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Abstract
BackgroundSleep 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 FindingsBy 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/SignificanceAn 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.
Highlights
According to the two-process model of sleep regulation, the timing of sleep and wakefulness is modulated by the interaction of a homeostatic process, ‘‘Process S’’, and by a circadian process, ‘‘Process C’’ [1]
To give further support to the hypothesis of a causal link between the increase in motor evoked potentials during wakefulness, induced by long-term potentiation (LTP)-like stimulation, and the magnitude of the slow-wave activity (SWA) changes during sleep, we examined whether changes in SWA topography both in NREM and REM sleep are predicted by the increase of motor evoked potentials in paired associative stimulation at 25-ms intervals (PAS-25)
The positive correlation between the spatial pattern of SWA changes and the magnitude of the plastic changes associated to paired associative stimulation at 25 ms in the whole night’s sleep supports the hypothesis of a relationship between LTP-like changes and sleep need, the latter expressed by the regional increase of SWA
Summary
According to the two-process model of sleep regulation, the timing of sleep and wakefulness is modulated by the interaction of a homeostatic process, ‘‘Process S’’, and by a circadian process, ‘‘Process C’’ [1]. Well established evidence on the homeostatic regulation of sleep suggests that slow-wave activity, i.e. EEG power in the 0.50–4.75 Hz range, depends on the duration of previous sleep and wakefulness, representing a marker of non-REM (NREM) sleep intensity [2]. This feature of sleep has consistently been shown in a broad range of species, including humans, cats, mice, rats, and squirrels [3]. 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. 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
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