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Savings for visuomotor adaptation require prior history of error, not prior repetition of successful actions

Identifieur interne : 001993 ( Pmc/Corpus ); précédent : 001992; suivant : 001994

Savings for visuomotor adaptation require prior history of error, not prior repetition of successful actions

Auteurs : Li-Ann Leow ; Aymar De Rugy ; Welber Marinovic ; Stephan Riek ; Timothy J. Carroll

Source :

RBID : PMC:5144718

Abstract

Learning to adapt movements to compensate for unexpected perturbations shows savings, or faster readaptation to a previously encountered perturbation. Using a factorial design, we examined how savings is affected by prior experience of similar errors and prior repetition of the action required to eliminate errors. The data show that prior experience of errors is both necessary and sufficient for savings, whereas prior repetition of a successful action is neither necessary nor sufficient for savings.


Url:
DOI: 10.1152/jn.01055.2015
PubMed: 27486109
PubMed Central: 5144718

Links to Exploration step

PMC:5144718

Le document en format XML

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<nlm:aff id="aff1">Centre for Sensorimotor Performance, School of Human Movement and Nutrition Sciences, The University of Queensland, Brisbane, Queensland, Australia;</nlm:aff>
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<name sortKey="De Rugy, Aymar" sort="De Rugy, Aymar" uniqKey="De Rugy A" first="Aymar" last="De Rugy">Aymar De Rugy</name>
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<nlm:aff id="aff1">Centre for Sensorimotor Performance, School of Human Movement and Nutrition Sciences, The University of Queensland, Brisbane, Queensland, Australia;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff2">Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, CNRS UMR 5287, Université de Bordeaux, Bordeaux, France;</nlm:aff>
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<name sortKey="Marinovic, Welber" sort="Marinovic, Welber" uniqKey="Marinovic W" first="Welber" last="Marinovic">Welber Marinovic</name>
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<nlm:aff id="aff4">Centre of Clinical Research Excellent in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Queensland, Australia</nlm:aff>
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<name sortKey="Riek, Stephan" sort="Riek, Stephan" uniqKey="Riek S" first="Stephan" last="Riek">Stephan Riek</name>
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<name sortKey="Riek, Stephan" sort="Riek, Stephan" uniqKey="Riek S" first="Stephan" last="Riek">Stephan Riek</name>
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<name sortKey="Carroll, Timothy J" sort="Carroll, Timothy J" uniqKey="Carroll T" first="Timothy J." last="Carroll">Timothy J. Carroll</name>
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<p>
<italic>Learning to adapt movements to compensate for unexpected perturbations shows savings, or faster readaptation to a previously encountered perturbation. Using a factorial design, we examined how savings is affected by prior experience of similar errors and prior repetition of the action required to eliminate errors. The data show that prior experience of errors is both necessary and sufficient for savings, whereas prior repetition of a successful action is neither necessary nor sufficient for savings</italic>
.</p>
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<journal-id journal-id-type="nlm-ta">J Neurophysiol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Neurophysiol</journal-id>
<journal-id journal-id-type="hwp">jn</journal-id>
<journal-id journal-id-type="pmc">jn</journal-id>
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<journal-title>Journal of Neurophysiology</journal-title>
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<issn pub-type="ppub">0022-3077</issn>
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<publisher>
<publisher-name>American Physiological Society</publisher-name>
<publisher-loc>Bethesda, MD</publisher-loc>
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<article-id pub-id-type="doi">10.1152/jn.01055.2015</article-id>
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<subject>Control of Movement</subject>
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<article-title>Savings for visuomotor adaptation require prior history of error, not prior repetition of successful actions</article-title>
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<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-9655-3181</contrib-id>
<name>
<surname>Leow</surname>
<given-names>Li-Ann</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>de Rugy</surname>
<given-names>Aymar</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
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<name>
<surname>Marinovic</surname>
<given-names>Welber</given-names>
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<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Riek</surname>
<given-names>Stephan</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
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<contrib contrib-type="author">
