Interaction of Visual and Proprioceptive Feedback During Adaptation of Human Reaching Movements
1 Department of Biomedical Engineering, Marquette University, Milwaukee, Wisconsin; 2 Department of Physical Medicine and Rehabilitation, Northwestern University Medical School, Chicago, Illinois; 3 Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, Illinois; 4 Institut...
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Veröffentlicht in: | Journal of neurophysiology 2005-06, Vol.93 (6), p.3200-3213 |
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creator | Scheidt, Robert A Conditt, Michael A Secco, Emanuele L Mussa-Ivaldi, Ferdinando A |
description | 1 Department of Biomedical Engineering, Marquette University, Milwaukee, Wisconsin; 2 Department of Physical Medicine and Rehabilitation, Northwestern University Medical School, Chicago, Illinois; 3 Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, Illinois; 4 Institute of Orthopaedic Research and Education, Houston, Texas; and 5 Dipartimento di Informatica e Sistemistica, Universita' di Pavia, Pavia, Italy
Submitted 3 September 2004;
accepted in final form 15 January 2005
People tend to make straight and smooth hand movements when reaching for an object. These trajectory features are resistant to perturbation, and both proprioceptive as well as visual feedback may guide the adaptive updating of motor commands enforcing this regularity. How is information from the two senses combined to generate a coherent internal representation of how the arm moves? Here we show that eliminating visual feedback of hand-path deviations from the straight-line reach (constraining visual feedback of motion within a virtual, "visual channel") prevents compensation of initial direction errors induced by perturbations. Because adaptive reduction in direction errors occurred with proprioception alone, proprioceptive and visual information are not combined in this reaching task using a fixed, linear weighting scheme as reported for static tasks not requiring arm motion. A computer model can explain these findings, assuming that proprioceptive estimates of initial limb posture are used to select motor commands for a desired reach and visual feedback of hand-path errors brings proprioceptive estimates into registration with a visuocentric representation of limb position relative to its target. Simulations demonstrate that initial configuration estimation errors lead to movement direction errors as observed experimentally. Registration improves movement accuracy when veridical visual feedback is provided but is not invoked when hand-path errors are eliminated. However, the visual channel did not exclude adjustment of terminal movement features maximizing hand-path smoothness. Thus visual and proprioceptive feedback may be combined in fundamentally different ways during trajectory control and final position regulation of reaching movements.
Address for reprint requests and other correspondence: R. A. Scheidt, Dept. of Biomedical Engineering, Olin Engineering Center, 303, P.O. Box 1881, Marquette University, Milwaukee, WI 53201-1881 (E-mail: scheidt{at}i |
doi_str_mv | 10.1152/jn.00947.2004 |
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Submitted 3 September 2004;
accepted in final form 15 January 2005
People tend to make straight and smooth hand movements when reaching for an object. These trajectory features are resistant to perturbation, and both proprioceptive as well as visual feedback may guide the adaptive updating of motor commands enforcing this regularity. How is information from the two senses combined to generate a coherent internal representation of how the arm moves? Here we show that eliminating visual feedback of hand-path deviations from the straight-line reach (constraining visual feedback of motion within a virtual, "visual channel") prevents compensation of initial direction errors induced by perturbations. Because adaptive reduction in direction errors occurred with proprioception alone, proprioceptive and visual information are not combined in this reaching task using a fixed, linear weighting scheme as reported for static tasks not requiring arm motion. A computer model can explain these findings, assuming that proprioceptive estimates of initial limb posture are used to select motor commands for a desired reach and visual feedback of hand-path errors brings proprioceptive estimates into registration with a visuocentric representation of limb position relative to its target. Simulations demonstrate that initial configuration estimation errors lead to movement direction errors as observed experimentally. Registration improves movement accuracy when veridical visual feedback is provided but is not invoked when hand-path errors are eliminated. However, the visual channel did not exclude adjustment of terminal movement features maximizing hand-path smoothness. Thus visual and proprioceptive feedback may be combined in fundamentally different ways during trajectory control and final position regulation of reaching movements.
