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Cognitive performance in healthy older adults relates to spontaneous switching between states of functional connectivity during rest

Identifieur interne : 000392 ( Pmc/Checkpoint ); précédent : 000391; suivant : 000393

Cognitive performance in healthy older adults relates to spontaneous switching between states of functional connectivity during rest

Auteurs : Joana Cabral [Royaume-Uni, Danemark] ; Diego Vidaurre [Royaume-Uni] ; Paulo Marques [Portugal] ; Ricardo Magalhães [Portugal] ; Pedro Silva Moreira [Portugal] ; José Miguel Soares [Portugal] ; Gustavo Deco [Espagne, Allemagne, Australie] ; Nuno Sousa [Portugal] ; Morten L. Kringelbach [Royaume-Uni, Danemark, France]

Source :

RBID : PMC:5506029

Abstract

Growing evidence has shown that brain activity at rest slowly wanders through a repertoire of different states, where whole-brain functional connectivity (FC) temporarily settles into distinct FC patterns. Nevertheless, the functional role of resting-state activity remains unclear. Here, we investigate how the switching behavior of resting-state FC relates with cognitive performance in healthy older adults. We analyse resting-state fMRI data from 98 healthy adults previously categorized as being among the best or among the worst performers in a cohort study of >1000 subjects aged 50+ who underwent neuropsychological assessment. We use a novel approach focusing on the dominant FC pattern captured by the leading eigenvector of dynamic FC matrices. Recurrent FC patterns – or states – are detected and characterized in terms of lifetime, probability of occurrence and switching profiles. We find that poorer cognitive performance is associated with weaker FC temporal similarity together with altered switching between FC states. These results provide new evidence linking the switching dynamics of FC during rest with cognitive performance in later life, reinforcing the functional role of resting-state activity for effective cognitive processing.


Url:
DOI: 10.1038/s41598-017-05425-7
PubMed: 28698644
PubMed Central: 5506029


Affiliations:


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PMC:5506029

Le document en format XML

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<institution>ICVS/3B’s - PT Government Associate Laboratory,</institution>
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4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>4710-057 Braga</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff6">Clinical Academic Center (2CA-Braga), 4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>Clinical Academic Center (2CA-Braga), 4710-057 Braga</wicri:regionArea>
<wicri:noRegion>4710-057 Braga</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Miguel Soares, Jose" sort="Miguel Soares, Jose" uniqKey="Miguel Soares J" first="José" last="Miguel Soares">José Miguel Soares</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff4">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2159 175X</institution-id>
<institution-id institution-id-type="GRID">grid.10328.38</institution-id>
<institution></institution>
<institution>Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho,</institution>
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4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>4710-057 Braga</wicri:regionArea>
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<affiliation wicri:level="1">
<nlm:aff id="Aff5">
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<institution-id institution-id-type="ISNI">0000 0001 2159 175X</institution-id>
<institution-id institution-id-type="GRID">grid.10328.38</institution-id>
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<institution>ICVS/3B’s - PT Government Associate Laboratory,</institution>
</institution-wrap>
4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>4710-057 Braga</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff6">Clinical Academic Center (2CA-Braga), 4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>Clinical Academic Center (2CA-Braga), 4710-057 Braga</wicri:regionArea>
<wicri:noRegion>4710-057 Braga</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Deco, Gustavo" sort="Deco, Gustavo" uniqKey="Deco G" first="Gustavo" last="Deco">Gustavo Deco</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff7">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2172 2676</institution-id>
<institution-id institution-id-type="GRID">grid.5612.0</institution-id>
<institution>Center for Brain and Cognition, Computational Neuroscience Group,</institution>
<institution>Universitat Pompeu Fabra,</institution>
</institution-wrap>
08018 Barcelona, Spain</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea>08018 Barcelona</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff8">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0000 9601 989X</institution-id>
<institution-id institution-id-type="GRID">grid.425902.8</institution-id>
<institution></institution>
<institution>Institució Catalana de Recerca i Estudis Avançats (ICREA),</institution>
</institution-wrap>
08010 Barcelona, Spain</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea>08010 Barcelona</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff9">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 0041 5028</institution-id>
<institution-id institution-id-type="GRID">grid.419524.f</institution-id>
<institution>Department of Neuropsychology,</institution>
<institution>Max Planck Institute for Human Cognitive and Brain Sciences,</institution>
</institution-wrap>
04103 Leipzig, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>04103 Leipzig</wicri:regionArea>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff10">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 7857</institution-id>
<institution-id institution-id-type="GRID">grid.1002.3</institution-id>
<institution>School of Psychological Sciences,</institution>
<institution>Monash University,</institution>
</institution-wrap>
Clayton VIC 3800, Melbourne, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Clayton VIC 3800, Melbourne</wicri:regionArea>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Sousa, Nuno" sort="Sousa, Nuno" uniqKey="Sousa N" first="Nuno" last="Sousa">Nuno Sousa</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff4">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2159 175X</institution-id>
<institution-id institution-id-type="GRID">grid.10328.38</institution-id>
<institution></institution>
<institution>Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho,</institution>
</institution-wrap>
4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>4710-057 Braga</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff5">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2159 175X</institution-id>
<institution-id institution-id-type="GRID">grid.10328.38</institution-id>
<institution></institution>
<institution>ICVS/3B’s - PT Government Associate Laboratory,</institution>
</institution-wrap>
4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>4710-057 Braga</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff6">Clinical Academic Center (2CA-Braga), 4710-057 Braga, Portugal</nlm:aff>
<country xml:lang="fr">Portugal</country>
<wicri:regionArea>Clinical Academic Center (2CA-Braga), 4710-057 Braga</wicri:regionArea>
<wicri:noRegion>4710-057 Braga</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Kringelbach, Morten L" sort="Kringelbach, Morten L" uniqKey="Kringelbach M" first="Morten L." last="Kringelbach">Morten L. Kringelbach</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 8948</institution-id>
<institution-id institution-id-type="GRID">grid.4991.5</institution-id>
<institution>Department of Psychiatry,</institution>
<institution>University of Oxford,</institution>
</institution-wrap>
OX37JX Oxford, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>OX37JX Oxford</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 1956 2722</institution-id>
<institution-id institution-id-type="GRID">grid.7048.b</institution-id>
<institution></institution>
<institution>Center for Music in the Brain, Aarhus University,</institution>
</institution-wrap>
8000 Aarhus, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>8000 Aarhus</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff11">Institut d’études avancées de Paris, 75004 Paris, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut d’études avancées de Paris, 75004 Paris</wicri:regionArea>
<wicri:noRegion>75004 Paris</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Scientific Reports</title>
<idno type="eISSN">2045-2322</idno>
<imprint>
