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Prolonged asymmetric vestibular stimulation induces opposite, long‐term effects on self‐motion perception and ocular responses
Key points • The semicircular canals of the labyrinths are a source of information for self‐motion perception and reflex eye movements. • Prolonged vestibular asymmetric stimulation of standing humans about the earth‐vertical axis, made of fast body rotation to one side and slow rotation to the ot...
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Published in: | The Journal of physiology 2013-04, Vol.591 (7), p.1907-1920 |
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container_title | The Journal of physiology |
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creator | Pettorossi, V. E. Panichi, R. Botti, F. M. Kyriakareli, A. Ferraresi, A. Faralli, M. Schieppati, M. Bronstein, A. M. |
description | Key points
•
The semicircular canals of the labyrinths are a source of information for self‐motion perception and reflex eye movements.
•
Prolonged vestibular asymmetric stimulation of standing humans about the earth‐vertical axis, made of fast body rotation to one side and slow rotation to the other side, induced different adaptive mechanisms in the perception of body motion and in the vestibulo‐ocular reflex (VOR).
•
Motion perception became progressively more asymmetric, increasing gradually in response to the fast body rotation and decreasing in response to the slow rotation. VOR became gradually more symmetric, decreasing for fast body movement and increasing for slow movement.
•
These oppositely directed adaptive effects in motion perception and VOR persisted for at least 30 min.
•
Long‐lasting asymmetric stimulation discloses independent brain mechanisms for perception of body motion and eye movement control.
•
These adaptive mechanisms may enhance awareness toward the side where the body is moving faster, while improving eye stabilizing properties of the VOR.
Self‐motion perception and the vestibulo‐ocular reflex (VOR) were investigated in healthy subjects during asymmetric whole body yaw plane oscillations while standing on a platform in the dark. Platform oscillation consisted of two half‐sinusoidal cycles of the same amplitude (40°) but different duration, featuring a fast (FHC) and a slow half‐cycle (SHC). Rotation consisted of four or 20 consecutive cycles to probe adaptation further with the longer duration protocol. Self‐motion perception was estimated by subjects tracking with a pointer the remembered position of an earth‐fixed visual target. VOR was measured by electro‐oculography. The asymmetric stimulation pattern consistently induced a progressive increase of asymmetry in motion perception, whereby the gain of the tracking response gradually increased during FHCs and decreased during SHCs. The effect was observed already during the first few cycles and further increased during 20 cycles, leading to a totally distorted location of the initial straight‐ahead. In contrast, after some initial interindividual variability, the gain of the slow phase VOR became symmetric, decreasing for FHCs and increasing for SHCs. These oppositely directed adaptive effects in motion perception and VOR persisted for nearly an hour. Control conditions using prolonged but symmetrical stimuli produced no adaptive effects on either motion perception or VO |
doi_str_mv | 10.1113/jphysiol.2012.241182 |
format | article |
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•
The semicircular canals of the labyrinths are a source of information for self‐motion perception and reflex eye movements.
•
Prolonged vestibular asymmetric stimulation of standing humans about the earth‐vertical axis, made of fast body rotation to one side and slow rotation to the other side, induced different adaptive mechanisms in the perception of body motion and in the vestibulo‐ocular reflex (VOR).
•
Motion perception became progressively more asymmetric, increasing gradually in response to the fast body rotation and decreasing in response to the slow rotation. VOR became gradually more symmetric, decreasing for fast body movement and increasing for slow movement.
•
These oppositely directed adaptive effects in motion perception and VOR persisted for at least 30 min.
•
Long‐lasting asymmetric stimulation discloses independent brain mechanisms for perception of body motion and eye movement control.
•
These adaptive mechanisms may enhance awareness toward the side where the body is moving faster, while improving eye stabilizing properties of the VOR.
