Role of Basal Ganglia Circuits in Resisting Interference by Distracters: A swLORETA Study
Identifieur interne : 000571 ( Pmc/Checkpoint ); précédent : 000570; suivant : 000572Role of Basal Ganglia Circuits in Resisting Interference by Distracters: A swLORETA Study
Auteurs : Perrine Bocquillon [France] ; Jean-Louis Bourriez [France] ; Ernesto Palmero-Soler [Allemagne] ; Alain Destée [France] ; Luc Defebvre [France] ; Philippe Derambure [France] ; Kathy Dujardin [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2012.
Abstract
The selection of task-relevant information requires both the focalization of attention on the task and resistance to interference from irrelevant stimuli. Both mechanisms rely on a dorsal frontoparietal network, while focalization additionally involves a ventral frontoparietal network. The role of subcortical structures in attention is less clear, despite the fact that the striatum interacts significantly with the frontal cortex via frontostriatal loops. One means of investigating the basal ganglia's contributions to attention is to examine the features of P300 components (i.e. amplitude, latency, and generators) in patients with basal ganglia damage (such as in Parkinson's disease (PD), in which attention is often impaired). Three-stimulus oddball paradigms can be used to study distracter-elicited and target-elicited P300 subcomponents.
In order to compare distracter- and target-elicited P300 components, high-density (128-channel) electroencephalograms were recorded during a three-stimulus visual oddball paradigm in 15 patients with early PD and 15 matched healthy controls. For each subject, the P300 sources were localized using standardized weighted low-resolution electromagnetic tomography (swLORETA). Comparative analyses (one-sample and two-sample t-tests) were performed using SPM5® software. The swLORETA analyses showed that PD patients displayed fewer dorsolateral prefrontal (DLPF) distracter-P300 generators but no significant differences in target-elicited P300 sources; this suggests dysfunction of the DLPF cortex when the executive frontostriatal loop is disrupted by basal ganglia damage.
Our results suggest that the cortical attention frontoparietal networks (mainly the dorsal one) are modulated by the basal ganglia. Disruption of this network in PD impairs resistance to distracters, which results in attention disorders.
Url:
DOI: 10.1371/journal.pone.0034239
PubMed: 22470542
PubMed Central: 3314607
Affiliations:
- Allemagne, France
- Berlin, Hauts-de-France, Nord-Pas-de-Calais
- Berlin, Lille
- Université Lille 2, Université Lille Nord de France
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<country xml:lang="fr">France</country>
<wicri:regionArea>Clinical Neurophysiology Department, Lille University Medical Center, Lille</wicri:regionArea>
<placeName><region type="region">Hauts-de-France</region>
<region type="old region">Nord-Pas-de-Calais</region>
<settlement type="city">Lille</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Dujardin, Kathy" sort="Dujardin, Kathy" uniqKey="Dujardin K" first="Kathy" last="Dujardin">Kathy Dujardin</name>
<affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>University of Lille Nord de France, Lille, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>University of Lille Nord de France, Lille</wicri:regionArea>
<placeName><region type="region">Hauts-de-France</region>
<region type="old region">Nord-Pas-de-Calais</region>
<settlement type="city">Lille</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Lab. Neurosciences Fonctionnelles et Pathologies, Lille, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Lab. Neurosciences Fonctionnelles et Pathologies, Lille</wicri:regionArea>
<placeName><region type="region">Hauts-de-France</region>
<region type="old region">Nord-Pas-de-Calais</region>
<settlement type="city">Lille</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>Neurology and Movement Disorders Department, Lille University Medical Center, Lille, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Neurology and Movement Disorders Department, Lille University Medical Center, Lille</wicri:regionArea>
<placeName><region type="region">Hauts-de-France</region>
<region type="old region">Nord-Pas-de-Calais</region>
<settlement type="city">Lille</settlement>
</placeName>
</affiliation>
</author>
</analytic>
<series><title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint><date when="2012">2012</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
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<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>The selection of task-relevant information requires both the focalization of attention on the task and resistance to interference from irrelevant stimuli. Both mechanisms rely on a dorsal frontoparietal network, while focalization additionally involves a ventral frontoparietal network. The role of subcortical structures in attention is less clear, despite the fact that the striatum interacts significantly with the frontal cortex via frontostriatal loops. One means of investigating the basal ganglia's contributions to attention is to examine the features of P300 components (i.e. amplitude, latency, and generators) in patients with basal ganglia damage (such as in Parkinson's disease (PD), in which attention is often impaired). Three-stimulus oddball paradigms can be used to study distracter-elicited and target-elicited P300 subcomponents.</p>