<date when="2017">2017</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p id="Par1">Growing evidence has shown that brain activity at rest slowly wanders through a repertoire of different states, where whole-brain functional connectivity (FC) temporarily settles into distinct FC patterns. Nevertheless, the functional role of resting-state activity remains unclear. Here, we investigate how the switching behavior of resting-state FC relates with cognitive performance in healthy older adults. We analyse resting-state fMRI data from 98 healthy adults previously categorized as being among the best or among the worst performers in a cohort study of >1000 subjects aged 50+ who underwent neuropsychological assessment. We use a novel approach focusing on the dominant FC pattern captured by the leading eigenvector of dynamic FC matrices. Recurrent FC patterns – or states – are detected and characterized in terms of lifetime, probability of occurrence and switching profiles. We find that poorer cognitive performance is associated with weaker FC temporal similarity together with altered switching between FC states. These results provide new evidence linking the switching dynamics of FC during rest with cognitive performance in later life, reinforcing the functional role of resting-state activity for effective cognitive processing.</p>
</div>
</front>
<back>
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<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group>
<journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher>
<publisher-name>Nature Publishing Group UK</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">28698644</article-id>
<article-id pub-id-type="pmc">5506029</article-id>
<article-id pub-id-type="publisher-id">5425</article-id>
<article-id pub-id-type="doi">10.1038/s41598-017-05425-7</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Cognitive performance in healthy older adults relates to spontaneous switching between states of functional connectivity during rest</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-6715-0826</contrib-id>
<name>
<surname>Cabral</surname>
<given-names>Joana</given-names>
</name>
<address>
<email>joana.cabral@psych.ox.ac.uk</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Vidaurre</surname>
<given-names>Diego</given-names>
</name>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Marques</surname>
<given-names>Paulo</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
<xref ref-type="aff" rid="Aff5">5</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-6279-2195</contrib-id>
<name>
<surname>Magalhães</surname>
<given-names>Ricardo</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
<xref ref-type="aff" rid="Aff5">5</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Silva Moreira</surname>
<given-names>Pedro</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
<xref ref-type="aff" rid="Aff5">5</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Miguel Soares</surname>
<given-names>José</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
<xref ref-type="aff" rid="Aff5">5</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Deco</surname>
<given-names>Gustavo</given-names>
</name>
<xref ref-type="aff" rid="Aff7">7</xref>
<xref ref-type="aff" rid="Aff8">8</xref>
<xref ref-type="aff" rid="Aff9">9</xref>
<xref ref-type="aff" rid="Aff10">10</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sousa</surname>
<given-names>Nuno</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
<xref ref-type="aff" rid="Aff5">5</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-3908-6898</contrib-id>
<name>
<surname>Kringelbach</surname>
<given-names>Morten L.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff11">11</xref>
</contrib>
<aff id="Aff1">
<label>1</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 8948</institution-id>
<institution-id institution-id-type="GRID">grid.4991.5</institution-id>
<institution>Department of Psychiatry,</institution>
<institution>University of Oxford,</institution>
</institution-wrap>
OX37JX Oxford, UK</aff>
<aff id="Aff2">
<label>2</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 1956 2722</institution-id>
<institution-id institution-id-type="GRID">grid.7048.b</institution-id>
<institution></institution>
<institution>Center for Music in the Brain, Aarhus University,</institution>
</institution-wrap>
8000 Aarhus, Denmark</aff>
<aff id="Aff3">
<label>3</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 8948</institution-id>
<institution-id institution-id-type="GRID">grid.4991.5</institution-id>
<institution></institution>
<institution>Oxford Centre for Human Brain Activity, University of Oxford,</institution>
</institution-wrap>
OX37JX Oxford, UK</aff>
<aff id="Aff4">
<label>4</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2159 175X</institution-id>
<institution-id institution-id-type="GRID">grid.10328.38</institution-id>
<institution></institution>
<institution>Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho,</institution>
</institution-wrap>
4710-057 Braga, Portugal</aff>
<aff id="Aff5">
<label>5</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2159 175X</institution-id>
<institution-id institution-id-type="GRID">grid.10328.38</institution-id>
<institution></institution>
<institution>ICVS/3B’s - PT Government Associate Laboratory,</institution>
</institution-wrap>
4710-057 Braga, Portugal</aff>
<aff id="Aff6">
<label>6</label>
Clinical Academic Center (2CA-Braga), 4710-057 Braga, Portugal</aff>
<aff id="Aff7">
<label>7</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2172 2676</institution-id>
<institution-id institution-id-type="GRID">grid.5612.0</institution-id>
<institution>Center for Brain and Cognition, Computational Neuroscience Group,</institution>
<institution>Universitat Pompeu Fabra,</institution>
</institution-wrap>
08018 Barcelona, Spain</aff>
<aff id="Aff8">
<label>8</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0000 9601 989X</institution-id>
<institution-id institution-id-type="GRID">grid.425902.8</institution-id>
<institution></institution>
<institution>Institució Catalana de Recerca i Estudis Avançats (ICREA),</institution>
</institution-wrap>
08010 Barcelona, Spain</aff>
<aff id="Aff9">
<label>9</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 0041 5028</institution-id>
<institution-id institution-id-type="GRID">grid.419524.f</institution-id>
<institution>Department of Neuropsychology,</institution>
<institution>Max Planck Institute for Human Cognitive and Brain Sciences,</institution>
</institution-wrap>