Self‐motion perception and the vestibulo‐ocular reflex (VOR) were investigated in healthy subjects during asymmetric whole body yaw plane oscillations while standing on a platform in the dark. Platform oscillation consisted of two half‐sinusoidal cycles of the same amplitude (40°) but different duration, featuring a fast (FHC) and a slow half‐cycle (SHC). Rotation consisted of four or 20 consecutive cycles to probe adaptation further with the longer duration protocol. Self‐motion perception was estimated by subjects tracking with a pointer the remembered position of an earth‐fixed visual target. VOR was measured by electro‐oculography. The asymmetric stimulation pattern consistently induced a progressive increase of asymmetry in motion perception, whereby the gain of the tracking response gradually increased during FHCs and decreased during SHCs. The effect was observed already during the first few cycles and further increased during 20 cycles, leading to a totally distorted location of the initial straight‐ahead. In contrast, after some initial interindividual variability, the gain of the slow phase VOR became symmetric, decreasing for FHCs and increasing for SHCs. These oppositely directed adaptive effects in motion perception and VOR persisted for nearly an hour. Control conditions using prolonged but symmetrical stimuli produced no adaptive effects on either motion perception or VOR. These findings show that prolonged asymmetric activation of the vestibular system leads to opposite patterns of adaptation of self‐motion perception and VOR. The results provide strong evidence that semicircular canal inputs are processed centrally by independent mechanisms for perception of body motion and eye movement control. These divergent adaptation mechanisms enhance awareness of movement toward the faster body rotation, while improving the eye stabilizing properties of the VOR.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/jphysiol.2012.241182</identifier><identifier>PMID: 23318876</identifier><identifier>CODEN: JPHYA7</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Adult ; Eye Movements - physiology ; Female ; Humans ; Male ; Middle Aged ; Motion Perception - physiology ; Neuroscience: Behavioural/Systems/Cognitive ; Reflex, Vestibulo-Ocular - physiology ; Rotation ; Young Adult</subject><ispartof>The Journal of physiology, 2013-04, Vol.591 (7), p.1907-1920</ispartof><rights>2013 The Authors. The Journal of Physiology © 2013 The Physiological Society</rights><rights>2013 The Authors. The Journal of Physiology © 2013 The Physiological Society 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5707-dcdb054053af580cac17a365b5df2e05830faeffcfff72d818ea51cff1373ef73</citedby><cites>FETCH-LOGICAL-c5707-dcdb054053af580cac17a365b5df2e05830faeffcfff72d818ea51cff1373ef73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3624859/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3624859/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23318876$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pettorossi, V. E.</creatorcontrib><creatorcontrib>Panichi, R.</creatorcontrib><creatorcontrib>Botti, F. M.</creatorcontrib><creatorcontrib>Kyriakareli, A.</creatorcontrib><creatorcontrib>Ferraresi, A.</creatorcontrib><creatorcontrib>Faralli, M.</creatorcontrib><creatorcontrib>Schieppati, M.</creatorcontrib><creatorcontrib>Bronstein, A. M.</creatorcontrib><title>Prolonged asymmetric vestibular stimulation induces opposite, long‐term effects on self‐motion perception and ocular responses</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
•
The semicircular canals of the labyrinths are a source of information for self‐motion perception and reflex eye movements.
•
Prolonged vestibular asymmetric stimulation of standing humans about the earth‐vertical axis, made of fast body rotation to one side and slow rotation to the other side, induced different adaptive mechanisms in the perception of body motion and in the vestibulo‐ocular reflex (VOR).
•
Motion perception became progressively more asymmetric, increasing gradually in response to the fast body rotation and decreasing in response to the slow rotation. VOR became gradually more symmetric, decreasing for fast body movement and increasing for slow movement.
•
These oppositely directed adaptive effects in motion perception and VOR persisted for at least 30 min.
•
Long‐lasting asymmetric stimulation discloses independent brain mechanisms for perception of body motion and eye movement control.
•
These adaptive mechanisms may enhance awareness toward the side where the body is moving faster, while improving eye stabilizing properties of the VOR.
