Time and Frequency-Dependent Modulation of Local Field Potential Synchronization by Deep Brain Stimulation
Identifieur interne : 000B14 ( Pmc/Curation ); précédent : 000B13; suivant : 000B15Time and Frequency-Dependent Modulation of Local Field Potential Synchronization by Deep Brain Stimulation
Auteurs : Clinton B. Mccracken ; Zelma H. T. KissSource :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
High-frequency electrical stimulation of specific brain structures, known as deep brain stimulation (DBS), is an effective treatment for movement disorders, but mechanisms of action remain unclear. We examined the time-dependent effects of DBS applied to the entopeduncular nucleus (EP), the rat homolog of the internal globus pallidus, a target used for treatment of both dystonia and Parkinson’s disease (PD). We performed simultaneous multi-site local field potential (LFP) recordings in urethane-anesthetized rats to assess the effects of high-frequency (HF, 130 Hz; clinically effective), low-frequency (LF, 15 Hz; ineffective) and sham DBS delivered to EP. LFP activity was recorded from dorsal striatum (STR), ventroanterior thalamus (VA), primary motor cortex (M1), and the stimulation site in EP. Spontaneous and acute stimulation-induced LFP oscillation power and functional connectivity were assessed at baseline, and after 30, 60, and 90 minutes of stimulation. HF EP DBS produced widespread alterations in spontaneous and stimulus-induced LFP oscillations, with some effects similar across regions and others occurring in a region- and frequency band-specific manner. Many of these changes evolved over time. HF EP DBS produced an initial transient reduction in power in the low beta band in M1 and STR; however, phase synchronization between these regions in the low beta band was markedly suppressed at all time points. DBS also enhanced low gamma synchronization throughout the circuit. With sustained stimulation, there were significant reductions in low beta synchronization between M1-VA and STR-VA, and increases in power within regions in the faster frequency bands. HF DBS also suppressed the ability of acute EP stimulation to induce beta oscillations in all regions along the circuit. This dynamic pattern of synchronizing and desynchronizing effects of EP DBS suggests a complex modulation of activity along cortico-BG-thalamic circuits underlying the therapeutic effects of GPi DBS for conditions such as PD and dystonia.
Url:
DOI: 10.1371/journal.pone.0102576
PubMed: 25029468
PubMed Central: 4100931
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Time and Frequency-Dependent Modulation of Local Field Potential Synchronization by Deep Brain Stimulation</title><author><name sortKey="Mccracken, Clinton B" sort="Mccracken, Clinton B" uniqKey="Mccracken C" first="Clinton B." last="Mccracken">Clinton B. Mccracken</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Kiss, Zelma H T" sort="Kiss, Zelma H T" uniqKey="Kiss Z" first="Zelma H. T." last="Kiss">Zelma H. T. Kiss</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25029468</idno><idno type="pmc">4100931</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4100931</idno><idno type="RBID">PMC:4100931</idno><idno type="doi">10.1371/journal.pone.0102576</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000B14</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B14</idno><idno type="wicri:Area/Pmc/Curation">000B14</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000B14</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Time and Frequency-Dependent Modulation of Local Field Potential Synchronization by Deep Brain Stimulation</title><author><name sortKey="Mccracken, Clinton B" sort="Mccracken, Clinton B" uniqKey="Mccracken C" first="Clinton B." last="Mccracken">Clinton B. Mccracken</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Kiss, Zelma H T" sort="Kiss, Zelma H T" uniqKey="Kiss Z" first="Zelma H. T." last="Kiss">Zelma H. T. Kiss</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>High-frequency electrical stimulation of specific brain structures, known as deep brain stimulation (DBS), is an effective treatment for movement disorders, but mechanisms of action remain unclear. We examined the time-dependent effects of DBS applied to the entopeduncular nucleus (EP), the rat homolog of the internal globus pallidus, a target used for treatment of both dystonia and Parkinson’s disease (PD). We performed simultaneous multi-site local field potential (LFP) recordings in urethane-anesthetized rats to assess the effects of high-frequency (HF, 130 Hz; clinically effective), low-frequency (LF, 15 Hz; ineffective) and sham DBS delivered to EP. LFP activity was recorded from dorsal striatum (STR), ventroanterior thalamus (VA), primary motor cortex (M1), and the stimulation site in EP. Spontaneous and acute stimulation-induced LFP oscillation power and functional connectivity were assessed at baseline, and after 30, 60, and 90 minutes of stimulation. HF EP DBS produced widespread alterations in spontaneous and stimulus-induced LFP oscillations, with some effects similar across regions and others occurring in a region- and frequency band-specific manner. Many of these changes evolved over time. HF EP DBS produced an initial transient reduction in power in the low beta band in M1 and STR; however, phase synchronization between these regions in the low beta band was markedly suppressed at all time points. DBS also enhanced low gamma synchronization throughout the circuit. With sustained stimulation, there were significant reductions in low beta synchronization between M1-VA and STR-VA, and increases in power within regions in the faster frequency bands. HF DBS also suppressed the ability of acute EP stimulation to induce beta oscillations in all regions along the circuit. This dynamic pattern of synchronizing and desynchronizing effects of EP DBS suggests a complex modulation of activity along cortico-BG-thalamic circuits underlying the therapeutic effects of GPi DBS for conditions such as PD and dystonia.