Disrupted Nodal and Hub Organization Account for Brain Network Abnormalities in Parkinson’s Disease
Identifieur interne : 000961 ( Pmc/Curation ); précédent : 000960; suivant : 000962Disrupted Nodal and Hub Organization Account for Brain Network Abnormalities in Parkinson’s Disease
Auteurs : Yuko Koshimori [Canada] ; Sang-Soo Cho [Canada] ; Marion Criaud [Canada] ; Leigh Christopher [Canada] ; Mark Jacobs [Canada] ; Christine Ghadery [Canada] ; Sarah Coakeley [Canada] ; Madeleine Harris [Canada] ; Romina Mizrahi [Canada] ; Clement Hamani [Canada] ; Anthony E. Lang [Canada] ; Sylvain Houle [Canada] ; Antonio P. Strafella [Canada]Source :
- Frontiers in Aging Neuroscience [ 1663-4365 ] ; 2016.
Abstract
The recent application of graph theory to brain networks promises to shed light on complex diseases such as Parkinson’s disease (PD). This study aimed to investigate functional changes in sensorimotor and cognitive networks in Parkinsonian patients, with a focus on inter- and intra-connectivity organization in the disease-associated nodal and hub regions using the graph theoretical analyses. Resting-state functional MRI data of a total of 65 participants, including 23 healthy controls (HCs) and 42 patients, were investigated in 120 nodes for local efficiency, betweenness centrality, and degree. Hub regions were identified in the HC and patient groups. We found nodal and hub changes in patients compared with HCs, including the right pre-supplementary motor area (SMA), left anterior insula, bilateral mid-insula, bilateral dorsolateral prefrontal cortex (DLPFC), and right caudate nucleus. In general, nodal regions within the sensorimotor network (i.e., right pre-SMA and right mid-insula) displayed weakened connectivity, with the former node associated with more severe bradykinesia, and impaired integration with default mode network regions. The left mid-insula also lost its hub properties in patients. Within the executive networks, the left anterior insular cortex lost its hub properties in patients, while a new hub region was identified in the right caudate nucleus, paralleled by an increased level of inter- and intra-connectivity in the bilateral DLPFC possibly representing compensatory mechanisms. These findings highlight the diffuse changes in nodal organization and regional hub disruption accounting for the distributed abnormalities across brain networks and the clinical manifestations of PD.
Url:
DOI: 10.3389/fnagi.2016.00259
PubMed: 27891090
PubMed Central: 5102897
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<front><div type="abstract" xml:lang="en"><p>The recent application of graph theory to brain networks promises to shed light on complex diseases such as Parkinson’s disease (PD). This study aimed to investigate functional changes in sensorimotor and cognitive networks in Parkinsonian patients, with a focus on inter- and intra-connectivity organization in the disease-associated nodal and hub regions using the graph theoretical analyses. Resting-state functional MRI data of a total of 65 participants, including 23 healthy controls (HCs) and 42 patients, were investigated in 120 nodes for local efficiency, betweenness centrality, and degree. Hub regions were identified in the HC and patient groups. We found nodal and hub changes in patients compared with HCs, including the right pre-supplementary motor area (SMA), left anterior insula, bilateral mid-insula, bilateral dorsolateral prefrontal cortex (DLPFC), and right caudate nucleus. In general, nodal regions within the sensorimotor network (i.e., right pre-SMA and right mid-insula) displayed weakened connectivity, with the former node associated with more severe bradykinesia, and impaired integration with default mode network regions. The left mid-insula also lost its hub properties in patients. Within the executive networks, the left anterior insular cortex lost its hub properties in patients, while a new hub region was identified in the right caudate nucleus, paralleled by an increased level of inter- and intra-connectivity in the bilateral DLPFC possibly representing compensatory mechanisms. These findings highlight the diffuse changes in nodal organization and regional hub disruption accounting for the distributed abnormalities across brain networks and the clinical manifestations of PD.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Aging Neurosci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Aging Neurosci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Aging Neurosci.</journal-id>
<journal-title-group><journal-title>Frontiers in Aging Neuroscience</journal-title>
</journal-title-group>
<issn pub-type="epub">1663-4365</issn>
<publisher><publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27891090</article-id>
<article-id pub-id-type="pmc">5102897</article-id>
<article-id pub-id-type="doi">10.3389/fnagi.2016.00259</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>Disrupted Nodal and Hub Organization Account for Brain Network Abnormalities in Parkinson’s Disease</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Koshimori</surname>
<given-names>Yuko</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="author-notes" rid="fn001"><sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/363233/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Cho</surname>
<given-names>Sang-Soo</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Criaud</surname>
<given-names>Marion</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/383258/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Christopher</surname>
<given-names>Leigh</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jacobs</surname>
