Excessive Sensitivity to Uncertain Visual Input in L-DOPA-Induced Dyskinesias in Parkinson’s Disease: Further Implications for Cerebellar Involvement
Identifieur interne : 000981 ( Pmc/Curation ); précédent : 000980; suivant : 000982Excessive Sensitivity to Uncertain Visual Input in L-DOPA-Induced Dyskinesias in Parkinson’s Disease: Further Implications for Cerebellar Involvement
Auteurs : James K. R. Stevenson [Canada] ; Chonho Lee [Singapour] ; Bu-Sung Lee [Singapour] ; Pouria Talebifard [Canada] ; Edna Ty [Canada] ; Kristina Aseeva [Canada] ; Meeko M. K. Oishi [États-Unis] ; Martin J. Mckeown [Canada]Source :
- Frontiers in Neurology [ 1664-2295 ] ; 2014.
Abstract
When faced with visual uncertainty during motor performance, humans rely more on predictive forward models and proprioception and attribute lesser importance to the ambiguous visual feedback. Though disrupted predictive control is typical of patients with cerebellar disease, sensorimotor deficits associated with the involuntary and often unconscious nature of
Url:
DOI: 10.3389/fneur.2014.00008
PubMed: 24550883
PubMed Central: 3912458
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Excessive Sensitivity to Uncertain Visual Input in L-DOPA-Induced Dyskinesias in Parkinson’s Disease: Further Implications for Cerebellar Involvement</title><author><name sortKey="Stevenson, James K R" sort="Stevenson, James K R" uniqKey="Stevenson J" first="James K. R." last="Stevenson">James K. R. Stevenson</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Kinsmen Laboratory of Neurological Research, Department of Neuroscience, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lee, Chonho" sort="Lee, Chonho" uniqKey="Lee C" first="Chonho" last="Lee">Chonho Lee</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Computer Engineering, Nanyang Technological University</institution>,<addr-line>Singapore</addr-line>,<country>Singapore</country></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lee, Bu Sung" sort="Lee, Bu Sung" uniqKey="Lee B" first="Bu-Sung" last="Lee">Bu-Sung Lee</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Computer Engineering, Nanyang Technological University</institution>,<addr-line>Singapore</addr-line>,<country>Singapore</country></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Talebifard, Pouria" sort="Talebifard, Pouria" uniqKey="Talebifard P" first="Pouria" last="Talebifard">Pouria Talebifard</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Electrical and Computer Engineering, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Ty, Edna" sort="Ty, Edna" uniqKey="Ty E" first="Edna" last="Ty">Edna Ty</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Aseeva, Kristina" sort="Aseeva, Kristina" uniqKey="Aseeva K" first="Kristina" last="Aseeva">Kristina Aseeva</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Oishi, Meeko M K" sort="Oishi, Meeko M K" uniqKey="Oishi M" first="Meeko M. K." last="Oishi">Meeko M. K. Oishi</name><affiliation wicri:level="1"><nlm:aff id="aff5"><institution>Department of Electrical and Computer Engineering, University of New Mexico</institution>,<addr-line>Albuquerque, NM</addr-line>,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Mckeown, Martin J" sort="Mckeown, Martin J" uniqKey="Mckeown M" first="Martin J." last="Mckeown">Martin J. Mckeown</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Kinsmen Laboratory of Neurological Research, Department of Neuroscience, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Electrical and Computer Engineering, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24550883</idno><idno type="pmc">3912458</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3912458</idno><idno type="RBID">PMC:3912458</idno><idno type="doi">10.3389/fneur.2014.00008</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000981</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000981</idno><idno type="wicri:Area/Pmc/Curation">000981</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000981</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Excessive Sensitivity to Uncertain Visual Input in L-DOPA-Induced Dyskinesias in Parkinson’s Disease: Further Implications for Cerebellar Involvement</title><author><name sortKey="Stevenson, James K R" sort="Stevenson, James K R" uniqKey="Stevenson J" first="James K. R." last="Stevenson">James K. R. Stevenson</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Kinsmen Laboratory of Neurological Research, Department of Neuroscience, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lee, Chonho" sort="Lee, Chonho" uniqKey="Lee C" first="Chonho" last="Lee">Chonho Lee</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Computer Engineering, Nanyang Technological University</institution>,<addr-line>Singapore</addr-line>,<country>Singapore</country></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lee, Bu Sung" sort="Lee, Bu Sung" uniqKey="Lee B" first="Bu-Sung" last="Lee">Bu-Sung Lee</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Computer Engineering, Nanyang Technological University</institution>,<addr-line>Singapore</addr-line>,<country>Singapore</country></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Talebifard, Pouria" sort="Talebifard, Pouria" uniqKey="Talebifard P" first="Pouria" last="Talebifard">Pouria Talebifard</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Electrical and Computer