La maladie de Parkinson en France (serveur d'exploration)

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Resonance in subthalamo-cortical circuits in Parkinson's disease

Identifieur interne : 000704 ( Pmc/Curation ); précédent : 000703; suivant : 000705

Resonance in subthalamo-cortical circuits in Parkinson's disease

Auteurs : Alexandre Eusebio [Royaume-Uni, France] ; Alek Pogosyan [Royaume-Uni] ; Shouyan Wang [Royaume-Uni] ; Bruno Averbeck [Royaume-Uni] ; Louise Doyle Gaynor [Royaume-Uni] ; Stéphanie Cantiniaux [France] ; Tatiana Witjas [France] ; Patricia Limousin [Royaume-Uni] ; Jean-Philippe Azulay [France] ; Peter Brown [Royaume-Uni]

Source :

RBID : PMC:2714058

Abstract

Neuronal activity within and across the cortex and basal ganglia is pathologically synchronized, particularly at ∼ 20 Hz in patients with Parkinson's disease. Defining how activities in spatially distributed brain regions overtly synchronize in narrow frequency bands is critical for understanding disease processes like Parkinson's disease. To address this, we studied cortical responses to electrical stimulation of the subthalamic nucleus (STN) at various frequencies between 5 and 30 Hz in two cohorts of eight patients with Parkinson's disease from two different surgical centres. We found that evoked activity consisted of a series of diminishing waves with a peak latency of 21 ms for the first wave in the series. The cortical evoked potentials (cEPs) averaged in each group were well fitted by a damped oscillator function (r ≥0.9, P < 0.00001). Fits suggested that the natural frequency of the subthalamo-cortical circuit was around 20 Hz. When the system was forced at this frequency by stimulation of the STN at 20 Hz, the undamped amplitude of the modelled cortical response increased relative to that with 5 Hz stimulation in both groups (P ≤ 0.005), consistent with resonance. Restoration of dopaminergic input by treatment with levodopa increased the damping of oscillatory activity (as measured by the modelled damping factor) in both patient groups (P ≤0.001). The increased damping would tend to limit resonance, as confirmed in simulations. Our results show that the basal ganglia–cortical network involving the STN has a tendency to resonate at ∼ 20 Hz in Parkinsonian patients. This resonance phenomenon may underlie the propagation and amplification of activities synchronized around this frequency. Crucially, dopamine acts to increase damping and thereby limit resonance in this basal ganglia–cortical network.


