EEG sigma and slow‐wave activity during NREM sleep correlate with overnight declarative and procedural memory consolidation

Abstract

SUMMARYPrevious studies suggest that sleep-specific brain activity patterns such as sleep spindles and electroencephalographic slow-wave activity contribute to the consolidation of novel memories. The generation of both sleep spindles and slow-wave activity relies on synchronized oscillations in a thalamo-cortical network that might be implicated in synaptic strengthening (spindles) and downscaling (slow-wave activity) during sleep. This study further examined the association between electroencephalographic power during non-rapid eye movement sleep in the spindle (sigma, 12-16 Hz) and slow-wave frequency range (0.1-3.5 Hz) and overnight memory consolidation in 20 healthy subjects (10 men, 27.1 ± 4.6 years). We found that both electroencephalographic sigma power and slow-wave activity were positively correlated with the pre-post-sleep consolidation of declarative (word list) and procedural (mirror-tracing) memories. These results, although only correlative in nature, are consistent with the view that processes of synaptic strengthening (sleep spindles) and synaptic downscaling (slow-wave activity) might act in concert to promote synaptic plasticity and the consolidation of both declarative and procedural memories during sleep. IN TROD UCTI ONEvidence from molecular to behavioural studies indicates that sleep fosters learning, memory and underlying neural plasticity (Diekelmann and Born, 2010). However, the contribution of the predominant sleep stages, rapid eye movement (REM) and non-REM (NREM) sleep, and of associated neural processes to the consolidation of newly encoded memories in the major memory systems, declarative and non-declarative memory, remains to be further elucidated.Recent findings suggest that sleep spindles, brief but powerful bursts of synchronous neuronal firing during mammalian stage 2 sleep in the electroencephalogram (EEG) sigma range (12-16 Hz), and EEG slow-wave activity (SWA), highly-synchronized oscillations during NREM sleep (0.1-3.5 Hz), might represent oscillatory activity that promotes sleep-related synaptic plasticity (Rosanova and Ulrich, 2005;Tononi and Cirelli, 2006). Animal studies indicate that sleep spindles might foster intracellular Ca 2+ -dependent mechanisms leading to the consolidation of new memories through synaptic strengthening (Steriade, 2003). In contrast, SWA and underlying Ôdown-statesÕ of extensive hyperpolarization and neuronal silencing and subsequent Ôup-statesÕ of depolarization and intense neuronal firing (Steriade, 2006) might sharpen the information-to-noise ratio and novel memory representations through synaptic downscaling (Tononi and Cirelli, 2006).Earlier work proposed that NREM sleep might preferentially promote declarative memory, whereas REM sleep might predominantly facilitate non-declarative learning (Plihal and Born, 1997). Consistently, NREM sleep-related sleep spindle density has been shown to be enhanced during nocturnal sleep following training on a declarative word-pair association task (Gais et al., 2002). Additionally, the increase in sle...

About Sleep's Role in Memory

“…In some studies the increase in spindle activity was topographically restricted to the cortex areas most strongly involved in skill performance, i.e., in the contralateral motor cortex after motor tapping training (862) and in the parietal cortex after training in a visuospatial skill (214). Also, correlations between different parameters of spindle activity or stage 2 sleep and overnight improvements in motor skills have been consistently reported (562,862,1216,1286,1287), and these correlations were revealed for fast rather than slow spindles, in the studies distinguishing these two spindle types (59, 962,1174).…”

“…In rats, robust increases in sleep spindles (12)(13)(14)(15) Hz) were observed after learning odor-reward associations (354) and after avoidance training (397). Furthermore, indicators of sleep spindle expression consistently correlated with the amount of overnight retention of declarative memories (86,213,214,235,446,562,822,1016,1024,1037,1044,1057). Interestingly, spindle activity (11)(12)(13)(14)(15) Hz) also correlated with signs of overnight lexical integration of newly learned information, suggesting that spindles contribute to the integration of new memories into existing neocortical knowledge networks (1175).…”

System Consolidation During Sleep – A Common Principle Underlying Psychological and Immunological Memory Formation

“…Numerous studies have demonstrated the importance of SWS and associated EEG slow oscillatory activity for the consolidation of hippocampus-dependent psychological memories [4,82]. Immunological studies identified SWS as part of the immune response that facilitates recovery from infections [69,83].…”

Modulation of Total Sleep Time by Transcranial Direct Current Stimulation (tDCS)

“…Sleep EEG spectral analysis was carried out to assess power spectra as described previously (eg, Holz et al, 2012;Nissen et al, 2001). The analysis was performed on the C3-A2 derivation in 30-s epochs for which sleep stages had been determined.…”