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Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep.

ABSTRACT: Sleep slow-wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the previous time awake and decreasing during sleep, although the underlying mechanisms are unclear. Recent studies have shown that procedures presumably leading to local plastic changes in the cerebral cortex can lead to local changes in SWA during subsequent sleep. To further investigate the connection between cortical plasticity and sleep SWA, in this study we used a paired associative stimulation (PAS) protocol, in which median nerve stimuli were followed at different intervals (25 or 10 ms) by transcranial magnetic stimulation (TMS) pulses to the contralateral cortical hand area. As expected, such a protocol led to a sustained increase (long-term potentiation-like) or decrease (long-term depression-like) of cortical excitability as measured by motor evoked potentials. By using a TMS-compatible high-density electroencephalographic (EEG) system, we also found that, in individual subjects, TMS-evoked cortical responses over sensorimotor cortex changed with different interstimulus intervals. Moreover, during subsequent sleep, SWA increased locally in subjects whose TMS-evoked cortical responses had increased after PAS, and decreased in subjects whose cortical responses had decreased. Changes in TMS-evoked cortical EEG response and change in sleep SWA were localized to similar cortical regions and were positively correlated. Together, these results suggest that changes in cortical excitability in opposite directions lead to corresponding changes in local sleep regulation, as reflected by SWA, providing evidence for a tight relationship between cortical plasticity and sleep intensity.

SUBMITTER: Huber R

PROVIDER: S-EPMC2809373 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep.

Huber Reto R Määttä Sara S Esser Steve K SK Sarasso Simone S Ferrarelli Fabio F Watson Adam A Ferreri Florinda F Peterson Michael J MJ Tononi Giulio G

The Journal of neuroscience : the official journal of the Society for Neuroscience 20080701 31

Sleep slow-wave activity (SWA) is thought to reflect sleep need, increasing in proportion to the previous time awake and decreasing during sleep, although the underlying mechanisms are unclear. Recent studies have shown that procedures presumably leading to local plastic changes in the cerebral cortex can lead to local changes in SWA during subsequent sleep. To further investigate the connection between cortical plasticity and sleep SWA, in this study we used a paired associative stimulation (PA ...[more]

PMID: 18667623

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Project description:OBJECTIVE:To determine whether neurophysiological mechanisms indicating cortical excitability, long-term potentiation (LTP)-like plasticity, GABAergic and glutamatergic function are altered in patients with anti-N-methyl-d-aspartate receptor (NMDAR) encephalitis and whether they can be helpful as markers of diagnostic assessment, disease progression, and potentially therapy response. METHODS:Neurophysiological characterizations of patients with NMDAR encephalitis (n = 34, mean age: 28 ± 11 years; 30 females) and age/gender-matched healthy controls (n = 27, 28.5 ± 10 years; 25 females) were performed using transcranial magnetic stimulation-derived protocols including resting motor threshold, recruitment curve, intracortical facilitation, short intracortical inhibition, and cortical silent period. Paired associative stimulation (PAS) was applied to assess LTP-like mechanisms which are mediated through NMDAR. Moreover, resting state functional connectivity was determined using functional magnetic resonance imaging. RESULTS:PAS-induced plasticity differed significantly between groups (P = 0.0056). Cortical excitability, as assessed via motor-evoked potentials after PAS, decreased in patients, whereas it increased in controls indicating malfunctioning of NMDAR in encephalitis patients. Lower PAS-induced plasticity significantly correlated with the modified Rankin Scale (mRS) (r = -0.41; P = 0.0031) and was correlated with lower functional connectivity within the motor network in NMDAR encephalitis patients (P < 0.001, uncorrected). Other neurophysiological parameters were not significantly different between groups. Follow-up assessments were available in six patients and demonstrated parallel improvement of PAS-induced plasticity and mRS. INTERPRETATION:Assessment of PAS-induced plasticity may help to determine NMDAR dysfunction and disease severity in NMDAR encephalitis, and might even aid as a sensitive, noninvasive, and well-tolerated "electrophysiological biomarker" to monitor therapy response in the future. CLINICAL TRIAL REGISTRATION:ClinicalTrials.gov: Identifier: NCT01865578.

Project description:Paired associative stimulation is a relatively new non-invasive brain stimulation technique that combines transcranial magnetic stimulation and peripheral nerve stimulation. The effects of paired associative stimulation on the excitability of the cerebral cortex can vary according to the time interval between the transcranial magnetic stimulation and peripheral nerve stimulation. We established a model of cerebral ischemia in rats via transient middle cerebral artery occlusion. We administered paired associative stimulation with a frequency of 0.05 Hz 90 times over 4 weeks. We then evaluated spatial learning and memory using the Morris water maze. Changes in the cerebral ultra-structure and synaptic plasticity were assessed via transmission electron microscopy and a 64-channel multi-electrode array. We measured mRNA and protein expression levels of brain-derived neurotrophic factor and N-methyl-D-aspartate receptor 1 in the hippocampus using a real-time polymerase chain reaction and western blot assay. Paired associative stimulation treatment significantly improved learning and memory in rats subjected to cerebral ischemia. The ultra-structures of synapses in the CA1 area of the hippocampus in rats subjected to cerebral ischemia were restored by paired associative stimulation. Long-term potentiation at synapses in the CA3 and CA1 regions of the hippocampus was enhanced as well. The protein and mRNA expression of brain-derived neurotrophic factor and N-methyl-D-aspartate receptor 1 increased after paired associative stimulation treatment. These data indicate that paired associative stimulation can protect cognition after cerebral ischemia. The observed effect may be mediated by increases in the mRNA and protein expression of brain-derived neurotrophic factor and N-methyl-D-aspartate receptor 1, and by enhanced synaptic plasticity in the CA1 area of the hippocampus. The animal experiments were approved by the Animal Ethics Committee of Tongji Medical College, Huazhong University of Science & Technology, China (approval No. TJ-A20151102) on July 11, 2015.

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Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep.

Publications

Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep.

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