</sec>
<sec><title>Methodology/Principal Findings</title>
<p>In order to compare distracter- and target-elicited P300 components, high-density (128-channel) electroencephalograms were recorded during a three-stimulus visual oddball paradigm in 15 patients with early PD and 15 matched healthy controls. For each subject, the P300 sources were localized using standardized weighted low-resolution electromagnetic tomography (swLORETA). Comparative analyses (one-sample and two-sample t-tests) were performed using SPM5® software. The swLORETA analyses showed that PD patients displayed fewer dorsolateral prefrontal (DLPF) distracter-P300 generators but no significant differences in target-elicited P300 sources; this suggests dysfunction of the DLPF cortex when the executive frontostriatal loop is disrupted by basal ganglia damage.</p>
</sec>
<sec><title>Conclusions/Significance</title>
<p>Our results suggest that the cortical attention frontoparietal networks (mainly the dorsal one) are modulated by the basal ganglia. Disruption of this network in PD impairs resistance to distracters, which results in attention disorders.</p>
</sec>
</div>
</front>
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<author><name sortKey="Davidsdottir, S" uniqKey="Davidsdottir S">S Davidsdottir</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Flowers, Ka" uniqKey="Flowers K">KA Flowers</name>
</author>
<author><name sortKey="Robertson, C" uniqKey="Robertson C">C Robertson</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Sawaki, R" uniqKey="Sawaki R">R Sawaki</name>
</author>
<author><name sortKey="Katayama, J" uniqKey="Katayama J">J Katayama</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Van Den Eeden, Sk" uniqKey="Van Den Eeden S">SK Van Den Eeden</name>
</author>
<author><name sortKey="Tanner, Cm" uniqKey="Tanner C">CM Tanner</name>
</author>
<author><name sortKey="Bernstein, Al" uniqKey="Bernstein A">AL Bernstein</name>
</author>
<author><name sortKey="Fross, Rd" uniqKey="Fross R">RD Fross</name>
</author>
<author><name sortKey="Leimpeter, A" uniqKey="Leimpeter A">A Leimpeter</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="De Lau, Lm" uniqKey="De Lau L">LM de Lau</name>
</author>
<author><name sortKey="Giesbergen, Pc" uniqKey="Giesbergen P">PC Giesbergen</name>
</author>
<author><name sortKey="De Rijk, Mc" uniqKey="De Rijk M">MC de Rijk</name>
</author>
<author><name sortKey="Hofman, A" uniqKey="Hofman A">A Hofman</name>
</author>
<author><name sortKey="Koudstaal, Pj" uniqKey="Koudstaal P">PJ Koudstaal</name>
</author>
</analytic>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22470542</article-id>
<article-id pub-id-type="pmc">3314607</article-id>
<article-id pub-id-type="publisher-id">PONE-D-11-21199</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0034239</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Anatomy and Physiology</subject>
<subj-group><subject>Neurological System</subject>
</subj-group>
</subj-group>
<subj-group><subject>Neuroscience</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject>
<subj-group><subject>Anatomy and Physiology</subject>
<subj-group><subject>Neurological System</subject>
</subj-group>
</subj-group>
<subj-group><subject>Mental Health</subject>
<subj-group><subject>Psychology</subject>
</subj-group>
</subj-group>
<subj-group><subject>Neurology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Role of Basal Ganglia Circuits in Resisting Interference by Distracters: A swLORETA Study</article-title>
<alt-title alt-title-type="running-head">Role of Basal Ganglia Circuits in Attention</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Bocquillon</surname>
<given-names>Perrine</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bourriez</surname>
<given-names>Jean-Louis</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Palmero-Soler</surname>
<given-names>Ernesto</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Destée</surname>
<given-names>Alain</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Defebvre</surname>
<given-names>Luc</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Derambure</surname>
<given-names>Philippe</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dujardin</surname>
<given-names>Kathy</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>University of Lille Nord de France, Lille, France</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Lab. Neurosciences Fonctionnelles et Pathologies, Lille, France</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Clinical Neurophysiology Department, Lille University Medical Center, Lille, France</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Eemagine Medical Imaging Solutions GmbH, Berlin, Germany</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>Neurology and Movement Disorders Department, Lille University Medical Center, Lille, France</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Zang</surname>
<given-names>Yu-Feng</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">Hangzhou Normal University, China</aff>
<author-notes><corresp id="cor1">* E-mail: <email>pebocq@hotmail.fr</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: PB JLB EP PD KD. Performed the experiments: PB KD. Analyzed the data: PB EP KD. Contributed reagents/materials/analysis tools: PB JLB EP KD. Wrote the paper: PB JLB EP KD LD PD AD.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>28</day>
