Background

Even modest sleep restriction, especially the loss of sleep slow wave activity (SWA), is invariably associated with slower electroencephalogram (EEG) activity during wake, the occurrence of local sleep in an otherwise awake brain, and impaired performance due to cognitive and memory deficits. Recent studies not only confirm the beneficial role of sleep in memory consolidation, but also point to a specific role for sleep slow waves. Thus, the implementation of methods to enhance sleep slow waves without unwanted arousals or lightening of sleep could have significant practical implications. Slow Wave Enhancement is a possible way to improve the restorative functions of sleep. 

Objective

Review the evidence that it is possible to enhance sleep slow waves in humans using transcranial direct-current stimulation (tDCS) and transcranial magnetic stimulation. Since these methods are currently impractical and their safety is questionable, especially for chronic long-term exposure, we then discuss novel data suggesting that it is possible to enhance slow waves using sensory stimuli. We consider the physiology of the K-complex (KC), a peripheral evoked slow wave, and show that, among different sensory modalities, acoustic stimulation is the most effective in increasing the magnitude of slow waves, likely through the activation of non-lemniscal ascending pathways to the thalamo-cortical system. In addition, we discuss how intensity and frequency of the acoustic stimuli, as well as exact timing and pattern of stimulation, affect sleep enhancement. Finally, we discuss automated algorithms that read the EEG and, in real-time, adjust the stimulation parameters in a closed-loop manner to obtain an increase in sleep slow waves and avoid undesirable arousals.

Methods

The effect of somatosensory and auditory stimulation was assessed by Tononi et al. (2010). While the change observed with somatosensory stimulation was minor, acoustic stimulation was particularly efficacious in enhancing sleep slow waves. Specifically, using an intermittent stimulation in which tones were played in blocks of 15 s spaced out by stimulation-free intervals, slow waves appeared remarkably large and numerous during the stimulation blocks (Figure 1A; Riedner et al., 2012).

Results

By reviewing the relevant literature, we pointed out several features (intensity, sound frequency, timing, and entrainment) of the acoustic stimulation that may play an important role in regulating the efficacy of the stimulation. Specifically, we indicate that stimulation intensity should be tuned according to sleep depth, because there is a threshold below which the stimulation intensity is effective in enhancing slow waves and above which it causes arousal. Changing the sound frequency could counteract the occurrence of habituation and hitting the thalamo-cortical system at convenient times could maximize the enhancing effect.

Conclusions

There is some evidence that acoustic stimulation could be used not only to enhance NREM slow waves, but also some features of REM sleep (Drucker-Colin et al., 1983; Arankowsky-Sandoval et al., 1986, 1992; Vazquez et al., 1998; Amici et al., 2000). The increased REM duration following acoustic stimulation was later confirmed by another group of researchers showing longer REM periods also for stimulations occurring during NREM sleep (Amici et al., 2000). In humans, an increase in both REM sleep duration and sleep efficiency occurs when acoustic stimulation is started at the beginning of REM sleep, whereas a disruptive effect with a larger number of awakenings has been reported when the stimulation starts near the end of a REM episode (Salin-Pascual et al., 1991). Increased REM sleep duration was also correlated with a pronounced decrease in the density of REMs (Mouze-Amady et al., 1986), and to a better retention of memories in a Morse code learning task (Guerrien et al., 1989). Nevertheless, despite several reports indicating that acoustic stimulation lengthens REM sleep, the behavioral impact of this manipulation requires further investigation.