Reward processing abnormalities in Parkinson's disease
Identifieur interne : 001980 ( Main/Corpus ); précédent : 001979; suivant : 001981Reward processing abnormalities in Parkinson's disease
Auteurs : Dimitrios Kapogiannis ; Eric Mooshagian ; Paul Campion ; Jordan Grafman ; Trelawny J. Zimmermann ; Kelsey C. Ladt ; Eric M. WassermannSource :
- Movement Disorders [ 0885-3185 ] ; 2011-07.
English descriptors
Abstract
The primary motor cortex is important for motor learning and response selection, functions that require information on the expected and actual outcomes of behavior. Therefore, it should receive signals related to reward. Pathways from reward centers to motor cortex exist in primates. Previously, we showed that gamma aminobutyric acid–A–mediated inhibition in the motor cortex, measured by paired transcranial magnetic stimulation, changes with expectation and uncertainty of money rewards generated by a slot machine simulation. We examined the role of dopamine in this phenomenon by testing 13 mildly affected patients with Parkinson's disease, off and on dopaminergic medications, and 13 healthy, age‐matched controls. Consistent with a dopaminergic mechanism, reward expectation or predictability modulated the response to paired transcranial magnetic stimulation in controls, but not in unmedicated patients. A single dose of pramipexole restored this effect of reward, mainly by increasing the paired transcranial magnetic stimulation response amplitude during low expectation. Levodopa produced no such effect. Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. The cortical response to reward expectation may represent an endophenotype for risk‐taking behavior in patients on agonist treatment. © 2011 Movement Disorder Society
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DOI: 10.1002/mds.23701
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Therefore, it should receive signals related to reward. Pathways from reward centers to motor cortex exist in primates. Previously, we showed that gamma aminobutyric acid–A–mediated inhibition in the motor cortex, measured by paired transcranial magnetic stimulation, changes with expectation and uncertainty of money rewards generated by a slot machine simulation. We examined the role of dopamine in this phenomenon by testing 13 mildly affected patients with Parkinson's disease, off and on dopaminergic medications, and 13 healthy, age‐matched controls. Consistent with a dopaminergic mechanism, reward expectation or predictability modulated the response to paired transcranial magnetic stimulation in controls, but not in unmedicated patients. A single dose of pramipexole restored this effect of reward, mainly by increasing the paired transcranial magnetic stimulation response amplitude during low expectation. Levodopa produced no such effect. Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. The cortical response to reward expectation may represent an endophenotype for risk‐taking behavior in patients on agonist treatment. © 2011 Movement Disorder Society</div></front></TEI><istex><corpusName>wiley</corpusName><author><json:item><name>Dimitrios Kapogiannis MD</name><affiliations><json:string>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string><json:string>Clinical Research Branch, National Institute on Aging, National Institutes of Health, Baltimore, Maryland, USA</json:string></affiliations></json:item><json:item><name>Eric Mooshagian PhD</name><affiliations><json:string>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string><json:string>Center for Neuroscience and Regenerative Medicine, Uniformed Services University of Health Sciences, Henry M. Jackson Foundation, Rockville, Maryland, USA</json:string></affiliations></json:item><json:item><name>Paul Campion MD</name><affiliations><json:string>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string></affiliations></json:item><json:item><name>Jordan Grafman PhD</name><affiliations><json:string>Cognitive Neuroscience Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string></affiliations></json:item><json:item><name>Trelawny J. Zimmermann MS</name><affiliations><json:string>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string></affiliations></json:item><json:item><name>Kelsey C. Ladt BS</name><affiliations><json:string>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string></affiliations></json:item><json:item><name>Eric M. Wassermann MD</name><affiliations><json:string>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</json:string></affiliations></json:item></author><subject><json:item><lang><json:string>eng</json:string></lang><value>transcranial magnetic stimulation</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>dopamine</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>gambling</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>motor cortex</value></json:item></subject><articleId><json:string>MDS23701</json:string></articleId><language><json:string>eng</json:string></language><abstract>The primary motor cortex is important for motor learning and response selection, functions that require information on the expected and actual outcomes of behavior. Therefore, it should receive signals related to reward. Pathways from reward centers to motor cortex exist in primates. Previously, we showed that gamma aminobutyric acid–A–mediated inhibition in the motor cortex, measured by paired transcranial magnetic stimulation, changes with expectation and uncertainty of money rewards generated by a slot machine simulation. We examined the role of dopamine in this phenomenon by testing 13 mildly affected patients with Parkinson's disease, off and on dopaminergic medications, and 13 healthy, age‐matched controls. Consistent with a dopaminergic mechanism, reward expectation or predictability modulated the response to paired transcranial magnetic stimulation in controls, but not in unmedicated patients. A single dose of pramipexole restored this effect of reward, mainly by increasing the paired transcranial magnetic stimulation response amplitude during low expectation. Levodopa produced no such effect. Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. 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Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. The cortical response to reward expectation may represent an endophenotype for risk‐taking behavior in patients on agonist treatment. © 2011 Movement Disorder Society</p></abstract><textClass xml:lang="en"><keywords scheme="keyword"><list><head>Keywords</head><item><term>transcranial magnetic stimulation</term></item><item><term>dopamine</term></item><item><term>gambling</term></item><item><term>motor cortex</term></item></list></keywords></textClass><textClass><keywords scheme="Journal Subject"><list><head>article category</head><item><term>Research Article</term></item></list></keywords></textClass></profileDesc><revisionDesc><change when="2010-10-01">Received</change><change when="2011-02-07">Registration</change><change when="2011-07">Published</change></revisionDesc></teiHeader></istex:fulltextTEI><json:item><original>false</original><mimetype>text/plain</mimetype><extension>txt</extension><uri>https://api.istex.fr/document/C990B442102A4540A02BEAE1B911A00849D27FEC/fulltext/txt</uri></json:item></fulltext><metadata><istex:metadataXml wicri:clean="Wiley, elements deleted: body"><istex:xmlDeclaration>version="1.0" encoding="UTF-8" standalone="yes"</istex:xmlDeclaration><istex:document><component version="2.0" type="serialArticle" xml:lang="en"><header><publicationMeta level="product"><publisherInfo><publisherName>Wiley Subscription Services, Inc., A Wiley Company</publisherName><publisherLoc>Hoboken</publisherLoc></publisherInfo><doi registered="yes">10.1002/(ISSN)1531-8257</doi><issn type="print">0885-3185</issn><issn type="electronic">1531-8257</issn><idGroup><id type="product" value="MDS"></id></idGroup><titleGroup><title type="main" xml:lang="en" sort="MOVEMENT DISORDERS">Movement Disorders</title><title type="short">Mov. 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Jackson Foundation, Rockville, Maryland, USA</unparsedAffiliation></affiliation><affiliation xml:id="af4" countryCode="US" type="organization"><unparsedAffiliation>Cognitive Neuroscience Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</unparsedAffiliation></affiliation></affiliationGroup><keywordGroup xml:lang="en" type="author"><keyword xml:id="kwd1">transcranial magnetic stimulation</keyword><keyword xml:id="kwd2">dopamine</keyword><keyword xml:id="kwd3">gambling</keyword><keyword xml:id="kwd4">motor cortex</keyword></keywordGroup><abstractGroup><abstract type="main" xml:lang="en"><title type="main">Abstract</title><p>The primary motor cortex is important for motor learning and response selection, functions that require information on the expected and actual outcomes of behavior. Therefore, it should receive signals related to reward. Pathways from reward centers to motor cortex exist in primates. Previously, we showed that gamma aminobutyric acid–A–mediated inhibition in the motor cortex, measured by paired transcranial magnetic stimulation, changes with expectation and uncertainty of money rewards generated by a slot machine simulation. We examined the role of dopamine in this phenomenon by testing 13 mildly affected patients with Parkinson's disease, off and on dopaminergic medications, and 13 healthy, age‐matched controls. Consistent with a dopaminergic mechanism, reward expectation or predictability modulated the response to paired transcranial magnetic stimulation in controls, but not in unmedicated patients. A single dose of pramipexole restored this effect of reward, mainly by increasing the paired transcranial magnetic stimulation response amplitude during low expectation. Levodopa produced no such effect. Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. The cortical response to reward expectation may represent an endophenotype for risk‐taking behavior in patients on agonist treatment. © 2011 Movement Disorder Society</p></abstract></abstractGroup></contentMeta><noteGroup><note xml:id="fn1"><p><b>Relevant conflicts of interest/financial disclosures:</b> Nothing to report.</p></note><note xml:id="fn2"><p>Funding for this work came exclusively from the Clinical Neuroscience Program of the National Institute of Neurological Disorders and Stroke and the Intramural Research Program of the National Institute on Aging (to Dr. Kapogiannis), National Institutes of Health, and the Center for Neuroscience and Regenerative Medicine at the Uniformed Service University of the Health Sciences, via the Henry Jackson foundation (to Dr. Mooshagian).</p></note><note xml:id="fn3"><p>Full financial disclosures and author roles may be found in the online version of this article.