology |
title | Vestibular information is necessary for maintaining metric properties of representational space: Evidence from mental imagery |
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