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      Cortical Plasticity Induced by Transcranial Magnetic Stimulation during Wakefulness Affects Electroencephalogram Activity during Sleep

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          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.

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          Most cited references 38

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          Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee.

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            Learning-induced LTP in neocortex.

            The hypothesis that learning occurs through long-term potentiation (LTP)- and long-term depression (LTD)-like mechanisms is widely held but unproven. This hypothesis makes three assumptions: Synapses are modifiable, they modify with learning, and they strengthen through an LTP-like mechanism. We previously established the ability for synaptic modification and a synaptic strengthening with motor skill learning in horizontal connections of the rat motor cortex (MI). Here we investigated whether learning strengthened these connections through LTP. We demonstrated that synapses in the trained MI were near the ceiling of their modification range, compared with the untrained MI, but the range of synaptic modification was not affected by learning. In the trained MI, LTP was markedly reduced and LTD was enhanced. These results are consistent with the use of LTP to strengthen synapses during learning.
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              Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity.

              Motor and visual cortices of normal volunteers were activated by transcranial magnetic stimulation. The electrical brain activity resulting from the brief electromagnetic pulse was recorded with high-resolution electroencephalography (HR-EEG) and located using inversion algorithms. The stimulation of the left sensorimotor hand area elicited an immediate response at the stimulated site. The activation had spread to adjacent ipsilateral motor areas within 5-10 ms and to homologous regions in the opposite hemisphere within 20 ms. Similar activation patterns were generated by magnetic stimulation of the visual cortex. This new non-invasive method provides direct information about cortical reactivity and area-to-area neuronal connections.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                25 June 2008
                : 3
                : 6
                Affiliations
                [1 ]Department of Psychology, University of Rome “La Sapienza”, Rome, Italy
                [2 ]IRCCS Centro S. Giovanni di Dio, Hosp. Fatebenefratelli, Brescia, Italy
                [3 ]Casa di Cura S. Raffaele Cassino and IRCCS S. Raffaele Pisana, Roma, Italy
                [4 ]Laboratory of Sleep Psychophysiology, Faculty of Psychology, University of L'Aquila, L'Aquila, Italy
                [5 ]Department of Internal Medicine and Public Health, University of L'Aquila, L'Aquila, Italy
                [6 ]AFaR, Department of Neuroscience, Hosp. Fatebenefratelli, Isola Tiberina, Rome, Italy
                [7 ]Neurology Clinic, University Campus Biomedico, Rome, Italy
                University of Southern California, United States of America
                Author notes

                Conceived and designed the experiments: MF LD PR. Performed the experiments: FM GC FF CM MP DT CP. Analyzed the data: LD. Wrote the paper: LD.

                Article
                08-PONE-RA-03834R2
                10.1371/journal.pone.0002483
                2423620
                18575583
                De Gennaro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 12
                Categories
                Research Article
                Neuroscience/Neural Homeostasis

                Uncategorized

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