<month>3</month>
<year>2012</year>
</pub-date>
<volume>7</volume>
<issue>3</issue>
<elocation-id>e34239</elocation-id>
<history><date date-type="received"><day>27</day>
<month>10</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>24</day>
<month>2</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Bocquillon et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</copyright-statement>
<copyright-year>2012</copyright-year>
</permissions>
<abstract><sec><title>Background</title>
<p>The selection of task-relevant information requires both the focalization of attention on the task and resistance to interference from irrelevant stimuli. Both mechanisms rely on a dorsal frontoparietal network, while focalization additionally involves a ventral frontoparietal network. The role of subcortical structures in attention is less clear, despite the fact that the striatum interacts significantly with the frontal cortex via frontostriatal loops. One means of investigating the basal ganglia's contributions to attention is to examine the features of P300 components (i.e. amplitude, latency, and generators) in patients with basal ganglia damage (such as in Parkinson's disease (PD), in which attention is often impaired). Three-stimulus oddball paradigms can be used to study distracter-elicited and target-elicited P300 subcomponents.</p>
</sec>
<sec><title>Methodology/Principal Findings</title>
<p>In order to compare distracter- and target-elicited P300 components, high-density (128-channel) electroencephalograms were recorded during a three-stimulus visual oddball paradigm in 15 patients with early PD and 15 matched healthy controls. For each subject, the P300 sources were localized using standardized weighted low-resolution electromagnetic tomography (swLORETA). Comparative analyses (one-sample and two-sample t-tests) were performed using SPM5® software. The swLORETA analyses showed that PD patients displayed fewer dorsolateral prefrontal (DLPF) distracter-P300 generators but no significant differences in target-elicited P300 sources; this suggests dysfunction of the DLPF cortex when the executive frontostriatal loop is disrupted by basal ganglia damage.</p>
</sec>
<sec><title>Conclusions/Significance</title>
<p>Our results suggest that the cortical attention frontoparietal networks (mainly the dorsal one) are modulated by the basal ganglia. Disruption of this network in PD impairs resistance to distracters, which results in attention disorders.</p>
</sec>
</abstract>
<counts><page-count count="12"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>France</li>
</country>
<region><li>Berlin</li>
<li>Hauts-de-France</li>
<li>Nord-Pas-de-Calais</li>
</region>
<settlement><li>Berlin</li>
<li>Lille</li>
</settlement>
<orgName><li>Université Lille 2</li>
<li>Université Lille Nord de France</li>
</orgName>
</list>
<tree><country name="France"><region name="Hauts-de-France"><name sortKey="Bocquillon, Perrine" sort="Bocquillon, Perrine" uniqKey="Bocquillon P" first="Perrine" last="Bocquillon">Perrine Bocquillon</name>
</region>
<name sortKey="Bocquillon, Perrine" sort="Bocquillon, Perrine" uniqKey="Bocquillon P" first="Perrine" last="Bocquillon">Perrine Bocquillon</name>
<name sortKey="Bocquillon, Perrine" sort="Bocquillon, Perrine" uniqKey="Bocquillon P" first="Perrine" last="Bocquillon">Perrine Bocquillon</name>
<name sortKey="Bourriez, Jean Louis" sort="Bourriez, Jean Louis" uniqKey="Bourriez J" first="Jean-Louis" last="Bourriez">Jean-Louis Bourriez</name>
<name sortKey="Bourriez, Jean Louis" sort="Bourriez, Jean Louis" uniqKey="Bourriez J" first="Jean-Louis" last="Bourriez">Jean-Louis Bourriez</name>
<name sortKey="Defebvre, Luc" sort="Defebvre, Luc" uniqKey="Defebvre L" first="Luc" last="Defebvre">Luc Defebvre</name>
<name sortKey="Defebvre, Luc" sort="Defebvre, Luc" uniqKey="Defebvre L" first="Luc" last="Defebvre">Luc Defebvre</name>
<name sortKey="Defebvre, Luc" sort="Defebvre, Luc" uniqKey="Defebvre L" first="Luc" last="Defebvre">Luc Defebvre</name>
<name sortKey="Derambure, Philippe" sort="Derambure, Philippe" uniqKey="Derambure P" first="Philippe" last="Derambure">Philippe Derambure</name>
<name sortKey="Derambure, Philippe" sort="Derambure, Philippe" uniqKey="Derambure P" first="Philippe" last="Derambure">Philippe Derambure</name>
<name sortKey="Derambure, Philippe" sort="Derambure, Philippe" uniqKey="Derambure P" first="Philippe" last="Derambure">Philippe Derambure</name>
<name sortKey="Destee, Alain" sort="Destee, Alain" uniqKey="Destee A" first="Alain" last="Destée">Alain Destée</name>
<name sortKey="Destee, Alain" sort="Destee, Alain" uniqKey="Destee A" first="Alain" last="Destée">Alain Destée</name>
<name sortKey="Dujardin, Kathy" sort="Dujardin, Kathy" uniqKey="Dujardin K" first="Kathy" last="Dujardin">Kathy Dujardin</name>
<name sortKey="Dujardin, Kathy" sort="Dujardin, Kathy" uniqKey="Dujardin K" first="Kathy" last="Dujardin">Kathy Dujardin</name>
<name sortKey="Dujardin, Kathy" sort="Dujardin, Kathy" uniqKey="Dujardin K" first="Kathy" last="Dujardin">Kathy Dujardin</name>
</country>
<country name="Allemagne"><region name="Berlin"><name sortKey="Palmero Soler, Ernesto" sort="Palmero Soler, Ernesto" uniqKey="Palmero Soler E" first="Ernesto" last="Palmero-Soler">Ernesto Palmero-Soler</name>
</region>
</country>
</tree>
</affiliations>
</record>
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