Resonance in subthalamo-cortical circuits in Parkinson's disease
Identifieur interne : 002165 ( Main/Exploration ); précédent : 002164; suivant : 002166Resonance 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 :
- Brain [ 0006-8950 ] ; 2009.
Descripteurs français
- Pascal (Inist)
English descriptors
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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 ∼20Hz 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.
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level="a">Resonance in subthalamo-cortical circuits in Parkinson's disease</title><author><name sortKey="Eusebio, Alexandre" sort="Eusebio, Alexandre" uniqKey="Eusebio A" first="Alexandre" last="Eusebio">Alexandre Eusebio</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>8 aut.</sZ><sZ>10 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation><affiliation wicri:level="3"><inist:fA14 i1="02"><s1>Department of Neurology and Movement Disorders, Timone University Hospital</s1><s2>Marseille</s2><s3>FRA</s3><sZ>1 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>9 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region">Provence-Alpes-Côte d'Azur</region><region type="old region">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Pogosyan, Alek" sort="Pogosyan, Alek" uniqKey="Pogosyan A" first="Alek" last="Pogosyan">Alek Pogosyan</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>8 aut.</sZ><sZ>10 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Shouyan Wang" sort="Shouyan Wang" uniqKey="Shouyan Wang" last="Shouyan Wang">SHOUYAN WANG</name><affiliation wicri:level="1"><inist:fA14 i1="03"><s1>Hearing and Balance Centre, Institute of Sound and Vibration Research, University of Southampton</s1><s3>GBR</s3><sZ>3 aut.</sZ></inist:fA14><country>Royaume-Uni</country><wicri:noRegion>Hearing and Balance Centre, Institute of Sound and Vibration Research, University of Southampton</wicri:noRegion></affiliation></author><author><name sortKey="Averbeck, Bruno" sort="Averbeck, Bruno" uniqKey="Averbeck B" first="Bruno" last="Averbeck">Bruno Averbeck</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>8 aut.</sZ><sZ>10 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Doyle Gaynor, Louise" sort="Doyle Gaynor, Louise" uniqKey="Doyle Gaynor L" first="Louise" last="Doyle Gaynor">Louise Doyle Gaynor</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>8 aut.</sZ><sZ>10 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Cantiniaux, Stephanie" sort="Cantiniaux, Stephanie" uniqKey="Cantiniaux S" first="Stéphanie" last="Cantiniaux">Stéphanie Cantiniaux</name><affiliation wicri:level="3"><inist:fA14 i1="02"><s1>Department of Neurology and Movement Disorders, Timone University Hospital</s1><s2>Marseille</s2><s3>FRA</s3><sZ>1 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>9 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region">Provence-Alpes-Côte d'Azur</region><region type="old region">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Witjas, Tatiana" sort="Witjas, Tatiana" uniqKey="Witjas T" first="Tatiana" last="Witjas">Tatiana Witjas</name><affiliation wicri:level="3"><inist:fA14 i1="02"><s1>Department of Neurology and Movement Disorders, Timone University Hospital</s1><s2>Marseille</s2><s3>FRA</s3><sZ>1 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>9 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region">Provence-Alpes-Côte d'Azur</region><region type="old region">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Limousin, Patricia" sort="Limousin, Patricia" uniqKey="Limousin P" first="Patricia" last="Limousin">Patricia Limousin</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>8 aut.</sZ><sZ>10 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation><affiliation wicri:level="3"><inist:fA14 i1="04"><s1>Unit of Functional Neurosurgery, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>8 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Azulay, Jean Philippe" sort="Azulay, Jean Philippe" uniqKey="Azulay J" first="Jean-Philippe" last="Azulay">Jean-Philippe Azulay</name><affiliation wicri:level="3"><inist:fA14 i1="02"><s1>Department of Neurology and Movement Disorders, Timone University Hospital</s1><s2>Marseille</s2><s3>FRA</s3><sZ>1 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>9 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region">Provence-Alpes-Côte d'Azur</region><region type="old region">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Brown, Peter" sort="Brown, Peter" uniqKey="Brown P" first="Peter" last="Brown">Peter Brown</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square</s1><s2>London</s2><s3>GBR</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>8 aut.</sZ><sZ>10 aut.</sZ></inist:fA14><country>Royaume-Uni</country><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author></analytic><series><title level="j" type="main">Brain</title><title level="j" type="abbreviated">Brain</title><idno type="ISSN">0006-8950</idno><imprint><date when="2009">2009</date></imprint></series></biblStruct></sourceDesc><seriesStmt><title level="j" type="main">Brain</title><title level="j" type="abbreviated">Brain</title><idno type="ISSN">0006-8950</idno></seriesStmt></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Basal ganglion</term><term>Deep brain stimulation</term><term>Nervous system diseases</term><term>Parkinson disease</term><term>Synchronization</term></keywords><keywords scheme="Pascal" xml:lang="fr"><term>Maladie de Parkinson</term><term>Pathologie du système nerveux</term><term>Synchronisation</term><term>Noyau gris central</term><term>Stimulation cérébrale profonde</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">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 ∼20Hz 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.</div></front></TEI><affiliations><list><country><li>France</li><li>Royaume-Uni</li></country><region><li>Angleterre</li><li>Grand Londres</li><li>Provence-Alpes-Côte d'Azur</li></region><settlement><li>Londres</li><li>Marseille</li></settlement></list><tree><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Eusebio, Alexandre" sort="Eusebio, Alexandre" uniqKey="Eusebio A" first="Alexandre" last="Eusebio">Alexandre Eusebio</name></region><name sortKey="Averbeck, Bruno" sort="Averbeck, Bruno" uniqKey="Averbeck B" first="Bruno" last="Averbeck">Bruno Averbeck</name><name sortKey="Brown, Peter" sort="Brown, Peter" uniqKey="Brown P" first="Peter" last="Brown">Peter Brown</name><name sortKey="Doyle Gaynor, Louise" sort="Doyle Gaynor, Louise" uniqKey="Doyle Gaynor L" first="Louise" last="Doyle Gaynor">Louise Doyle Gaynor</name><name sortKey="Limousin, Patricia" sort="Limousin, Patricia" uniqKey="Limousin P" first="Patricia" last="Limousin">Patricia Limousin</name><name sortKey="Limousin, Patricia" sort="Limousin, Patricia" uniqKey="Limousin P" first="Patricia" last="Limousin">Patricia Limousin</name><name sortKey="Pogosyan, Alek" sort="Pogosyan, Alek" uniqKey="Pogosyan A" first="Alek" last="Pogosyan">Alek Pogosyan</name><name sortKey="Shouyan Wang" sort="Shouyan Wang" uniqKey="Shouyan Wang" last="Shouyan Wang">SHOUYAN WANG</name></country><country name="France"><region name="Provence-Alpes-Côte d'Azur"><name sortKey="Eusebio, Alexandre" sort="Eusebio, Alexandre" uniqKey="Eusebio A" first="Alexandre" last="Eusebio">Alexandre Eusebio</name></region><name sortKey="Azulay, Jean Philippe" sort="Azulay, Jean Philippe" uniqKey="Azulay J" first="Jean-Philippe" last="Azulay">Jean-Philippe Azulay</name><name sortKey="Cantiniaux, Stephanie" sort="Cantiniaux, Stephanie" uniqKey="Cantiniaux S" first="Stéphanie" last="Cantiniaux">Stéphanie Cantiniaux</name><name sortKey="Witjas, Tatiana" sort="Witjas, Tatiana" uniqKey="Witjas T" first="Tatiana" last="Witjas">Tatiana Witjas</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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