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Rodriguez Oroz, Mc" uniqKey="Rodriguez Oroz M">MC Rodriguez-Oroz</name></author><author><name sortKey="Obeso, Ja" uniqKey="Obeso J">JA Obeso</name></author><author><name sortKey="Lang, Ae" uniqKey="Lang A">AE Lang</name></author><author><name sortKey="Houeto, Jl" uniqKey="Houeto J">JL Houeto</name></author><author><name sortKey="Pollak, P" uniqKey="Pollak P">P Pollak</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kupsch, A" uniqKey="Kupsch A">A Kupsch</name></author><author><name sortKey="Benecke, R" uniqKey="Benecke R">R Benecke</name></author><author><name sortKey="Muller, J" uniqKey="Muller J">J 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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">25029468</article-id><article-id pub-id-type="pmc">4100931</article-id><article-id pub-id-type="publisher-id">PONE-D-14-05032</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0102576</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 and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Nervous System</subject><subj-group><subject>Motor System</subject></subj-group></subj-group></subj-group><subj-group><subject>Neuroscience</subject><subj-group><subject>Neural Networks</subject></subj-group></subj-group><subj-group><subject>Physiology</subject><subj-group><subject>Electrophysiology</subject><subject>Nervous System Physiology</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Time and Frequency-Dependent Modulation of Local Field Potential Synchronization by Deep Brain Stimulation</article-title><alt-title alt-title-type="running-head">Entopeduncular Nucleus DBS Alters LFP Synchronization</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>McCracken</surname><given-names>Clinton B.</given-names></name><xref ref-type="aff" rid="aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Kiss</surname><given-names>Zelma H. T.</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><addr-line>Department of Clinical Neurosciences and Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Tort</surname><given-names>Adriano B. L.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Federal University of Rio Grande do Norte, Brazil</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>zkiss@ucalgary.ca</email></corresp><fn fn-type="conflict"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: CM ZK. Performed the experiments: CM. Analyzed the data: CM. Wrote the paper: CM ZK.</p></fn></author-notes><pub-date pub-type="collection"><year>2014</year></pub-date><pub-date pub-type="epub"><day>16</day><month>7</month><year>2014</year></pub-date><volume>9</volume><issue>7</issue><elocation-id>e102576</elocation-id><history><date date-type="received"><day>3</day><month>2</month><year>2014</year></date><date date-type="accepted"><day>20</day><month>6</month><year>2014</year></date></history><permissions><copyright-year>2014</copyright-year><copyright-holder>McCracken, Kiss</copyright-holder><license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><abstract><p>High-frequency electrical stimulation of specific brain structures, known as deep brain stimulation (DBS), is an effective treatment for movement disorders, but mechanisms of action remain unclear. We examined the time-dependent effects of DBS applied to the entopeduncular nucleus (EP), the rat homolog of the internal globus pallidus, a target used for treatment of both dystonia and Parkinson’s disease (PD). We performed simultaneous multi-site local field potential (LFP) recordings in urethane-anesthetized rats to assess the effects of high-frequency (HF, 130 Hz; clinically effective), low-frequency (LF, 15 Hz; ineffective) and sham DBS delivered to EP. LFP activity was recorded from dorsal striatum (STR), ventroanterior thalamus (VA), primary motor cortex (M1), and the stimulation site in EP. Spontaneous and acute stimulation-induced LFP oscillation power and functional connectivity were assessed at baseline, and after 30, 60, and 90 minutes of stimulation. HF EP DBS produced widespread alterations in spontaneous and stimulus-induced LFP oscillations, with some effects similar across regions and others occurring in a region- and frequency band-specific manner. Many of these changes evolved over time. HF EP DBS produced an initial transient reduction in power in the low beta band in M1 and STR; however, phase synchronization between these regions in the low beta band was markedly suppressed at all time points. DBS also enhanced low gamma synchronization throughout the circuit. With sustained stimulation, there were significant reductions in low beta synchronization between M1-VA and STR-VA, and increases in power within regions in the faster frequency bands. HF DBS also suppressed the ability of acute EP stimulation to induce beta oscillations in all regions along the circuit. This dynamic pattern of synchronizing and desynchronizing effects of EP DBS suggests a complex modulation of activity along cortico-BG-thalamic circuits underlying the therapeutic effects of GPi DBS for conditions such as PD and dystonia.</p></abstract><funding-group><funding-statement>This work was supported by a grant from the Canadian Institutes of Health Research. Dr. Kiss is a Clinical Scholar of the Alberta Heritage Foundation for Medical Research. Dr. McCracken received fellowship support from Parkinson Society Canada and Hotchkiss Brain Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="13"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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