Even though it is known that sleep benefits declarative memory consolidation, the role of sleep in the storage of temporal sequences has rarely been examined. Thus we explored the influence of sleep on temporal order in an episodic memory task followed by sleep or sleep deprivation. Thirty-four healthy subjects (17 men) aged between 19 and 28 years participated in the randomized, counterbalanced, between-subject design. Parameters of interests were NREM/REM cycles, spindle activity and spindle-related EEG power spectra. Participants of both groups (sleep group/sleep deprivation group) performed retrieval in the evening, morning and three days after the learning night. Results revealed that performance in temporal order memory significantly deteriorated over three days only in sleep deprived participants. Furthermore our data showed a positive relationship between the ratios of the (i) first NREM/REM cycle with more REM being associated with delayed temporal order recall. Most interestingly, data additionally indicated that (ii) memory enhancers in the sleep group show more fast spindle related alpha power at frontal electrode sites possibly indicating access to a yet to be consolidated memory trace. We suggest that distinct sleep mechanisms subserve different aspects of episodic memory and are jointly involved in sleep-dependent memory consolidation.
The different functions of sleep have not yet been completely understood although some kind of involvement in memory consolidation seems to be widely accepted (for review see Diekelmann and Born, 2010). More specifically, sleep has been proven to enhance hippocampus dependent temporal sequence memory in rats (Fortin et al., 2002). In humans there is to date only one study which demonstrates that sleep in comparison to wakefulness strengthens the original temporal sequence structure of a memory trace (Drosopoulos et al., 2007). In that study subjects were asked to learn triplets of words presented one after the other. Later, recall was tested by presenting word by word and asking which one came after the other. Sleep was found to enhance word recall, but only when students were asked to reproduce the learned words in the original forward direction (cueing with A and B and asking for B and C, respectively). Still debated, however, are the exact mechanisms which underlie the transformation of newly learned information into more stable forms during sleep.
Different sleep stages are assumed to be crucial for different types of memory. One of the main hypotheses, the “dual process theory”, assumes that a specific sleep stage is characteristic for a specific memory type. Slow wave sleep (SWS) supports declarative memory consolidation whereas rapid eye movement (REM) sleep does so for procedural memories (Gais and Born, 2004, Maquet, 2001, Plihal and Born, 1997 and Plihal and Born, 1999). The “sequential hypothesis” on the other hand, proposes that the alternation of sleep stages in cycles supports effective memory re-processing (Ficca and Salzarulo, 2004 and Giuditta et al., 1995). This idea of complementary functions of SWS and REM sleep for successful memory consolidation was revived by Diekelmann and Born (2010) who suggested an essential role of SWS for system consolidation which is complemented by synaptic consolidation taking place during REM sleep. However, data directly supporting this latter hypothesis is still incomplete.
Neuronal replay during both SWS (Nadasdy et al., 1999 and Wilson and McNaughton, 1994) and REM sleep (Poe et al., 2000), as usually observed in animal studies, seems to underlie the beneficial effect of sleep over wakefulness with regard to memory consolidation. Specifically, hippocampal replay during the night but also during quiet restfulness following spatial learning is a well-documented phenomenon (Frank et al., 2011 and Zugaro and Girardeau, 2011).
Concerning memory relevant sleep features during the night, most empirical evidence is present for individual slow waves (Mölle et al., 2002), sharp wave ripples (Buzsaki, 1984 and Mölle et al., 2009) and sleep spindles (Clemens et al., 2005, Fogel and Smith, 2006 and Schabus et al., 2004). Here, the fast spindle type (>13 Hz) appears to be more relevant for sleep-dependent memory consolidation, specifically for motor memory formation (Morin et al., 2008 and Tamaki et al., 2009). Additionally sleep spindles have been found to be significantly related to general cognitive abilities or “intelligence” (Bodizs et al., 2005, Fogel et al., 2007 and Schabus et al., 2006).
In contrast to the idea of memory consolidation in sleep, EEG specific alpha oscillations seem to play an important role for successful memory reactivation during waking (Klimesch et al., 2006). In light of this data and the finding that sleep spindles are temporally linked to hippocampal reactivation (Siapas and Wilson, 1998) the question arises if alpha might not also play a crucial role during nightly “replay” or spindle occurrence.
In summary, given the well investigated role of sleep in memory consolidation surprisingly little is known about sleep effects on temporal order in episodic memories. In this study we therefore focused on the effect of sleep on (emotional) episodic stories using a sleep group and a sleep deprivation group. As it is well known that SWS enhances declarative memory consolidation and REM sleep is specifically beneficial for emotional content, an overall advantage in memory performance was expected for the sleep group. In the analyses we further focused on fine-grained investigation of non-REM (NREM)/REM cycles, and sleep spindle related oscillatory EEG changes. As will be shown, no one single sleep stage or mechanism appears to support sleep-dependent temporal order consolidation in our task, but rather the orderly interplay of NREM/REM cycles and spindle-related α-oscillations.