</p></note></noteGroup></header></component></istex:document></istex:metadataXml><mods version="3.6"><titleInfo lang="en"><title>Reward processing abnormalities in Parkinson's disease</title></titleInfo><titleInfo type="abbreviated" lang="en"><title>Reward Processing Abnormalities in PD</title></titleInfo><titleInfo type="alternative" contentType="CDATA" lang="en"><title>Reward processing abnormalities in Parkinson's disease</title></titleInfo><name type="personal"><namePart type="given">Dimitrios</namePart><namePart type="family">Kapogiannis</namePart><namePart type="termsOfAddress">MD</namePart><affiliation>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><affiliation>Clinical Research Branch, National Institute on Aging, National Institutes of Health, Baltimore, Maryland, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Eric</namePart><namePart type="family">Mooshagian</namePart><namePart type="termsOfAddress">PhD</namePart><affiliation>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><affiliation>Center for Neuroscience and Regenerative Medicine, Uniformed Services University of Health Sciences, Henry M. Jackson Foundation, Rockville, Maryland, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Paul</namePart><namePart type="family">Campion</namePart><namePart type="termsOfAddress">MD</namePart><affiliation>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Jordan</namePart><namePart type="family">Grafman</namePart><namePart type="termsOfAddress">PhD</namePart><affiliation>Cognitive Neuroscience Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Trelawny J.</namePart><namePart type="family">Zimmermann</namePart><namePart type="termsOfAddress">MS</namePart><affiliation>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Kelsey C.</namePart><namePart type="family">Ladt</namePart><namePart type="termsOfAddress">BS</namePart><affiliation>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Eric M.</namePart><namePart type="family">Wassermann</namePart><namePart type="termsOfAddress">MD</namePart><affiliation>Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA</affiliation><description>Correspondence: 10 Center Dr., MSC 1440, Bethesda, MD 20892‐1440, USA</description><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="article" displayLabel="article"></genre><originInfo><publisher>Wiley Subscription Services, Inc., A Wiley Company</publisher><place><placeTerm type="text">Hoboken</placeTerm></place><dateIssued encoding="w3cdtf">2011-07</dateIssued><dateCaptured encoding="w3cdtf">2010-10-01</dateCaptured><dateValid encoding="w3cdtf">2011-02-07</dateValid><copyrightDate encoding="w3cdtf">2011</copyrightDate></originInfo><language><languageTerm type="code" authority="rfc3066">en</languageTerm><languageTerm type="code" authority="iso639-2b">eng</languageTerm></language><physicalDescription><internetMediaType>text/html</internetMediaType><extent unit="figures">4</extent><extent unit="tables">1</extent><extent unit="references">40</extent><extent unit="words">5333</extent></physicalDescription><abstract lang="en">The primary motor cortex is important for motor learning and response selection, functions that require information on the expected and actual outcomes of behavior. Therefore, it should receive signals related to reward. Pathways from reward centers to motor cortex exist in primates. Previously, we showed that gamma aminobutyric acid–A–mediated inhibition in the motor cortex, measured by paired transcranial magnetic stimulation, changes with expectation and uncertainty of money rewards generated by a slot machine simulation. We examined the role of dopamine in this phenomenon by testing 13 mildly affected patients with Parkinson's disease, off and on dopaminergic medications, and 13 healthy, age‐matched controls. Consistent with a dopaminergic mechanism, reward expectation or predictability modulated the response to paired transcranial magnetic stimulation in controls, but not in unmedicated patients. A single dose of pramipexole restored this effect of reward, mainly by increasing the paired transcranial magnetic stimulation response amplitude during low expectation. Levodopa produced no such effect. Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. The cortical response to reward expectation may represent an endophenotype for risk‐taking behavior in patients on agonist treatment. © 2011 Movement Disorder Society</abstract><note type="content">*Relevant conflicts of interest/financial disclosures: Nothing to report.</note><note type="content">*Funding for this work came exclusively from the Clinical Neuroscience Program of the National Institute of Neurological Disorders and Stroke and the Intramural Research Program of the National Institute on Aging (to Dr. Kapogiannis), National Institutes of Health, and the Center for Neuroscience and Regenerative Medicine at the Uniformed Service University of the Health Sciences, via the Henry Jackson foundation (to Dr. Mooshagian).</note><note type="content">*Full financial disclosures and author roles may be found in the online version of this article.</note><subject lang="en"><genre>Keywords</genre><topic>transcranial magnetic stimulation</topic><topic>dopamine</topic><topic>gambling</topic><topic>motor cortex</topic></subject><relatedItem type="host"><titleInfo><title>Movement Disorders</title></titleInfo><titleInfo type="abbreviated"><title>Mov. 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