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<surname>Carroll</surname>
<given-names>Timothy J.</given-names>
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<sup>1</sup>
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<aff id="aff1">
<sup>1</sup>
Centre for Sensorimotor Performance, School of Human Movement and Nutrition Sciences, The University of Queensland, Brisbane, Queensland, Australia;</aff>
<aff id="aff2">
<sup>2</sup>
Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, CNRS UMR 5287, Université de Bordeaux, Bordeaux, France;</aff>
<aff id="aff3">
<sup>3</sup>
School of Psychology and Speech Pathology, Curtin University, Bentley, Western Australia, Australia; and</aff>
<aff id="aff4">
<sup>4</sup>
Centre of Clinical Research Excellent in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Queensland, Australia</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">Address for reprint requests and other correspondence: L.-A. Leow,
<addr-line>Centre for Sensorimotor Performance, School of Human Movement and Nutrition Sciences, Bldg. 26B, The Univ. of Queensland, Brisbane, Qld 4072, Australia</addr-line>
(e-mail:
<email>l.leow@uq.edu.au</email>
).</corresp>
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<pub-date pub-type="epub">
<day>13</day>
<month>7</month>
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<month>10</month>
<year>2016</year>
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<pmc-comment> PMC Release delay is 12 months and 0 days and was based on the . </pmc-comment>
<volume>116</volume>
<issue>4</issue>
<fpage>1603</fpage>
<lpage>1614</lpage>
<history>
<date date-type="received">
<day>25</day>
<month>11</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>5</day>
<month>7</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2016 the American Physiological Society</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>American Physiological Society</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="z9k01016001603.pdf"></self-uri>
<abstract abstract-type="precis">
<p>
<italic>Learning to adapt movements to compensate for unexpected perturbations shows savings, or faster readaptation to a previously encountered perturbation. Using a factorial design, we examined how savings is affected by prior experience of similar errors and prior repetition of the action required to eliminate errors. The data show that prior experience of errors is both necessary and sufficient for savings, whereas prior repetition of a successful action is neither necessary nor sufficient for savings</italic>
.</p>
</abstract>
<abstract>
<p>When we move, perturbations to our body or the environment can elicit discrepancies between predicted and actual outcomes. We readily adapt movements to compensate for such discrepancies, and the retention of this learning is evident as savings, or faster readaptation to a previously encountered perturbation. The mechanistic processes contributing to savings, or even the necessary conditions for savings, are not fully understood. One theory suggests that savings requires increased sensitivity to previously experienced errors: when perturbations evoke a sequence of correlated errors, we increase our sensitivity to the errors experienced, which subsequently improves error correction (
<xref rid="B11" ref-type="bibr">Herzfeld et al. 2014</xref>
). An alternative theory suggests that a memory of actions is necessary for savings: when an action becomes associated with successful target acquisition through repetition, that action is more rapidly retrieved at subsequent learning (
<xref rid="B13" ref-type="bibr">Huang et al. 2011</xref>
). In the present study, to better understand the necessary conditions for savings, we tested how savings is affected by prior experience of similar errors and prior repetition of the action required to eliminate errors using a factorial design. Prior experience of errors induced by a visuomotor rotation in the savings block was either prevented at initial learning by gradually removing an oppositely signed perturbation or enforced by abruptly removing the perturbation. Prior repetition of the action required to eliminate errors in the savings block was either deprived or enforced by manipulating target location in preceding trials. The data suggest that prior experience of errors is both necessary and sufficient for savings, whereas prior repetition of a successful action is neither necessary nor sufficient for savings.</p>
</abstract>
<kwd-group>
<kwd>motor adaptation</kwd>
<kwd>motor learning</kwd>
<kwd>savings</kwd>
<kwd>memory of errors</kwd>
<kwd>memory of actions</kwd>
<kwd>repetition</kwd>
<kwd>anterograde interference</kwd>
<kwd>use-dependent plasticity</kwd>
</kwd-group>
<funding-group>
<award-group id="award1">
<funding-source>
<named-content content-type="funder-id">http://doi.org/10.13039/501100000923</named-content>
Department of Industry, Innovation, Science, Research and Tertiary Education, Australian Government | Australian Research Council (ARC)</funding-source>
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<award-id>FT120100391</award-id>
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