<given-names>Mark</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ghadery</surname>
<given-names>Christine</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Coakeley</surname>
<given-names>Sarah</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harris</surname>
<given-names>Madeleine</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mizrahi</surname>
<given-names>Romina</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hamani</surname>
<given-names>Clement</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/168746/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Lang</surname>
<given-names>Anthony E.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Houle</surname>
<given-names>Sylvain</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Strafella</surname>
<given-names>Antonio P.</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="aff4"><sup>4</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Research Imaging Centre, Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, University of Toronto, Toronto</institution>
<country>ON, Canada</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Division of Brain, Imaging and Behaviour – Systems Neuroscience, Krembil Research Institute, University Health Network, University of Toronto, Toronto</institution>
<country>ON, Canada</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>Division of Neurosurgery, Toronto Western Hospital, University Health Network, University of Toronto, Toronto</institution>
<country>ON, Canada</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Morton and Gloria Shulman Movement Disorder Unit & E. J. Safra Parkinson Disease Program, Neurology Division, Department of Medicine, Toronto Western Hospital, University Health Network, University of Toronto, Toronto</institution>
<country>ON, Canada</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Isidre Ferrer, University of Barcelona, Spain</italic>
</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: <italic>Philippe Boulinguez, Claude Bernard University Lyon 1, France; Simon J. G. Lewis, Brain and Mind Research Institute, Australia; Roberto Cilia, Parkinson Institute, Italy</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence: <italic>Yuko Koshimori, <email xlink:type="simple">yuko.koshimori@mail.utoronto.ca</email>
; <email xlink:type="simple">ykoshee321@gmail.com</email>
</italic>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>10</day>
<month>11</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>8</volume>
<elocation-id>259</elocation-id>
<history><date date-type="received"><day>25</day>
<month>7</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>19</day>
<month>10</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016 Koshimori, Cho, Criaud, Christopher, Jacobs, Ghadery, Coakeley, Harris, Mizrahi, Hamani, Lang, Houle and Strafella.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Koshimori, Cho, Criaud, Christopher, Jacobs, Ghadery, Coakeley, Harris, Mizrahi, Hamani, Lang, Houle and Strafella</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><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>The recent application of graph theory to brain networks promises to shed light on complex diseases such as Parkinson’s disease (PD). This study aimed to investigate functional changes in sensorimotor and cognitive networks in Parkinsonian patients, with a focus on inter- and intra-connectivity organization in the disease-associated nodal and hub regions using the graph theoretical analyses. Resting-state functional MRI data of a total of 65 participants, including 23 healthy controls (HCs) and 42 patients, were investigated in 120 nodes for local efficiency, betweenness centrality, and degree. Hub regions were identified in the HC and patient groups. We found nodal and hub changes in patients compared with HCs, including the right pre-supplementary motor area (SMA), left anterior insula, bilateral mid-insula, bilateral dorsolateral prefrontal cortex (DLPFC), and right caudate nucleus. In general, nodal regions within the sensorimotor network (i.e., right pre-SMA and right mid-insula) displayed weakened connectivity, with the former node associated with more severe bradykinesia, and impaired integration with default mode network regions. The left mid-insula also lost its hub properties in patients. Within the executive networks, the left anterior insular cortex lost its hub properties in patients, while a new hub region was identified in the right caudate nucleus, paralleled by an increased level of inter- and intra-connectivity in the bilateral DLPFC possibly representing compensatory mechanisms. These findings highlight the diffuse changes in nodal organization and regional hub disruption accounting for the distributed abnormalities across brain networks and the clinical manifestations of PD.</p>
</abstract>
<kwd-group><kwd>Parkinson’s disease</kwd>
<kwd>bradykinesia</kwd>
<kwd>cognitive impairment</kwd>
<kwd>resting-state functional MRI (rsfMRI)</kwd>
<kwd>brain network</kwd>
</kwd-group>
<funding-group><award-group><funding-source id="cn001">Canadian Institutes of Health Research<named-content content-type="fundref-id">10.13039/501100000024</named-content>
</funding-source>
<award-id rid="cn001">MOP 136778</award-id>
</award-group>
</funding-group>
<counts><fig-count count="3"></fig-count>
<table-count count="4"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="64"></ref-count>
<page-count count="10"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
</pmc>
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