Self‐motion perception and the vestibulo‐ocular reflex (VOR) were investigated in healthy subjects during asymmetric whole body yaw plane oscillations while standing on a platform in the dark. Platform oscillation consisted of two half‐sinusoidal cycles of the same amplitude (40°) but different duration, featuring a fast (FHC) and a slow half‐cycle (SHC). Rotation consisted of four or 20 consecutive cycles to probe adaptation further with the longer duration protocol. Self‐motion perception was estimated by subjects tracking with a pointer the remembered position of an earth‐fixed visual target. VOR was measured by electro‐oculography. The asymmetric stimulation pattern consistently induced a progressive increase of asymmetry in motion perception, whereby the gain of the tracking response gradually increased during FHCs and decreased during SHCs. The effect was observed already during the first few cycles and further increased during 20 cycles, leading to a totally distorted location of the initial straight‐ahead. In contrast, after some initial interindividual variability, the gain of the slow phase VOR became symmetric, decreasing for FHCs and increasing for SHCs. These oppositely directed adaptive effects in motion perception and VOR persisted for nearly an hour. Control conditions using prolonged but symmetrical stimuli produced no adaptive effects on either motion perception or VOR. These findings show that prolonged asymmetric activation of the vestibular system leads to opposite patterns of adaptation of self‐motion perception and VOR. The results provide strong evidence that semicircular canal inputs are processed centrally by independent mechanisms for perception of body motion and eye movement control. These divergent adaptation mechanisms enhance awareness of movement toward the faster body rotation, while improving the eye stabilizing properties of the VOR.</description><subject>Adult</subject><subject>Eye Movements - physiology</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Motion Perception - physiology</subject><subject>Neuroscience: Behavioural/Systems/Cognitive</subject><subject>Reflex, Vestibulo-Ocular - physiology</subject><subject>Rotation</subject><subject>Young Adult</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqNks9u1DAQxi0EokvhDRCKxIUDWTx2vHYuSFXFX1Wih3K2vM649Sqxg50U7Q3xBDwjT4J3t62AC5w89vy-T-PRR8hToEsA4K8249U2-9gvGQW2ZA2AYvfIAppVW0vZ8vtkQSljNZcCjsijnDeUAqdt-5AcMc5BKblakO_nKfYxXGJXmbwdBpySt9U15smv596kqhRDKSYfQ-VDN1vMVRzHmP2EL6ud9Oe3HxOmoULn0E6lG6qMvSvPQ9zLRkwWx31pQldFuzdOmMcYMubH5IEzfcYnN-cx-fz2zcXp-_rs07sPpydntRWSyrqz3ZqKhgpunFDUGgvS8JVYi84xpEJx6kyZwTrnJOsUKDQCyg245OgkPyavD77jvB6wsximZHo9Jj-YtNXReP1nJ_grfRmvNV-xRom2GLy4MUjxy1xWpAefLfa9CRjnrKGBlgvVUvVvlDPOZCvpqqDP_0I3cU6hbGJHMWAKQBSqOVA2xZwTuru5gepdHvRtHvQuD_qQhyJ79vuf70S3AShAewC--h63_2WqLz6eC9FI_gvlT8y4</recordid><startdate>201304</startdate><enddate>201304</enddate><creator>Pettorossi, V. E.</creator><creator>Panichi, R.</creator><creator>Botti, F. M.</creator><creator>Kyriakareli, A.</creator><creator>Ferraresi, A.</creator><creator>Faralli, M.</creator><creator>Schieppati, M.</creator><creator>Bronstein, A. M.</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><general>Blackwell Science Inc</general><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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201304</creationdate><title>Prolonged asymmetric vestibular stimulation induces opposite, long‐term effects on self‐motion perception and ocular responses</title><author>Pettorossi, V. E. ; Panichi, R. ; Botti, F. M. ; Kyriakareli, A. ; Ferraresi, A. ; Faralli, M. ; Schieppati, M. ; Bronstein, A. M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5707-dcdb054053af580cac17a365b5df2e05830faeffcfff72d818ea51cff1373ef73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adult</topic><topic>Eye Movements - physiology</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Motion Perception - physiology</topic><topic>Neuroscience: Behavioural/Systems/Cognitive</topic><topic>Reflex, Vestibulo-Ocular - physiology</topic><topic>Rotation</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pettorossi, V. E.</creatorcontrib><creatorcontrib>Panichi, R.</creatorcontrib><creatorcontrib>Botti, F. M.</creatorcontrib><creatorcontrib>Kyriakareli, A.</creatorcontrib><creatorcontrib>Ferraresi, A.