Sleep spindles preferentially consolidate weakly encoded memories

Abstract

Sleep has been shown to be critical for memory consolidation, and recent research has demonstrated that this consolidation effect is selective, with certain memories being prioritized for strengthening. Initial strength of a memory appears to be one metric the brain uses to prioritize memory traces for sleep-based consolidation, but the role of consolidation-mediating cortical oscillations, such as sleep spindles and slow oscillations, has not been explored. Here, N=54 participants studied pairs of words to three distinct encoding strengths, with recall being tested immediately following learning and again six hours later.N=36 had a two-hour afternoon nap opportunity following learning, whilst the remaining (n=18) remained awake throughout. Results showed a selective benefit of sleep on memory, with sleep preferentially consolidating weakly encoded items (p=.003). The magnitude of this effect (d=0.90, 95%CI=0.29-1.50) was similar when compared to a previous study examining the benefits of a full night of sleep (d=1.36, 95% CI=0.59-2.12). Within the nap group, consolidation of weakly encoded items was associated with sleep spindle density during slow wave sleep (r=.48, p=.003). This association was present when separately examining spindles coupled (r=.41, p=.013), and uncoupled (r=.44, p=.007) with slow oscillations. Memory was significantly better in individuals who showed an amount of slow oscillation-spindle coupling that was greater than what would be expected by chance (p=.006, d=1.15).These relationships were unique to weakly encoded items, with spindles not correlating with memory for intermediate or strong items. This suggests that sleep spindles facilitate selective memory consolidation, guided in part by memory strength. Significance statementGiven the countless pieces of information we encode each day, how does the brain select which memories to commit to long-term storage? Sleep is known to aid in memory consolidation, but less research has examined which memories are prioritized to receive this benefit. Here, we found that compared to staying awake, sleep was associated with better memory for weakly encoded information. This suggests sleep helps to rescue weak memory traces from being forgotten. Sleep spindles, a hallmark oscillation of nonrapid eye movement sleep, mediates consolidation processes. We extended this to show that spindles selectively facilitated consolidation of weakly encoded memories. This provides new evidence for the selective nature of sleep-based consolidation and elucidates a physiological correlate of this preferential benefit.

Using EEG Microstates to Examine Post-Encoding Quiet Rest and Subsequent Word-Pair Memory

“…Our results from the DSOE data suggest that increased microstate D GEV, and the magnitude of the GEV increase, are associated with better memory for 1 PRES encoded words. These findings are in line with the plethora of research in the sleep and memory literature that indicate the prioritization of weakly encoded memories during sleep-based consolidation [Drosopoulos et al, 2007;Schapiro et al, 2017;Djonlagic et al, 2009;Denis et al, 2019;Denis et al, 2020].…”

“…Sleep-based memory consolidation is selective, meaning only certain information is designated for further processing. Recent research has suggested that one contributing factor to the modulation of memory consolidation across sleep is the initial encoding strength of the memory [sleep benefits weakly encoded memories: Drosopoulos et al, 2007;Schapiro et al, 2017;Djonlagic et al, 2009;Denis et al, 2019;Denis et al, 2020;sleep benefits strongly encoded memories: Tucker and Fishbein, 2008;Schoch et al, 2017;and Wislowska et al, 2017]. In this vein, there are differing factions of evidence-some suggesting sleep benefits weakly encoded memories and others suggesting a benefit for stronger encodings.…”

The roles of item exposure and visualization success in the consolidation of memories across wake and sleep

“…This suggests that during sleep weaker memories receive a consolidation benefit when compared to wake where those same memories deteriorate the most. While the neurophysiological mechanism underlying this effect is unclear, recent research has shown that the consolidation of weak memories is uniquely associated with sleep spindles (Denis et al 2020;Baena et al 2020), 12-15Hz waxing and waning oscillations that are characteristic of non-rapid eye movement sleep. This builds on other evidence showing that sleep spindles facilitate memory consolidation (Schabus et al 2004;Cox et al 2012), Furthermore, memory replay in the hippocampus during quiet rest is preferential for weakly encoded memories (Schapiro et al 2018).…”

Slow oscillation-spindle coupling is negatively associated with emotional memory formation following stress

“…We found that stress alters the association between SWS and memory. It is notable that no associations between SWS activity and memory were found in the control group, given other research showing SWS-related benefits for both neutral and emotional episodic memory in nonstressed participants (Ackermann & Rasch, 2014;Cox et al, 2012;Denis et al, 2020;Groch et al, 2013;Mikutta et al, 2019;Niknazar et al, 2015;Payne, Chambers, et al, 2012;Payne et al, 2015;Plihal & Born, 1997). While the reason for this finding is unclear, one possible explanation may be the delay interval used in this study design.…”

“…In humans, this coordination has been demonstrated in epilepsy patients with intracranial hippocampal recordings (Staresina et al, 2015). Although hippocampal ripples cannot be detected non-invasively, slow oscillation-spindle coupling as detected via scalp EEG has been associated with memory consolidation in healthy humans (Denis et al, 2020;Mikutta et al, 2019;Niknazar et al, 2015;Zhang et al, 2020).…”