Sleep stage II contributes to the consolidation of declarative memories

Abstract

Various studies suggest that non-rapid eye movement (NREM) sleep, especially slow-wave sleep (SWS), is vital to the consolidation of declarative memories. However, sleep stage 2 (S2), which is the other NREM sleep stage besides SWS, has gained only little attention. The current study investigated whether S2 during an afternoon nap contributes to the consolidation of declarative memories. Participants learned associations between faces and cities prior to a brief nap. A cued recall test was administered before and following the nap. Spindle, delta and slow oscillation activity was recorded during S2 in the nap following learning and in a control nap. Increases in spindle activity, delta activity, and slow oscillation activity in S2 in the nap following learning compared to the control nap were associated with enhanced retention of face-city associations. Furthermore, spindles tended to occur more frequently during up-states than down-states within slow oscillations during S2 following learning versus S2 of the control nap. These findings suggest that spindles, delta waves, and slow oscillations might promote memory consolidation not only during SWS, as shown earlier, but also during S2.

Introduction

Research of the last decade has produced a large corpus of evidence indicating that sleep plays a key function in the consolidation of newly acquired memories. Consolidation refers to the process by which newly acquired and therefore labile memories are strengthened, stabilized and integrated into long-term memory (Squire, Cohen, & Nadel, 1984). Consolidation in different memory systems is not equally influenced by the various sleep stages (e.g., Plihal & Born, 1997). Central to the present study is the finding that declarative memories – i.e., memories for facts and events that one can consciously recollect (Squire, 1987) – profit from the deep sleep stage slow-wave sleep (SWS). Plihal and Born, 1997, Plihal and Born, 1999 showed that new declarative memories are better remembered if recall follows a period of sleep that is rich in SWS compared to a period of sleep rich in rapid eye-movement (REM) sleep. While there is growing evidence for the relevance of SWS in declarative memory consolidation (for reviews see Diekelmann and Born, 2010, Marshall and Born, 2007), little is known about the specific role of sleep stage 2 (S2), which is the other sleep stage besides SWS that constitutes human non-rapid eye-movement (NREM) sleep. Our study aims at investigating whether and how S2 is involved in declarative memory consolidation. We asked whether sleep spindle activity, delta wave activity, and slow oscillation activity as measured during S2 in daytime naps, are related to the consolidation of newly acquired declarative memories. Spindles are transient electroencephalographic oscillations of at least 0.5 s duration with a frequency between 11–15 Hz. They are a defining feature of S2 but do occur during SWS as well. Slow oscillations and delta waves are large amplitude electroencephalographic waves of 0.5–1 Hz and 1–4 Hz, respectively. They are defining features of SWS but are also present during S2.

Here, we focus on spindles and slow oscillations because they are thought to contribute to memory consolidation by coordinating the reactivation of memories during sleep and by enhancing the effect of memory reactivation on the neuronal substrate (Diekelmann and Born, 2010, Marshall and Born, 2007). Standard models of memory consolidation (Diekelmann and Born, 2010, Marshall and Born, 2007) posit that new declarative memories (Rasch et al., 2007, Rudoy et al., 2009) are reactivated during sleep. The reactivation of memories presumably leads to long lasting plastic synaptic changes within the neuronal networks that represent these memories. The consolidating effect of sleep is believed to be accomplished by these synaptic changes. The beneficial effect of spindles and slow oscillations is assumed to be strongest if spindles occur during the neuronally active up-states of slow oscillations.

We also focus on the activity in the delta frequency range (1–4 Hz) because delta waves might contribute to memory consolidation in similar ways as slow oscillations. Although delta waves differ from slow oscillations with regard to how they are generated (thalamo–cortical versus cortical–cortical interactions; see Steriade, Nunez, & Amzica, 1993a), delta waves may still be functionally similar to slow oscillations (e.g., Sirota et al., 2003, Steriade, 2006). Some authors suggested that delta waves might be faster and less potent exemplars of slow oscillations (Buzsáki, 2006, Marshall and Born, 2007).

Growing evidence suggests that high spindle activity (Clemens et al., 2005, Clemens et al., 2006) and high slow oscillation activity (Marshall, Helgadóttir, Mölle, & Born, 2006) and delta activity (Marshall, Mölle, Hallschmid, & Born, 2004) recorded during NREM sleep or SWS contribute to declarative memory consolidation. In addition, learning prior to sleep has been shown to redistribute spindles to the neuronally active up-states within slow oscillations during NREM sleep (Mölle, Eschenko, Gais, Sara, & Born, 2009). Whether spindles, slow oscillations and delta waves occurring during S2 would also contribute to declarative memory consolidation has rarely been investigated. Some studies suggest that spindles (Gais et al., 2002, Genzel et al., 2009, Meier-Koll et al., 1999, Schabus et al., 2004, van der Helm et al., 2011) and delta waves (Wamsley, Tucker, Payne, & Stickgold, 2010) during S2 might be relevant to the consolidation of declarative memories. However, most investigations on the memory functions of S2 point to a role of S2 in the consolidation of procedural motor memories – i.e., nondeclarative memories (Backhaus and Junghanns, 2006, Genzel et al., 2009, Smith and Macneill, 1994). Performing new procedural motor tasks before going to sleep increases not only the amount of time spent in S2 (Fogel and Smith, 2006, Fogel et al., 2007) but also the spindle density in S2 (Fogel and Smith, 2006, Fogel et al., 2007, Peters et al., 2008). Both, the increased amount of S2 (Nishida and Walker, 2007, Walker et al., 2002) and the increased spindle density (Fogel and Smith, 2006, Nishida and Walker, 2007, Peters et al., 2007) were correlated with the gain in the performance of the motor task from pre- to post-sleep.

Here, we investigated whether and how S2 during a brief afternoon nap contributes to the consolidation of declarative memories. We administered an associative learning task prior to an afternoon nap and measured retrieval performance with a cued recall task given both before and following the nap. We computed performance changes in the cued recall task from pre- to post-sleep and correlated these changes with the occurrence of sleep spindles, delta waves and slow oscillations during S2. We also correlated the performance change across sleep with the difference in participants’ spindle, delta and slow oscillation activity between their experimental nap (that followed the declarative memory task) and their control nap (that did not follow a declarative memory task). We expected an association between memory retention and a heightened spindle, delta and slow oscillation activity in S2 during the experimental but not the control nap.