Address for reprint requests and other correspondence: R. A. Scheidt, Dept. of Biomedical Engineering, Olin Engineering Center, 303, P.O. Box 1881, Marquette University, Milwaukee, WI 53201-1881 (E-mail: scheidt{at}ieee.org )</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00947.2004</identifier><identifier>PMID: 15659526</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Adaptation, Physiological - physiology ; Computer Simulation ; Feedback - physiology ; Hand - physiology ; Humans ; Movement - physiology ; Orientation - physiology ; Proprioception - physiology ; Psychomotor Performance - physiology ; Space life sciences ; Time Factors ; Visual Perception - physiology</subject><ispartof>Journal of neurophysiology, 2005-06, Vol.93 (6), p.3200-3213</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c503t-5a83584596042d57febed941911347eff4ff18f8d34e5bff1704be014c047ca43</citedby><cites>FETCH-LOGICAL-c503t-5a83584596042d57febed941911347eff4ff18f8d34e5bff1704be014c047ca43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,3039,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15659526$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Scheidt, Robert A</creatorcontrib><creatorcontrib>Conditt, Michael A</creatorcontrib><creatorcontrib>Secco, Emanuele L</creatorcontrib><creatorcontrib>Mussa-Ivaldi, Ferdinando A</creatorcontrib><title>Interaction of Visual and Proprioceptive Feedback During Adaptation of Human Reaching Movements</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>1 Department of Biomedical Engineering, Marquette University, Milwaukee, Wisconsin; 2 Department of Physical Medicine and Rehabilitation, Northwestern University Medical School, Chicago, Illinois; 3 Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, Illinois; 4 Institute of Orthopaedic Research and Education, Houston, Texas; and 5 Dipartimento di Informatica e Sistemistica, Universita' di Pavia, Pavia, Italy
Submitted 3 September 2004;
accepted in final form 15 January 2005
People tend to make straight and smooth hand movements when reaching for an object. These trajectory features are resistant to perturbation, and both proprioceptive as well as visual feedback may guide the adaptive updating of motor commands enforcing this regularity. How is information from the two senses combined to generate a coherent internal representation of how the arm moves? Here we show that eliminating visual feedback of hand-path deviations from the straight-line reach (constraining visual feedback of motion within a virtual, "visual channel") prevents compensation of initial direction errors induced by perturbations. Because adaptive reduction in direction errors occurred with proprioception alone, proprioceptive and visual information are not combined in this reaching task using a fixed, linear weighting scheme as reported for static tasks not requiring arm motion. A computer model can explain these findings, assuming that proprioceptive estimates of initial limb posture are used to select motor commands for a desired reach and visual feedback of hand-path errors brings proprioceptive estimates into registration with a visuocentric representation of limb position relative to its target. Simulations demonstrate that initial configuration estimation errors lead to movement direction errors as observed experimentally. Registration improves movement accuracy when veridical visual feedback is provided but is not invoked when hand-path errors are eliminated. However, the visual channel did not exclude adjustment of terminal movement features maximizing hand-path smoothness. Thus visual and proprioceptive feedback may be combined in fundamentally different ways during trajectory control and final position regulation of reaching movements.
Address for reprint requests and other correspondence: R. A. Scheidt, Dept. of Biomedical Engineering, Olin Engineering Center, 303, P.O. Box 1881, Marquette University, Milwaukee, WI 53201-1881 (E-mail: scheidt{at}ieee.org )</description><subject>Adaptation, Physiological - physiology</subject><subject>Computer Simulation</subject><subject>Feedback - physiology</subject><subject>Hand - physiology</subject><subject>Humans</subject><subject>Movement - physiology</subject><subject>Orientation - physiology</subject><subject>Proprioception - physiology</subject><subject>Psychomotor Performance - physiology</subject><subject>Space life sciences</subject><subject>Time Factors</subject><subject>Visual Perception - physiology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkEFv1DAQRi0EotvCkSvKCU5ZxrEdJ8eqsLRSEQgVrpbjjHezJHawk8L--zrsAifEaUYz7_sOj5AXFNaUiuLN3q0Bai7XBQB_RFbpVuRU1NVjsgJIOwMpz8h5jHsAkAKKp-SMilLUoihXRN24CYM2U-dd5m32tYuz7jPt2uxT8GPovMFx6u4x2yC2jTbfsrdz6Nw2u2z1OOnfuet50C77jNrslucHf48Duik-I0-s7iM-P80L8mXz7u7qOr_9-P7m6vI2NwLYlAtdMVFxUZfAi1ZIiw22Nac1pYxLtJZbSytbtYyjaNIugTcIlBvg0mjOLsirY-8Y_PcZ46SGLhrse-3Qz1GVsiqpLMR_QSoZZwVdwPwImuBjDGhVsjHocFAU1KJe7Z36pV4t6hP_8lQ8NwO2f-mT6wS8PgK7brv70QVU4-4QO9_77WHpqpkqFUtdiWT_Jjdz39_hzylF_iTU2Fr2AFpmn1Y</recordid><startdate>20050601</startdate><enddate>20050601</enddate><creator>Scheidt, Robert