TMS-Induced Cortical Potentiation during Wakefulness Locally Increases Slow Wave Activity during Sleep

Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a...

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Published inPloS one Vol. 2; no. 3; p. e276
Main Authors Huber, Reto, Esser, Steve K., Ferrarelli, Fabio, Massimini, Marcello, Peterson, Michael J., Tononi, Giulio
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.03.2007
Public Library of Science (PLoS)
Subjects
Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0000276

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Abstract Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning. To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1+/-17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep. These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
AbstractList Background Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning. Methodology/Principal Findings To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1±17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep. Conclusions/Significance These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning. To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1+/-17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep. These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning. To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1±17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep. These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
Background Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning. Methodology/Principal Findings To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1±17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep. Conclusions/Significance These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning.To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1+/-17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep.These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning.BACKGROUNDSleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep. However, the process responsible for SWA regulation is not known. We showed recently that SWA increases locally after a learning task involving a circumscribed brain region, suggesting that SWA may reflect plastic changes triggered by learning.To test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1+/-17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep.METHODOLOGY/PRINCIPAL FINDINGSTo test this hypothesis directly, we used transcranial magnetic stimulation (TMS) in conjunction with high-density EEG in humans. We show that 5-Hz TMS applied to motor cortex induces a localized potentiation of TMS-evoked cortical EEG responses. We then show that, in the sleep episode following 5-Hz TMS, SWA increases markedly (+39.1+/-17.4%, p<0.01, n = 10). Electrode coregistration with magnetic resonance images localized the increase in SWA to the same premotor site as the maximum TMS-induced potentiation during wakefulness. Moreover, the magnitude of potentiation during wakefulness predicts the local increase in SWA during sleep.These results provide direct evidence for a link between plastic changes and the local regulation of sleep need.CONCLUSIONS/SIGNIFICANCEThese results provide direct evidence for a link between plastic changes and the local regulation of sleep need.
Audience Academic
Author Esser, Steve K.
Ferrarelli, Fabio
Tononi, Giulio
Huber, Reto
Peterson, Michael J.
Massimini, Marcello
AuthorAffiliation University of California, Irvine, United States of America
Department of Psychiatry, University of Wisconsin, Madison, Madison, Wisconsin, United States of America
AuthorAffiliation_xml – name: University of California, Irvine, United States of America
– name: Department of Psychiatry, University of Wisconsin, Madison, Madison, Wisconsin, United States of America
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  givenname: Reto
  surname: Huber
  fullname: Huber, Reto
– sequence: 2
  givenname: Steve K.
  surname: Esser
  fullname: Esser, Steve K.
– sequence: 3
  givenname: Fabio
  surname: Ferrarelli
  fullname: Ferrarelli, Fabio
– sequence: 4
  givenname: Marcello
  surname: Massimini
  fullname: Massimini, Marcello
– sequence: 5
  givenname: Michael J.
  surname: Peterson
  fullname: Peterson, Michael J.
– sequence: 6
  givenname: Giulio
  surname: Tononi
  fullname: Tononi, Giulio
BackLink https://www.ncbi.nlm.nih.gov/pubmed/17342210$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2007 Public Library of Science
2007 Huber et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Huber et al. 2007
Copyright_xml – notice: COPYRIGHT 2007 Public Library of Science
– notice: 2007 Huber et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Conceived and designed the experiments: RH GT SE. Performed the experiments: RH SE FF MM MP. Analyzed the data: RH SE. Contributed reagents/materials/analysis tools: RH SE FF MM. Wrote the paper: RH GT.
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Snippet Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during sleep....
Background Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during...
Background Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the length of prior wakefulness and decreasing during...
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SubjectTerms Brain
Brain Mapping - methods
Cerebral Cortex - physiology
Cortex
Cortex (motor)
Cortex (premotor)
EEG
Electrodes
Electroencephalography
Electromagnetism
Evoked Potentials - physiology
Homeostasis
Human subjects
Humans
Hypotheses
Laws, regulations and rules
Long-Term Potentiation - physiology
Magnetic fields
Magnetic resonance
Magnetic resonance imaging
Medical imaging
Motor Cortex - physiology
Neuroscience
Neuroscience/Neural Homeostasis
Neuroscience/Neuronal and Glial Cell Biology
Plasticity
Potentiation
Psychiatry
Sleep
Sleep - physiology
Sleep and wakefulness
Sleep Stages - physiology
Studies
Time Factors
Tomography
Transcranial Magnetic Stimulation
Wakefulness
Wakefulness - physiology
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Title TMS-Induced Cortical Potentiation during Wakefulness Locally Increases Slow Wave Activity during Sleep
URI https://www.ncbi.nlm.nih.gov/pubmed/17342210
https://www.proquest.com/docview/1289130645
https://www.proquest.com/docview/1950105344
https://www.proquest.com/docview/70238372
https://pubmed.ncbi.nlm.nih.gov/PMC1803030
https://doaj.org/article/14d84f85f4bc4be7b9be694dab8e84b0
http://dx.doi.org/10.1371/journal.pone.0000276
Volume 2
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