Response of Human Thalamic Neurons to High-Frequency Stimulation
Identifieur interne : 000940 ( Main/Exploration ); précédent : 000939; suivant : 000941Response of Human Thalamic Neurons to High-Frequency Stimulation
Auteurs : Merrill J. Birdno [États-Unis] ; Wei Tang [Canada] ; Jonathan O. Dostrovsky [Canada] ; William D. Hutchison [Canada] ; Warren M. Grill [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
Thalamic deep brain stimulation (DBS) is an effective treatment for tremor, but the mechanisms of action remain unclear. Previous studies of human thalamic neurons to noted transient rebound bursting activity followed by prolonged inhibition after cessation of high frequency extracellular stimulation, and the present study sought to identify the mechanisms underlying this response. Recordings from 13 thalamic neurons exhibiting low threshold spike (LTS) bursting to brief periods of extracellular stimulation were made during surgeries to implant DBS leads in 6 subjects with Parkinson's disease. The response immediately after cessation of stimulation included a short epoch of burst activity, followed by a prolonged period of silence before a return to LTS bursting. A computational model of a population of thalamocortical relay neurons and presynaptic axons terminating on the neurons was used to identify cellular mechanisms of the observed responses. The model included the actions of neuromodulators through inhibition of a non-pertussis toxin sensitive K+ current (IKL), activation of a pertussis toxin sensitive K+ current (IKG), and a shift in the activation curve of the hyperpolarization-activated cation current (Ih). The model replicated well the measured responses, and the prolonged inhibition was associated most strongly with changes in IKG while modulation of IKL or Ih had minimal effects on post-stimulus inhibition suggesting that neuromodulators released in response to high frequency stimulation are responsible for mediating the post-stimulation bursting and subsequent long duration silence of thalamic neurons. The modeling also indicated that the axons of the model neurons responded robustly to suprathreshold stimulation despite the inhibitory effects on the soma. The findings suggest that during DBS the axons of thalamocortical neurons are activated while the cell bodies are inhibited thus blocking the transmission of pathological signals through the network and replacing them with high frequency regular firing.
Url:
DOI: 10.1371/journal.pone.0096026
PubMed: 24804767
PubMed Central: 4013084
Affiliations:
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Grill</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Biomedical Engineering, Duke University, Durham, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biomedical Engineering, Duke University, Durham, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Electrical and Computer Engineering, Duke University, Durham, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Electrical and Computer Engineering, Duke University, Durham, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Department of Neurobiology, Duke University, Durham, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Neurobiology, Duke University, Durham, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Surgery, Duke University, Durham, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, Duke University, Durham, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></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>Thalamic deep brain stimulation (DBS) is an effective treatment for tremor, but the mechanisms of action remain unclear. Previous studies of human thalamic neurons to noted transient rebound bursting activity followed by prolonged inhibition after cessation of high frequency extracellular stimulation, and the present study sought to identify the mechanisms underlying this response. Recordings from 13 thalamic neurons exhibiting low threshold spike (LTS) bursting to brief periods of extracellular stimulation were made during surgeries to implant DBS leads in 6 subjects with Parkinson's disease. The response immediately after cessation of stimulation included a short epoch of burst activity, followed by a prolonged period of silence before a return to LTS bursting. A computational model of a population of thalamocortical relay neurons and presynaptic axons terminating on the neurons was used to identify cellular mechanisms of the observed responses. The model included the actions of neuromodulators through inhibition of a non-pertussis toxin sensitive K<sup>+</sup> current (I<sub>KL</sub>), activation of a pertussis toxin sensitive K<sup>+</sup> current (I<sub>KG</sub>), and a shift in the activation curve of the hyperpolarization-activated cation current (I<sub>h</sub>). The model replicated well the measured responses, and the prolonged inhibition was associated most strongly with changes in I<sub>KG</sub> while modulation of I<sub>KL</sub> or I<sub>h</sub> had minimal effects on post-stimulus inhibition suggesting that neuromodulators released in response to high frequency stimulation are responsible for mediating the post-stimulation bursting and subsequent long duration silence of thalamic neurons. The modeling also indicated that the axons of the model neurons responded robustly to suprathreshold stimulation despite the inhibitory effects on the soma. The findings suggest that during DBS the axons of thalamocortical neurons are activated while the cell bodies are inhibited thus blocking the transmission of pathological signals through the network and replacing them with high frequency regular firing.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Birdno, Mj" uniqKey="Birdno M">MJ Birdno</name></author><author><name sortKey="Grill, Wm" uniqKey="Grill W">WM Grill</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Benabid, Al" uniqKey="Benabid A">AL Benabid</name></author><author><name sortKey="Pollak, P" uniqKey="Pollak P">P Pollak</name></author><author><name sortKey="Gervason, C" uniqKey="Gervason C">C Gervason</name></author><author><name sortKey="Hoffmann, D" uniqKey="Hoffmann D">D Hoffmann</name></author><author><name sortKey="Gao, Dm" uniqKey="Gao D">DM Gao</name></author></analytic></biblStruct><biblStruct><analytic><author><name 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uniqKey="Bruet N">N Bruet</name></author><author><name sortKey="Poupard, A" uniqKey="Poupard A">A Poupard</name></author><author><name sortKey="Feuerstein, C" uniqKey="Feuerstein C">C Feuerstein</name></author><author><name sortKey="Bertrand, A" uniqKey="Bertrand A">A Bertrand</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Canada</li><li>États-Unis</li></country><region><li>Caroline du Nord</li><li>Ontario</li></region><settlement><li>Toronto</li></settlement><orgName><li>Université de Toronto</li></orgName></list><tree><country name="États-Unis"><region name="Caroline du Nord"><name sortKey="Birdno, Merrill J" sort="Birdno, Merrill J" uniqKey="Birdno M" first="Merrill J." last="Birdno">Merrill J. Birdno</name></region><name sortKey="Grill, Warren M" sort="Grill, Warren M" uniqKey="Grill W" first="Warren M." last="Grill">Warren M. Grill</name><name sortKey="Grill, Warren M" sort="Grill, Warren M" uniqKey="Grill W" first="Warren M." last="Grill">Warren M. Grill</name><name sortKey="Grill, Warren M" sort="Grill, Warren M" uniqKey="Grill W" first="Warren M." last="Grill">Warren M. Grill</name><name sortKey="Grill, Warren M" sort="Grill, Warren M" uniqKey="Grill W" first="Warren M." last="Grill">Warren M. Grill</name></country><country name="Canada"><region name="Ontario"><name sortKey="Tang, Wei" sort="Tang, Wei" uniqKey="Tang W" first="Wei" last="Tang">Wei Tang</name></region><name sortKey="Dostrovsky, Jonathan O" sort="Dostrovsky, Jonathan O" uniqKey="Dostrovsky J" first="Jonathan O." last="Dostrovsky">Jonathan O. Dostrovsky</name><name sortKey="Dostrovsky, Jonathan O" sort="Dostrovsky, Jonathan O" uniqKey="Dostrovsky J" first="Jonathan O." last="Dostrovsky">Jonathan O. Dostrovsky</name><name sortKey="Hutchison, William D" sort="Hutchison, William D" uniqKey="Hutchison W" first="William D." last="Hutchison">William D. Hutchison</name><name sortKey="Hutchison, William D" sort="Hutchison, William D" uniqKey="Hutchison W" first="William D." last="Hutchison">William D. Hutchison</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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