Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep

Luigi De Gennaro, Fabiana Fratello, Cristina Marzano, Fabio Moroni, Giuseppe Curcio, Daniela Tempesta, Maria Concetta Pellicciari, Cornelia Pirulli, Michele Ferrara, Paolo Maria Rossini

Research output: Contribution to journalArticle

40 Citations (Scopus)

Abstract

Background: Sleep electroencephalogram (EEG) brain oscillations in the low-frequency range show local signs of homeostatic regulation after learning. Such increases and decreases of slow wave activity are limited to the cortical regions involved in specific task performance during wakefulness. Here, we test the hypothesis that reorganization of motor cortex produced by long-term potentiation (LTP) affects EEG activity of this brain area during subsequent sleep. Methodology/Principal Findings: By pairing median nerve stimulation with transcranial magnetic stimulation over the contralateral motor cortex, one can potentiate the motor output, which is presumed to reflect plasticity of the neural circuitry. This paired associative stimulation increases M1 cortical excitability at interstimulus intervals of 25 ms. We compared the scalp distribution of sleep EEG power following paired associative stimulation at 25 ms to that following a control paradigm with 50 ms intervals. It is shown that the experimental manipulation by paired associative stimulation at 25 ms induces a 48% increase in amplitude of motor evoked potentials. This LTP-like potentiation, induced during waking, affects delta and theta EEG power in both REM and non-REM sleep, measured during the following night. Slow-wave activity increases in some frontal and prefrontal derivations and decreases at sites neighboring and contralateral to the stimulated motor cortex. The magnitude of increased amplitudes of motor evoked potentials by the paired associative stimulation at 25 ms predicts enhancements of slow-wave activity in prefrontal regions. Conclusions/Significance: An LTP-like paradigm, presumably inducing increased synaptic strength, leads to changes in local sleep regulation, as indexed by EEG slow-wave activity. Enhancement and depression of slow-wave activity are interpreted in terms of a simultaneous activation of both excitatory and inhibitory circuits consequent to the paired associative stimulation at 25 ms.

Original languageEnglish
Article numbere2483
JournalPLoS One
Volume3
Issue number6
DOIs
Publication statusPublished - Jun 25 2008

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electroencephalography
Transcranial Magnetic Stimulation
Wakefulness
Electroencephalography
sleep
Plasticity
Sleep
Long-Term Potentiation
Motor Cortex
Motor Evoked Potentials
evoked potentials
Bioelectric potentials
Brain
brain
Thermodynamic properties
Neuronal Plasticity
Median Nerve
Task Performance and Analysis
Scalp
oscillation

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep. / De Gennaro, Luigi; Fratello, Fabiana; Marzano, Cristina; Moroni, Fabio; Curcio, Giuseppe; Tempesta, Daniela; Pellicciari, Maria Concetta; Pirulli, Cornelia; Ferrara, Michele; Rossini, Paolo Maria.

In: PLoS One, Vol. 3, No. 6, e2483, 25.06.2008.

Research output: Contribution to journalArticle

De Gennaro, L, Fratello, F, Marzano, C, Moroni, F, Curcio, G, Tempesta, D, Pellicciari, MC, Pirulli, C, Ferrara, M & Rossini, PM 2008, 'Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep', PLoS One, vol. 3, no. 6, e2483. https://doi.org/10.1371/journal.pone.0002483
De Gennaro, Luigi ; Fratello, Fabiana ; Marzano, Cristina ; Moroni, Fabio ; Curcio, Giuseppe ; Tempesta, Daniela ; Pellicciari, Maria Concetta ; Pirulli, Cornelia ; Ferrara, Michele ; Rossini, Paolo Maria. / Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep. In: PLoS One. 2008 ; Vol. 3, No. 6.
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