Effects of Skilled Training on Sleep Slow Wave Activity and Cortical Gene Expression in the Rat

Abstract

SO FAR. IN MAMMALS, THE BEST CHARACTERIZED marker of sleep homeostasis is slow wave activity (SWA), the power density in the electroencephalogram (EEG) between 0.5 and 4 Hz during NREM sleep. SWA is high at sleep onset and declines during sleep, suggesting that it may reflect the accumulation of sleep pressure as a function of duration and/or intensity of prior waking. 1,2 Why and how SWA should reflect sleep homeostasis, however, is still unclear.We hypothesized that SWA is high at sleep onset because it reflects the occurrence, during waking, of widespread synaptic potentiation in cortical and subcortical areas. 3,4 This increase would be detrimental in the long term, because stronger synapses need more energy, space, and cellular supplies, and may lead to saturation of the ability to learn. Sleep would thus be crucial to renormalize synaptic strength to an energetically sustainable level. Molecular and electrophysiological markers of synaptic potentiation increase after waking in rat cortex and hippocampus, while markers of synaptic depression do so after sleep. 5,6 Moreover, in rats and humans, procedures presumably leading to synaptic potentiation or depression result in SWA increases and decreases, respectively. 7-12 More specifically, a study in humans using highdensity EEG found that performing a visuomotor learning task produced a local increase in SWA during subsequent sleep. 7 The increase was restricted to the right parietal cortical areas presumably modified by learning. 13 Moreover, it was specific for NREM sleep, reversible within the first 90 minutes of sleep, and correlated with the improvement in performance after sleep. 7 However, there is no direct evidence that the motor adaptation task used in that study activates neurons in parietal cortex, nor that it causes synaptic potentiation specifically in that region.Previous studies have suggested that activity-dependent genes activated during a specific waking experience may be reactivated during sleep, perhaps to potentiate the same synapses previously engaged during waking. 14 Ribeiro and colleagues found that the exposure to a new environment for 3 hours 15 results in the immediate cortical and hippocampal induction, during waking, of plasticity-related gene zif-268, 16 followed by its downregulation during NREM sleep, and then again by its increased expression during REM sleep (relative to NREM sleep). Intriguingly ~ 3 min of NREM sleep were enough to downregulate waking-induced zif-268 expression, and ~ 2 min of REM sleep were sufficient to detect its selective reinduction, even if both NREM and REM rats were awake during the last 30 min before sacrifice. Another study 17 recently found, using fluorescent in situ hybridization, that the number of hippocampal CA1 neurons showing induction of Arc and/or Homer1a was similar during "rest" periods before and after the exploration of a new environment. However, more cells were active during both exploration and post-task rest than during exploration and pre-task rest. Based on these findings, it h...

Sleep Slow-Wave Activity Reveals Developmental Changes in Experience-Dependent Plasticity

“…In the post-learning night, we observed a gain in SWA in a cluster of eight electrodes over the right parietal scalp that was strongest in children compared with adolescents and adults. The finding of increased local SWA in a region that is known to be recruited during task performance is in line with a number of previous experiments in humans and rodents reporting a link between learning experiences during the wake phase and local SWA during subsequent sleep (Kattler et al, 1994;Huber et al, 2004Huber et al, , 2006Hanlon et al, 2009;Mascetti et al, 2013). SWA in the surface EEG reflects a highly synchronous alternating pattern of neuronal firing (depolarization) and neuronal silence (hyperpolarization) in large neuronal networks (Steriade et al, 1993).…”

“…An increase in synaptic density and efficacy has been shown to enhance neuronal synchronization, which in turn results in increased sleep slow-wave activity (SWA;Esser et al, 2007;Dash et al, 2009;; EEG activity at a frequency of 1-4.5 Hz that hallmarks deep slow-wave sleep). Specific learning experiences involving, for instance, intense visuomotor adaptation during the day resulted in an increase in post-learning SWA specifically over the cortical region that was shown to be involved during learning Hanlon et al, 2009;Landsness et al, 2009;Määttä et al, 2010;Mascetti et al, 2013). Brain maturation is another factor that strongly affects sleep SWA.…”

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

“…It has been proposed that such a response may reflect frequency-independent increases in neuronal synchrony owing to a strengthening of synapses during prior wakefulness [24], but the activity in the mesopallium seemingly argues against this idea. While the low frequencies of the SWA bandwidth increased symmetrically in the mesopallium during recovery sleep, faster frequencies (6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18) were asymmetric between the left and right mesopallia, with the mesopallium contralateral to the stimulated eye showing lower activity. Although the functional significance of this asymmetry remains unclear, three points are noteworthy.…”

“…Regardless of the specific mechanism(s) by which SWS facilitates downscaling, several lines of evidence suggest that synapses weaken during SWS [4,7,42 -46,52,58,59]. In addition to maintaining synaptic weights at an optimum level, synaptic homeostasis can also account for some of the enhancements in performance on various cognitive tasks observed in mammals post-sleep [11,12,14,15], perhaps by increasing the signal-to-noise ratio of relevant circuits [59,67]. Although recent evidence suggests that sleep plays a role in imprinting [68], auditory discrimination [69] and song learning [70 -74] in birds, the role (if any) of synaptic downscaling in these processes is unknown.…”

Epileptic Activity and Cognitive Impairment: Hijacking Plasticity during Sleep

“…In humans and animals, both global and regional sleep SWA power have been shown to increase after learning new tasks (6,7). Boly et al proposed that epileptic activity in adults can negatively impact sleep SWA power, and the negative slope of sleep slow waves, and correlate with cognitive impairment.…”