Subthalamic Nucleus Electrical Stimulation Modulates Calcium Activity of Nigral Astrocytes
Identifieur interne : 000565 ( Pmc/Checkpoint ); précédent : 000564; suivant : 000566Subthalamic Nucleus Electrical Stimulation Modulates Calcium Activity of Nigral Astrocytes
Auteurs : Elodie Barat [France] ; Sylvie Boisseau [France] ; Céline Bouyssières [France] ; Florence Appaix [France] ; Marc Savasta [France] ; Mireille Albrieux [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2012.
Abstract
The substantia nigra pars reticulata (SNr) is a major output nucleus of the basal ganglia, delivering inhibitory efferents to the relay nuclei of the thalamus. Pathological hyperactivity of SNr neurons is known to be responsible for some motor disorders
In this work, we developed a rat brain slice model to study the influence of spontaneous and induced excitability of afferent nuclei on SNr astrocytes calcium activity. Astrocytes represent the main cellular population in the SNr and display spontaneous calcium activities in basal conditions. Half of this activity is autonomous (
Astrocytes are now viewed as active components of neural networks but their role depends on the brain structure concerned. In the SNr, evoked activity prevails and autonomous calcium activity is lower than in the cortex or hippocampus. Our data therefore reflect a specific role of SNr astrocytes in sensing the STN-GPe-SNr loops activity and suggest that SNr astrocytes could potentially feedback on SNr neuronal activity. These findings have major implications given the position of SNr in the basal ganglia network.
Url:
DOI: 10.1371/journal.pone.0041793
PubMed: 22848608
PubMed Central: 3407058
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Base, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Joseph Fourier, Grenoble F- 38042</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><orgName type="university">Université Joseph Fourier</orgName></affiliation></author><author><name sortKey="Boisseau, Sylvie" sort="Boisseau, Sylvie" uniqKey="Boisseau S" first="Sylvie" last="Boisseau">Sylvie Boisseau</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Joseph Fourier, Grenoble F- 38042</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><orgName type="university">Université Joseph Fourier</orgName></affiliation></author><author><name sortKey="Bouyssieres, Celine" sort="Bouyssieres, Celine" uniqKey="Bouyssieres C" first="Céline" last="Bouyssières">Céline Bouyssières</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Joseph Fourier, Grenoble F- 38042</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><orgName type="university">Université Joseph Fourier</orgName></affiliation></author><author><name sortKey="Appaix, Florence" sort="Appaix, Florence" uniqKey="Appaix F" first="Florence" last="Appaix">Florence Appaix</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Joseph Fourier, Grenoble F- 38042</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><orgName type="university">Université Joseph Fourier</orgName></affiliation></author><author><name sortKey="Savasta, Marc" sort="Savasta, Marc" uniqKey="Savasta M" first="Marc" last="Savasta">Marc Savasta</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Joseph Fourier, Grenoble F- 38042</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><orgName type="university">Université Joseph Fourier</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>Centre Hospitalier Universitaire de Grenoble, BP217, Grenoble F-38043, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre Hospitalier Universitaire de Grenoble, BP217, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation></author><author><name sortKey="Albrieux, Mireille" sort="Albrieux, Mireille" uniqKey="Albrieux M" first="Mireille" last="Albrieux">Mireille Albrieux</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Joseph Fourier, Grenoble F- 38042</wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><orgName type="university">Université Joseph Fourier</orgName></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></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>The substantia nigra pars reticulata (SNr) is a major output nucleus of the basal ganglia, delivering inhibitory efferents to the relay nuclei of the thalamus. Pathological hyperactivity of SNr neurons is known to be responsible for some motor disorders <italic>e.g.</italic> in Parkinson's disease. One way to restore this pathological activity is to electrically stimulate one of the SNr input, the excitatory subthalamic nucleus (STN), which has emerged as an effective treatment for parkinsonian patients. The neuronal network and signal processing of the basal ganglia are well known but, paradoxically, the role of astrocytes in the regulation of SNr activity has never been studied.