Engineering, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Ty, Edna" sort="Ty, Edna" uniqKey="Ty E" first="Edna" last="Ty">Edna Ty</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Aseeva, Kristina" sort="Aseeva, Kristina" uniqKey="Aseeva K" first="Kristina" last="Aseeva">Kristina Aseeva</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Oishi, Meeko M K" sort="Oishi, Meeko M K" uniqKey="Oishi M" first="Meeko M. K." last="Oishi">Meeko M. K. Oishi</name><affiliation wicri:level="1"><nlm:aff id="aff5"><institution>Department of Electrical and Computer Engineering, University of New Mexico</institution>,<addr-line>Albuquerque, NM</addr-line>,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Mckeown, Martin J" sort="Mckeown, Martin J" uniqKey="Mckeown M" first="Martin J." last="Mckeown">Martin J. Mckeown</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Kinsmen Laboratory of Neurological Research, Department of Neuroscience, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Electrical and Computer Engineering, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Frontiers in Neurology</title><idno type="eISSN">1664-2295</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>When faced with visual uncertainty during motor performance, humans rely more on predictive forward models and proprioception and attribute lesser importance to the ambiguous visual feedback. Though disrupted predictive control is typical of patients with cerebellar disease, sensorimotor deficits associated with the involuntary and often unconscious nature of <sc>l</sc>-DOPA-induced dyskinesias in Parkinson’s disease (PD) suggests dyskinetic subjects may also demonstrate impaired predictive motor control.</p><p><bold>Methods:</bold> We investigated the motor performance of 9 dyskinetic and 10 non-dyskinetic PD subjects on and off <sc>l</sc>-DOPA, and of 10 age-matched control subjects, during a large-amplitude, overlearned, visually guided tracking task. Ambiguous visual feedback was introduced by adding “jitter” to a moving target that followed a Lissajous pattern. Root mean square (RMS) tracking error was calculated, and ANOVA, robust multivariate linear regression, and linear dynamical system analyses were used to determine the contribution of speed and ambiguity to tracking performance.</p><p><bold>Results:</bold> Increasing target ambiguity and speed contributed significantly more to the RMS error of dyskinetic subjects off medication. <sc>l</sc>-DOPA improved the RMS tracking performance of both PD groups. At higher speeds, controls and PDs without dyskinesia were able to effectively de-weight ambiguous visual information.</p><p><bold>Conclusion:</bold> PDs’ visually guided motor performance degrades with visual jitter and speed of movement to a greater degree compared to age-matched controls. However, there are fundamental differences in PDs with and without dyskinesia: subjects without dyskinesia are generally slow, and less responsive to dynamic changes in motor task requirements, but in PDs with dyskinesia, there was a trade-off between overall performance and inappropriate reliance on ambiguous visual feedback. This is likely associated with functional changes in posterior parietal–ponto–cerebellar pathways.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Wolpert, Dm" uniqKey="Wolpert D">DM Wolpert</name></author><author><name sortKey="Ghahramani, Z" uniqKey="Ghahramani Z">Z Ghahramani</name></author><author><name sortKey="Jordan, Mi" uniqKey="Jordan M">MI Jordan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gritsenko, V" uniqKey="Gritsenko V">V Gritsenko</name></author><author><name sortKey="Yakovenko, S" uniqKey="Yakovenko S">S Yakovenko</name></author><author><name sortKey="Kalaska, Jf" uniqKey="Kalaska J">JF Kalaska</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kuo, Ad" uniqKey="Kuo A">AD Kuo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Merfeld, Dm" uniqKey="Merfeld D">DM Merfeld</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Neurol</journal-id><journal-id journal-id-type="iso-abbrev">Front Neurol</journal-id><journal-id journal-id-type="publisher-id">Front. Neurol.</journal-id><journal-title-group><journal-title>Frontiers in Neurology</journal-title></journal-title-group><issn pub-type="epub">1664-2295</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24550883</article-id><article-id pub-id-type="pmc">3912458</article-id><article-id pub-id-type="doi">10.3389/fneur.2014.00008</article-id><article-categories><subj-group subj-group-type="heading"><subject>Neuroscience</subject><subj-group><subject>Original Research</subject></subj-group></subj-group></article-categories><title-group><article-title>Excessive Sensitivity to Uncertain Visual Input in L-DOPA-Induced Dyskinesias in Parkinson’s Disease: Further Implications for Cerebellar Involvement</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Stevenson</surname><given-names>James K. R.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/129106"></uri></contrib><contrib contrib-type="author"><name><surname>Lee</surname><given-names>Chonho</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/129043"></uri></contrib><contrib contrib-type="author"><name><surname>Lee</surname><given-names>Bu-Sung</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>TalebiFard</surname><given-names>Pouria</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ty</surname><given-names>Edna</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Aseeva</surname><given-names>Kristina</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/124519"></uri></contrib><contrib contrib-type="author"><name><surname>Oishi</surname><given-names>Meeko M. K.