Url:
DOI: 10.1093/brain/awp079
PubMed: 19369488
PubMed Central: 2714058

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<p>Neuronal activity within and across the cortex and basal ganglia is pathologically synchronized, particularly at ∼ 20 Hz in patients with Parkinson's disease. Defining how activities in spatially distributed brain regions overtly synchronize in narrow frequency bands is critical for understanding disease processes like Parkinson's disease. To address this, we studied cortical responses to electrical stimulation of the subthalamic nucleus (STN) at various frequencies between 5 and 30 Hz in two cohorts of eight patients with Parkinson's disease from two different surgical centres. We found that evoked activity consisted of a series of diminishing waves with a peak latency of 21 ms for the first wave in the series. The cortical evoked potentials (cEPs) averaged in each group were well fitted by a damped oscillator function (
<italic>r</italic>
 ≥0.9,
<italic>P</italic>
 < 0.00001). Fits suggested that the natural frequency of the subthalamo-cortical circuit was around 20 Hz. When the system was forced at this frequency by stimulation of the STN at 20 Hz, the undamped amplitude of the modelled cortical response increased relative to that with 5 Hz stimulation in both groups (
<italic>P</italic>
 ≤ 0.005), consistent with resonance. Restoration of dopaminergic input by treatment with levodopa increased the damping of oscillatory activity (as measured by the modelled damping factor) in both patient groups (
<italic>P</italic>
 ≤0.001). The increased damping would tend to limit resonance, as confirmed in simulations. Our results show that the basal ganglia–cortical network involving the STN has a tendency to resonate at ∼ 20 Hz in Parkinsonian patients. This resonance phenomenon may underlie the propagation and amplification of activities synchronized around this frequency. Crucially, dopamine acts to increase damping and thereby limit resonance in this basal ganglia–cortical network.</p>
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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">Brain</journal-id>
<journal-id journal-id-type="publisher-id">brainj</journal-id>
<journal-id journal-id-type="hwp">brain</journal-id>
<journal-title-group>
<journal-title>Brain</journal-title>
</journal-title-group>
<issn pub-type="ppub">0006-8950</issn>
<issn pub-type="epub">1460-2156</issn>
<publisher>
<publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">19369488</article-id>
<article-id pub-id-type="pmc">2714058</article-id>
<article-id pub-id-type="doi">10.1093/brain/awp079</article-id>
<article-id pub-id-type="publisher-id">awp079</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Original Articles</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Resonance in subthalamo-cortical circuits in Parkinson's disease</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Eusebio</surname>
<given-names>Alexandre</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>Pogosyan</surname>
<given-names>Alek</given-names>
</name>
<xref ref-type="aff" rid="AFF1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Shouyan</given-names>
</name>
<xref ref-type="aff" rid="AFF3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Averbeck</surname>
<given-names>Bruno</given-names>
</name>
<xref ref-type="aff" rid="AFF1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gaynor</surname>
<given-names>Louise Doyle</given-names>
</name>
<xref ref-type="aff" rid="AFF1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Cantiniaux</surname>
<given-names>Stéphanie</given-names>
</name>
<xref ref-type="aff" rid="AFF2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Witjas</surname>
<given-names>Tatiana</given-names>
</name>
<xref ref-type="aff" rid="AFF2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Limousin</surname>
<given-names>Patricia</given-names>
</name>
<xref ref-type="aff" rid="AFF1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="AFF4">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Azulay</surname>
<given-names>Jean-Philippe</given-names>
</name>
<xref ref-type="aff" rid="AFF2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Brown</surname>
<given-names>Peter</given-names>
</name>
<xref ref-type="aff" rid="AFF1">
<sup>1</sup>
</xref>
</contrib>
</contrib-group>
<aff id="AFF1">1 Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London, UK</aff>
<aff id="AFF2">2 Department of Neurology and Movement Disorders, Timone University Hospital, Marseille, France</aff>
<aff id="AFF3">3 Hearing and Balance Centre, Institute of Sound and Vibration Research, University of Southampton, UK</aff>
<aff id="AFF4">4 Unit of Functional Neurosurgery, Institute of Neurology, Queen Square, London, UK</aff>
<author-notes>
<corresp>Correspondence to: Peter Brown, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, 33 Queen Square, London, WC1N 3BG, UK E-mail:
<email>p.brown@ion.ucl.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub">
<month>8</month>
<year>2009</year>
</pub-date>
<pub-date pub-type="epub">
<day>15</day>
<month>4</month>
<year>2009</year>
</pub-date>
<volume>132</volume>
<issue>8</issue>
<fpage>2139</fpage>
<lpage>2150</lpage>
<history>
<date date-type="received">
<day>1</day>
<month>10</month>
<year>2008</year>
</date>
<date date-type="rev-recd">
<day>2</day>
<month>3</month>
<year>2009</year>
</date>
<date date-type="accepted">
<day>4</day>
<month>3</month>
<year>2009</year>
</date>
</history>
<permissions>
<copyright-statement>© 2009 The Author(s)</copyright-statement>
<copyright-year>2009</copyright-year>
<license license-type="openaccess">
<license-p>
<pmc-comment>CREATIVE COMMONS</pmc-comment>
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/2.0/uk/">http://creativecommons.org/licenses/by-nc/2.0/uk/</ext-link>
) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract>
<p>Neuronal activity within and across the cortex and basal ganglia is pathologically synchronized, particularly at ∼ 20 Hz in patients with Parkinson's disease. Defining how activities in spatially distributed brain regions overtly synchronize in narrow frequency bands is critical for understanding disease processes like Parkinson's disease. To address this, we studied cortical responses to electrical stimulation of the subthalamic nucleus (STN) at various frequencies between 5 and 30 Hz in two cohorts of eight patients with Parkinson's disease from two different surgical centres. We found that evoked activity consisted of a series of diminishing waves with a peak latency of 21 ms for the first wave in the series. The cortical evoked potentials (cEPs) averaged in each group were well fitted by a damped oscillator function (
<italic>r</italic>
 ≥0.9,
<italic>P</italic>
 < 0.00001). Fits suggested that the natural frequency of the subthalamo-cortical circuit was around 20 Hz. When the system was forced at this frequency by stimulation of the STN at 20 Hz, the undamped amplitude of the modelled cortical response increased relative to that with 5 Hz stimulation in both groups (
<italic>P</italic>
 ≤ 0.005), consistent with resonance. Restoration of dopaminergic input by treatment with levodopa increased the damping of oscillatory activity (as measured by the modelled damping factor) in both patient groups (
<italic>P</italic>
 ≤0.001). The increased damping would tend to limit resonance, as confirmed in simulations. Our results show that the basal ganglia–cortical network involving the STN has a tendency to resonate at ∼ 20 Hz in Parkinsonian patients. This resonance phenomenon may underlie the propagation and amplification of activities synchronized around this frequency. Crucially, dopamine acts to increase damping and thereby limit resonance in this basal ganglia–cortical network.</p>
</abstract>
<kwd-group>
<kwd>synchronization</kwd>
<kwd>basal ganglia</kwd>
<kwd>resonance</kwd>
<kwd>Parkinson's disease</kwd>
<kwd>deep brain stimulation</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>

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