</p></sec><sec><title>Principal Findings</title><p>In this work, we developed a rat brain slice model to study the influence of spontaneous and induced excitability of afferent nuclei on SNr astrocytes calcium activity. Astrocytes represent the main cellular population in the SNr and display spontaneous calcium activities in basal conditions. Half of this activity is autonomous (<italic>i.e.</italic> independent of synaptic activity) while the other half is dependent on spontaneous glutamate and GABA release, probably controlled by the pace-maker activity of the pallido-nigral and subthalamo-nigral loops. Modification of the activity of the loops by STN electrical stimulation disrupted this astrocytic calcium excitability through an increase of glutamate and GABA releases. Astrocytic AMPA, mGlu and GABA<sub>A</sub> receptors were involved in this effect.</p></sec><sec><title>Significance</title><p>Astrocytes are now viewed as active components of neural networks but their role depends on the brain structure concerned. In the SNr, evoked activity prevails and autonomous calcium activity is lower than in the cortex or hippocampus. Our data therefore reflect a specific role of SNr astrocytes in sensing the STN-GPe-SNr loops activity and suggest that SNr astrocytes could potentially feedback on SNr neuronal activity. These findings have major implications given the position of SNr in the basal ganglia network.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hikosaka, O" uniqKey="Hikosaka O">O Hikosaka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Richards, Cd" uniqKey="Richards C">CD Richards</name></author><author><name sortKey="Shiroyama, T" uniqKey="Shiroyama T">T Shiroyama</name></author><author><name sortKey="Kitai, St" uniqKey="Kitai S">ST Kitai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Delong, Mr" uniqKey="Delong M">MR DeLong</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plenz, D" uniqKey="Plenz D">D Plenz</name></author><author><name sortKey="Kital, St" uniqKey="Kital S">ST Kital</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kitai, St" uniqKey="Kitai S">ST 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<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">22848608</article-id><article-id pub-id-type="pmc">3407058</article-id><article-id pub-id-type="publisher-id">PONE-D-12-06749</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0041793</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>Model Organisms</subject><subj-group><subject>Animal Models</subject><subj-group><subject>Rat</subject></subj-group></subj-group></subj-group><subj-group><subject>Molecular Cell Biology</subject><subj-group><subject>Cellular Types</subject><subj-group><subject>Neurons</subject></subj-group></subj-group></subj-group><subj-group><subject>Neuroscience</subject><subj-group><subject>Cellular Neuroscience</subject><subj-group><subject>Ion Channels</subject></subj-group></subj-group><subj-group><subject>Neuroimaging</subject><subj-group><subject>Calcium Imaging</subject></subj-group></subj-group><subj-group><subject>Neurophysiology</subject><subj-group><subject>Motor Systems</subject></subj-group></subj-group><subj-group><subject>Neurotransmitters</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Subthalamic Nucleus Electrical Stimulation Modulates Calcium Activity of Nigral Astrocytes</article-title><alt-title alt-title-type="running-head">Astrocytes Excitability in the SNr</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Barat</surname><given-names>Elodie</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>Boisseau</surname><given-names>Sylvie</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>Bouyssières</surname><given-names>Céline</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>Appaix</surname><given-names>Florence</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>Savasta</surname><given-names>Marc</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>Albrieux</surname><given-names>Mireille</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="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Institut National de la Santé et de la Recherche Médicale, U 836, Grenoble Institut des Neurosciences, Equipe Dynamique et Physiopathologie des Ganglions de la Base, Grenoble F-38043, France</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Université Joseph Fourier, Grenoble F- 38042, France</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Centre Hospitalier Universitaire de Grenoble, BP217, Grenoble F-38043, France</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Finkelstein</surname><given-names>David I.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">The Mental Health Research Institute of Victoria, The University of Melbourne, Australia</aff><author-notes><corresp id="cor1">* E-mail: <email>mireille.albrieux@ujf-grenoble.fr</email></corresp><fn fn-type="con"><p>Conceived and designed the experiments: EB SB CB MA. Performed the experiments: EB SB CB FA MA. Analyzed the data: EB SB CB MA. Contributed reagents/materials/analysis tools: FA MS MA. Wrote the paper: EB SB MS MA.