</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/95643"></uri></contrib><contrib contrib-type="author"><name><surname>McKeown</surname><given-names>Martin J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="corresp" rid="cor1">*</xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/9879"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Kinsmen Laboratory of Neurological Research, Department of Neuroscience, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></aff><aff id="aff2"><sup>2</sup><institution>School of Computer Engineering, Nanyang Technological University</institution>,<addr-line>Singapore</addr-line>,<country>Singapore</country></aff><aff id="aff3"><sup>3</sup><institution>Department of Electrical and Computer Engineering, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></aff><aff id="aff4"><sup>4</sup><institution>Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia</institution>,<addr-line>Vancouver, BC</addr-line>,<country>Canada</country></aff><aff id="aff5"><sup>5</sup><institution>Department of Electrical and Computer Engineering, University of New Mexico</institution>,<addr-line>Albuquerque, NM</addr-line>,<country>USA</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Antonio Cerasa, Consiglio Nazionale delle Ricerche, Italy</p></fn><fn fn-type="edited-by"><p>Reviewed by: Giulia Donzuso, University “Magna Graecia” di Catanzaro, Italy; Gennarina Arabia, University “Magna Graecia” di Catanzaro, Italy</p></fn><corresp content-type="corresp" id="cor1">*Correspondence: Martin J. McKeown, Pacific Parkinson’s Research Centre, University Hospital, University of British Columbia, Purdy Pavilion, 2221 Wesbrook Mall, Vancouver, BC V6T 2B5, Canada e-mail: <email>martin.mckeown@ubc.ca</email></corresp><fn fn-type="other" id="fn001"><p>This article was submitted to Movement Disorders, a section of the journal Frontiers in Neurology.</p></fn></author-notes><pub-date pub-type="epreprint"><day>21</day><month>12</month><year>2013</year></pub-date><pub-date pub-type="epub"><day>04</day><month>2</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>5</volume><elocation-id>8</elocation-id><history><date date-type="received"><day>01</day><month>12</month><year>2013</year></date><date date-type="accepted"><day>10</day><month>1</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 Stevenson, Lee, Lee, TalebiFard, Ty, Aseeva, Oishi and McKeown.</copyright-statement><copyright-year>2014</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>When faced with visual uncertainty during motor performance, humans rely more on predictive forward models and proprioception and attribute lesser importance to the ambiguous visual feedback. Though disrupted predictive control is typical of patients with cerebellar disease, sensorimotor deficits associated with the involuntary and often unconscious nature of <sc>l</sc>-DOPA-induced dyskinesias in Parkinson’s disease (PD) suggests dyskinetic subjects may also demonstrate impaired predictive motor control.</p><p><bold>Methods:</bold> We investigated the motor performance of 9 dyskinetic and 10 non-dyskinetic PD subjects on and off <sc>l</sc>-DOPA, and of 10 age-matched control subjects, during a large-amplitude, overlearned, visually guided tracking task. Ambiguous visual feedback was introduced by adding “jitter” to a moving target that followed a Lissajous pattern. Root mean square (RMS) tracking error was calculated, and ANOVA, robust multivariate linear regression, and linear dynamical system analyses were used to determine the contribution of speed and ambiguity to tracking performance.</p><p><bold>Results:</bold> Increasing target ambiguity and speed contributed significantly more to the RMS error of dyskinetic subjects off medication. <sc>l</sc>-DOPA improved the RMS tracking performance of both PD groups. At higher speeds, controls and PDs without dyskinesia were able to effectively de-weight ambiguous visual information.</p><p><bold>Conclusion:</bold> PDs’ visually guided motor performance degrades with visual jitter and speed of movement to a greater degree compared to age-matched controls. However, there are fundamental differences in PDs with and without dyskinesia: subjects without dyskinesia are generally slow, and less responsive to dynamic changes in motor task requirements, but in PDs with dyskinesia, there was a trade-off between overall performance and inappropriate reliance on ambiguous visual feedback. This is likely associated with functional changes in posterior parietal–ponto–cerebellar pathways.</p></abstract><kwd-group><kwd><sc>l</sc>-DOPA-induced dyskinesias</kwd><kwd>Parkinson’s disease</kwd><kwd>dynamical system models</kwd><kwd>visually guided tracking</kwd><kwd>visual uncertainty</kwd></kwd-group><counts><fig-count count="6"></fig-count><table-count count="5"></table-count><equation-count count="1"></equation-count><ref-count count="99"></ref-count><page-count count="13"></page-count><word-count count="10330"></word-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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