A</creator><creator>Conditt, Michael A</creator><creator>Secco, Emanuele L</creator><creator>Mussa-Ivaldi, Ferdinando A</creator><general>Am Phys Soc</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>7TK</scope><scope>7X8</scope></search><sort><creationdate>20050601</creationdate><title>Interaction of Visual and Proprioceptive Feedback During Adaptation of Human Reaching Movements</title><author>Scheidt, Robert A ; Conditt, Michael A ; Secco, Emanuele L ; Mussa-Ivaldi, Ferdinando A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-5a83584596042d57febed941911347eff4ff18f8d34e5bff1704be014c047ca43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Adaptation, Physiological - physiology</topic><topic>Computer Simulation</topic><topic>Feedback - physiology</topic><topic>Hand - physiology</topic><topic>Humans</topic><topic>Movement - physiology</topic><topic>Orientation - physiology</topic><topic>Proprioception - physiology</topic><topic>Psychomotor Performance - physiology</topic><topic>Space life sciences</topic><topic>Time Factors</topic><topic>Visual Perception - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Scheidt, Robert A</creatorcontrib><creatorcontrib>Conditt, Michael A</creatorcontrib><creatorcontrib>Secco, Emanuele L</creatorcontrib><creatorcontrib>Mussa-Ivaldi, Ferdinando A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Scheidt, Robert A</au><au>Conditt, Michael A</au><au>Secco, Emanuele L</au><au>Mussa-Ivaldi, Ferdinando A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interaction of Visual and Proprioceptive Feedback During Adaptation of Human Reaching Movements</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2005-06-01</date><risdate>2005</risdate><volume>93</volume><issue>6</issue><spage>3200</spage><epage>3213</epage><pages>3200-3213</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>1 Department of Biomedical Engineering, Marquette University, Milwaukee, Wisconsin; 2 Department of Physical Medicine and Rehabilitation, Northwestern University Medical School, Chicago, Illinois; 3 Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, Illinois; 4 Institute of Orthopaedic Research and Education, Houston, Texas; and 5 Dipartimento di Informatica e Sistemistica, Universita' di Pavia, Pavia, Italy
Submitted 3 September 2004;
accepted in final form 15 January 2005
People tend to make straight and smooth hand movements when reaching for an object. These trajectory features are resistant to perturbation, and both proprioceptive as well as visual feedback may guide the adaptive updating of motor commands enforcing this regularity. How is information from the two senses combined to generate a coherent internal representation of how the arm moves? Here we show that eliminating visual feedback of hand-path deviations from the straight-line reach (constraining visual feedback of motion within a virtual, "visual channel") prevents compensation of initial direction errors induced by perturbations. Because adaptive reduction in direction errors occurred with proprioception alone, proprioceptive and visual information are not combined in this reaching task using a fixed, linear weighting scheme as reported for static tasks not requiring arm motion. A computer model can explain these findings, assuming that proprioceptive estimates of initial limb posture are used to select motor commands for a desired reach and visual feedback of hand-path errors brings proprioceptive estimates into registration with a visuocentric representation of limb position relative to its target. Simulations demonstrate that initial configuration estimation errors lead to movement direction errors as observed experimentally. Registration improves movement accuracy when veridical visual feedback is provided but is not invoked when hand-path errors are eliminated. However, the visual channel did not exclude adjustment of terminal movement features maximizing hand-path smoothness. Thus visual and proprioceptive feedback may be combined in fundamentally different ways during trajectory control and final position regulation of reaching movements.
Address for reprint requests and other correspondence: R. A. Scheidt, Dept. of Biomedical Engineering, Olin Engineering Center, 303, P.O. Box 1881, Marquette University, Milwaukee, WI 53201-1881 (E-mail: scheidt{at}ieee.org )</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>15659526</pmid><doi>10.1152/jn.00947.2004</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Physiological - physiology Computer Simulation Feedback - physiology Hand - physiology Humans Movement - physiology Orientation - physiology Proprioception - physiology Psychomotor Performance - physiology Space life sciences Time Factors Visual Perception - physiology |
title | Interaction of Visual and Proprioceptive Feedback During Adaptation of Human Reaching Movements |
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