</creatorcontrib><creatorcontrib>Faralli, M.</creatorcontrib><creatorcontrib>Schieppati, M.</creatorcontrib><creatorcontrib>Bronstein, A. M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pettorossi, V. E.</au><au>Panichi, R.</au><au>Botti, F. M.</au><au>Kyriakareli, A.</au><au>Ferraresi, A.</au><au>Faralli, M.</au><au>Schieppati, M.</au><au>Bronstein, A. M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prolonged asymmetric vestibular stimulation induces opposite, long‐term effects on self‐motion perception and ocular responses</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2013-04</date><risdate>2013</risdate><volume>591</volume><issue>7</issue><spage>1907</spage><epage>1920</epage><pages>1907-1920</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><coden>JPHYA7</coden><abstract>Key points
•
The semicircular canals of the labyrinths are a source of information for self‐motion perception and reflex eye movements.
•
Prolonged vestibular asymmetric stimulation of standing humans about the earth‐vertical axis, made of fast body rotation to one side and slow rotation to the other side, induced different adaptive mechanisms in the perception of body motion and in the vestibulo‐ocular reflex (VOR).
•
Motion perception became progressively more asymmetric, increasing gradually in response to the fast body rotation and decreasing in response to the slow rotation. VOR became gradually more symmetric, decreasing for fast body movement and increasing for slow movement.
•
These oppositely directed adaptive effects in motion perception and VOR persisted for at least 30 min.
•
Long‐lasting asymmetric stimulation discloses independent brain mechanisms for perception of body motion and eye movement control.
•
These adaptive mechanisms may enhance awareness toward the side where the body is moving faster, while improving eye stabilizing properties of the VOR.
Self‐motion perception and the vestibulo‐ocular reflex (VOR) were investigated in healthy subjects during asymmetric whole body yaw plane oscillations while standing on a platform in the dark. Platform oscillation consisted of two half‐sinusoidal cycles of the same amplitude (40°) but different duration, featuring a fast (FHC) and a slow half‐cycle (SHC). Rotation consisted of four or 20 consecutive cycles to probe adaptation further with the longer duration protocol. Self‐motion perception was estimated by subjects tracking with a pointer the remembered position of an earth‐fixed visual target. VOR was measured by electro‐oculography. The asymmetric stimulation pattern consistently induced a progressive increase of asymmetry in motion perception, whereby the gain of the tracking response gradually increased during FHCs and decreased during SHCs. The effect was observed already during the first few cycles and further increased during 20 cycles, leading to a totally distorted location of the initial straight‐ahead. In contrast, after some initial interindividual variability, the gain of the slow phase VOR became symmetric, decreasing for FHCs and increasing for SHCs. These oppositely directed adaptive effects in motion perception and VOR persisted for nearly an hour. Control conditions using prolonged but symmetrical stimuli produced no adaptive effects on either motion perception or VOR. These findings show that prolonged asymmetric activation of the vestibular system leads to opposite patterns of adaptation of self‐motion perception and VOR. The results provide strong evidence that semicircular canal inputs are processed centrally by independent mechanisms for perception of body motion and eye movement control. These divergent adaptation mechanisms enhance awareness of movement toward the faster body rotation, while improving the eye stabilizing properties of the VOR.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>23318876</pmid><doi>10.1113/jphysiol.2012.241182</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adult Eye Movements - physiology Female Humans Male Middle Aged Motion Perception - physiology Neuroscience: Behavioural/Systems/Cognitive Reflex, Vestibulo-Ocular - physiology Rotation Young Adult |
title | Prolonged asymmetric vestibular stimulation induces opposite, long‐term effects on self‐motion perception and ocular responses |
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