04103 Leipzig, Germany</aff>
<aff id="Aff10">
<label>10</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 7857</institution-id>
<institution-id institution-id-type="GRID">grid.1002.3</institution-id>
<institution>School of Psychological Sciences,</institution>
<institution>Monash University,</institution>
</institution-wrap>
Clayton VIC 3800, Melbourne, Australia</aff>
<aff id="Aff11">
<label>11</label>
Institut d’études avancées de Paris, 75004 Paris, France</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>11</day>
<month>7</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>11</day>
<month>7</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<year>2017</year>
</pub-date>
<volume>7</volume>
<elocation-id>5135</elocation-id>
<history>
<date date-type="received">
<day>19</day>
<month>12</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>30</day>
<month>5</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>© The Author(s) 2017</copyright-statement>
<license license-type="OpenAccess">
<license-p>
<bold>Open Access</bold>
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<p id="Par1">Growing evidence has shown that brain activity at rest slowly wanders through a repertoire of different states, where whole-brain functional connectivity (FC) temporarily settles into distinct FC patterns. Nevertheless, the functional role of resting-state activity remains unclear. Here, we investigate how the switching behavior of resting-state FC relates with cognitive performance in healthy older adults. We analyse resting-state fMRI data from 98 healthy adults previously categorized as being among the best or among the worst performers in a cohort study of >1000 subjects aged 50+ who underwent neuropsychological assessment. We use a novel approach focusing on the dominant FC pattern captured by the leading eigenvector of dynamic FC matrices. Recurrent FC patterns – or states – are detected and characterized in terms of lifetime, probability of occurrence and switching profiles. We find that poorer cognitive performance is associated with weaker FC temporal similarity together with altered switching between FC states. These results provide new evidence linking the switching dynamics of FC during rest with cognitive performance in later life, reinforcing the functional role of resting-state activity for effective cognitive processing.</p>
</abstract>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2017</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Australie</li>
<li>Danemark</li>
<li>Espagne</li>
<li>France</li>
<li>Portugal</li>
<li>Royaume-Uni</li>
</country>
<region>
<li>Victoria (État)</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Melbourne</li>
<li>Paris</li>
</settlement>
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<name sortKey="Kringelbach, Morten L" sort="Kringelbach, Morten L" uniqKey="Kringelbach M" first="Morten L." last="Kringelbach">Morten L. Kringelbach</name>
<name sortKey="Vidaurre, Diego" sort="Vidaurre, Diego" uniqKey="Vidaurre D" first="Diego" last="Vidaurre">Diego Vidaurre</name>
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<name sortKey="Cabral, Joana" sort="Cabral, Joana" uniqKey="Cabral J" first="Joana" last="Cabral">Joana Cabral</name>
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<name sortKey="Kringelbach, Morten L" sort="Kringelbach, Morten L" uniqKey="Kringelbach M" first="Morten L." last="Kringelbach">Morten L. Kringelbach</name>
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<name sortKey="Marques, Paulo" sort="Marques, Paulo" uniqKey="Marques P" first="Paulo" last="Marques">Paulo Marques</name>
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<name sortKey="Magalhaes, Ricardo" sort="Magalhaes, Ricardo" uniqKey="Magalhaes R" first="Ricardo" last="Magalhães">Ricardo Magalhães</name>
<name sortKey="Magalhaes, Ricardo" sort="Magalhaes, Ricardo" uniqKey="Magalhaes R" first="Ricardo" last="Magalhães">Ricardo Magalhães</name>
<name sortKey="Magalhaes, Ricardo" sort="Magalhaes, Ricardo" uniqKey="Magalhaes R" first="Ricardo" last="Magalhães">Ricardo Magalhães</name>
<name sortKey="Marques, Paulo" sort="Marques, Paulo" uniqKey="Marques P" first="Paulo" last="Marques">Paulo Marques</name>
<name sortKey="Marques, Paulo" sort="Marques, Paulo" uniqKey="Marques P" first="Paulo" last="Marques">Paulo Marques</name>
<name sortKey="Miguel Soares, Jose" sort="Miguel Soares, Jose" uniqKey="Miguel Soares J" first="José" last="Miguel Soares">José Miguel Soares</name>
<name sortKey="Miguel Soares, Jose" sort="Miguel Soares, Jose" uniqKey="Miguel Soares J" first="José" last="Miguel Soares">José Miguel Soares</name>
<name sortKey="Miguel Soares, Jose" sort="Miguel Soares, Jose" uniqKey="Miguel Soares J" first="José" last="Miguel Soares">José Miguel Soares</name>
<name sortKey="Silva Moreira, Pedro" sort="Silva Moreira, Pedro" uniqKey="Silva Moreira P" first="Pedro" last="Silva Moreira">Pedro Silva Moreira</name>
<name sortKey="Silva Moreira, Pedro" sort="Silva Moreira, Pedro" uniqKey="Silva Moreira P" first="Pedro" last="Silva Moreira">Pedro Silva Moreira</name>
<name sortKey="Silva Moreira, Pedro" sort="Silva Moreira, Pedro" uniqKey="Silva Moreira P" first="Pedro" last="Silva Moreira">Pedro Silva Moreira</name>
<name sortKey="Sousa, Nuno" sort="Sousa, Nuno" uniqKey="Sousa N" first="Nuno" last="Sousa">Nuno Sousa</name>
<name sortKey="Sousa, Nuno" sort="Sousa, Nuno" uniqKey="Sousa N" first="Nuno" last="Sousa">Nuno Sousa</name>
<name sortKey="Sousa, Nuno" sort="Sousa, Nuno" uniqKey="Sousa N" first="Nuno" last="Sousa">Nuno Sousa</name>
</country>
<country name="Espagne">
<noRegion>
<name sortKey="Deco, Gustavo" sort="Deco, Gustavo" uniqKey="Deco G" first="Gustavo" last="Deco">Gustavo Deco</name>
</noRegion>
<name sortKey="Deco, Gustavo" sort="Deco, Gustavo" uniqKey="Deco G" first="Gustavo" last="Deco">Gustavo Deco</name>
</country>
<country name="Allemagne">
<noRegion>
<name sortKey="Deco, Gustavo" sort="Deco, Gustavo" uniqKey="Deco G" first="Gustavo" last="Deco">Gustavo Deco</name>
</noRegion>
</country>
<country name="Australie">
<region name="Victoria (État)">
<name sortKey="Deco, Gustavo" sort="Deco, Gustavo" uniqKey="Deco G" first="Gustavo" last="Deco">Gustavo Deco</name>
</region>
</country>
<country name="France">
<region name="Île-de-France">
<name sortKey="Kringelbach, Morten L" sort="Kringelbach, Morten L" uniqKey="Kringelbach M" first="Morten L." last="Kringelbach">Morten L. Kringelbach</name>
</region>
</country>
</tree>
</affiliations>
</record>

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