</p></fn></author-notes><pub-date pub-type="collection"><year>2012</year></pub-date><pub-date pub-type="epub"><day>27</day><month>7</month><year>2012</year></pub-date><volume>7</volume><issue>7</issue><elocation-id>e41793</elocation-id><history><date date-type="received"><day>6</day><month>3</month><year>2012</year></date><date date-type="accepted"><day>25</day><month>6</month><year>2012</year></date></history><permissions><copyright-statement>Barat 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 substantia nigra pars reticulata (SNr) is a major output nucleus of the basal ganglia, delivering inhibitory efferents to the relay nuclei of the thalamus. Pathological hyperactivity of SNr neurons is known to be responsible for some motor disorders <italic>e.g.</italic> in Parkinson's disease. One way to restore this pathological activity is to electrically stimulate one of the SNr input, the excitatory subthalamic nucleus (STN), which has emerged as an effective treatment for parkinsonian patients. The neuronal network and signal processing of the basal ganglia are well known but, paradoxically, the role of astrocytes in the regulation of SNr activity has never been studied.</p></sec><sec><title>Principal Findings</title><p>In this work, we developed a rat brain slice model to study the influence of spontaneous and induced excitability of afferent nuclei on SNr astrocytes calcium activity. Astrocytes represent the main cellular population in the SNr and display spontaneous calcium activities in basal conditions. Half of this activity is autonomous (<italic>i.e.</italic> independent of synaptic activity) while the other half is dependent on spontaneous glutamate and GABA release, probably controlled by the pace-maker activity of the pallido-nigral and subthalamo-nigral loops. Modification of the activity of the loops by STN electrical stimulation disrupted this astrocytic calcium excitability through an increase of glutamate and GABA releases. Astrocytic AMPA, mGlu and GABA<sub>A</sub> receptors were involved in this effect.</p></sec><sec><title>Significance</title><p>Astrocytes are now viewed as active components of neural networks but their role depends on the brain structure concerned. In the SNr, evoked activity prevails and autonomous calcium activity is lower than in the cortex or hippocampus. Our data therefore reflect a specific role of SNr astrocytes in sensing the STN-GPe-SNr loops activity and suggest that SNr astrocytes could potentially feedback on SNr neuronal activity. These findings have major implications given the position of SNr in the basal ganglia network.</p></sec></abstract><counts><page-count count="13"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>France</li></country><region><li>Auvergne-Rhône-Alpes</li><li>Rhône-Alpes</li></region><orgName><li>Université Joseph Fourier</li></orgName></list><tree><country name="France"><region name="Auvergne-Rhône-Alpes"><name sortKey="Barat, Elodie" sort="Barat, Elodie" uniqKey="Barat E" first="Elodie" last="Barat">Elodie Barat</name></region><name sortKey="Albrieux, Mireille" sort="Albrieux, Mireille" uniqKey="Albrieux M" first="Mireille" last="Albrieux">Mireille Albrieux</name><name sortKey="Albrieux, Mireille" sort="Albrieux, Mireille" uniqKey="Albrieux M" first="Mireille" last="Albrieux">Mireille Albrieux</name><name sortKey="Appaix, Florence" sort="Appaix, Florence" uniqKey="Appaix F" first="Florence" last="Appaix">Florence Appaix</name><name sortKey="Appaix, Florence" sort="Appaix, Florence" uniqKey="Appaix F" first="Florence" last="Appaix">Florence Appaix</name><name sortKey="Barat, Elodie" sort="Barat, Elodie" uniqKey="Barat E" first="Elodie" last="Barat">Elodie Barat</name><name sortKey="Boisseau, Sylvie" sort="Boisseau, Sylvie" uniqKey="Boisseau S" first="Sylvie" last="Boisseau">Sylvie Boisseau</name><name sortKey="Boisseau, Sylvie" sort="Boisseau, Sylvie" uniqKey="Boisseau S" first="Sylvie" last="Boisseau">Sylvie Boisseau</name><name sortKey="Bouyssieres, Celine" sort="Bouyssieres, Celine" uniqKey="Bouyssieres C" first="Céline" last="Bouyssières">Céline Bouyssières</name><name sortKey="Bouyssieres, Celine" sort="Bouyssieres, Celine" uniqKey="Bouyssieres C" first="Céline" last="Bouyssières">Céline Bouyssières</name><name sortKey="Savasta, Marc" sort="Savasta, Marc" uniqKey="Savasta M" first="Marc" last="Savasta">Marc Savasta</name><name sortKey="Savasta, Marc" sort="Savasta, Marc" uniqKey="Savasta M" first="Marc" last="Savasta">Marc Savasta</name><name sortKey="Savasta, Marc" sort="Savasta, Marc" uniqKey="Savasta M" first="Marc" last="Savasta">Marc Savasta</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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