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. 2021 May 5;41(18):4088-4099.
doi: 10.1523/JNEUROSCI.0818-20.2021. Epub 2021 Mar 19.

Sleep Spindles Preferentially Consolidate Weakly Encoded Memories

Dan Denis  1   2   3 , Dimitrios Mylonas  3   4   5 , Craig Poskanzer  2   6 , Verda Bursal  2 , Jessica D Payne  7 , Robert Stickgold  2   3
Affiliations

Sleep Spindles Preferentially Consolidate Weakly Encoded Memories

Dan Denis et al. J Neurosci. .

Abstract

Sleep has been shown to be critical for memory consolidation, with some research suggesting that certain memories are prioritized for consolidation. Initial strength of a memory appears to be an important boundary condition in determining which memories are consolidated during sleep. However, the role of consolidation-mediating oscillations, such as sleep spindles and slow oscillations, in this preferential consolidation has not been explored. Here, 54 human participants (76% female) studied pairs of words to three distinct encoding strengths, with recall being tested immediately following learning and again 6 h later. Thirty-six had a 2 h nap opportunity following learning, while the remaining 18 remained awake throughout. Results showed that, across 6 h awake, weakly encoded memories deteriorated the fastest. In the nap group, however, this effect was attenuated, with forgetting rates equivalent across encoding strengths. Within the nap group, consolidation of weakly encoded items was associated with fast sleep spindle density during non-rapid eye movement sleep. Moreover, sleep spindles that were coupled to slow oscillations predicted the consolidation of weak memories independently of uncoupled sleep spindles. 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 memory consolidation, guided in part by memory strength.SIGNIFICANCE STATEMENT Given 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, and it appears that certain memories are prioritized to receive this benefit. Here, we found that, compared with staying awake, sleep was associated with better memory for weakly encoded information. This suggests that sleep helps attenuate the forgetting of weak memory traces. Fast sleep spindles, a hallmark oscillation of non-rapid eye movement sleep, mediate consolidation processes. We extend this to show that fast spindles were uniquely associated with the consolidation of weakly encoded memories. This provides new evidence for preferential sleep-based consolidation and elucidates a physiological correlate of this benefit.

Keywords: memory; memory consolidation; memory strength; sleep; sleep spindles; slow oscillations.

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Figures

Figure 1.
Figure 1.
Experimental design. A, Timeline of the protocol. All participants arrived at the sleep laboratory at ∼9:00 A.M. and were wired for EEG. During Session 1, participants completed a 5 min rest period followed by the encoding task (B) and a second 5 min rest session. They then performed a cued recall test (immediate recall; C), followed by a final quiet rest session. Following that, 36 participants had a 2 h nap opportunity, followed by a 4 h wake delay spent in the sleep laboratory. The remaining 18 did not have a nap opportunity and stayed awake in the laboratory for 6 h. Session 2 started at ∼6:00 P.M. and began with a fourth quiet rest, followed by a second cued recall test (delayed recall; C), and a fifth quiet rest. B, Encoding. Each encoding trial began with a fixation cross that appeared on the screen for 2000-3000 ms, followed by the word pair for 2000 ms. After the presentation of each word pair, participants were asked if they had been able to successfully visualize a scene containing the two word-pair objects. A total of 180 word pairs were displayed, with 60 being viewed 1 time, 60 being viewed 2 times, and 60 being viewed 4 times, for a total of 420 trials. C, Recall. Both the immediate and delayed test followed the same procedure. First, a fixation cross appeared for 2000-3000 ms. Then, the first word of the pair appeared alone for 2000-2500 ms. During this window, participants were instructed to think as hard as possible about what the correct second word was. Then, a box appeared underneath the first word, indicating that they could start typing in their answer. There was a total of 180 recall trials. D, Purple and orange lines indicate fast and slow spindle components as derived using generalized eigen decomposition from a single participant. Overlaid in gray is the frequency response of the wavelet used for spindle detection, separately tuned for fast and slow spindles based on the participant's peaks. Note the low degree of overlap in the fast and slow wavelet frequency response.
Figure 2.
Figure 2.
Behavior. A, Percentage of word pairs recalled during immediate test. B, Percentage of word pairs recalled during delayed test. C, Relative change in the percentage of word pairs recalled between delayed and immediate test. The change is calculated as %delayed – %immediate test/each individual participant's %immediate test score. Error bars indicate the within-participant standard error.. “n PRES” indicates encoding condition; for instance, 4PRES = recall/change in recall to items that were presented 4 times during encoding. ***p < 0.001. **p < 0.01.
Figure 3.
Figure 3.
Change in 1PRES memory across delay periods. The data for the 12 and 24 h delay groups have been previously published (Denis et al., 2020).
Figure 4.
Figure 4.
Sleep spindles during NREM sleep. A, Fast sleep spindles. Fast spindle density (spindles/min) during NREM sleep shown in column 1. Columns 2-4, Correlations between fast spindle density and change in recall for 1PRES, 2PRES, and 4PRES items, respectively. Cluster statistics presented above topographies. Pink dots represent significant electrodes in cluster. B, Slow sleep spindles. Slow spindle density (spindles/min) during NREM sleep shown in column 2. Columns 2-4, Correlations between slow spindle density and change in recall for 1PRES, 2PRES, and 4PRES items, respectively. C, Topography of t values indicating differences between fast and slow spindle density. Cluster statistics presented above topography. Pink dots represent significant electrodes in cluster.
Figure 5.
Figure 5.
Fast and slow spindles show opposite associations with change in 1PRES memory. Spindle density derived by averaging significant electrodes in cluster (see topographies). p values indicate significance of a robust regression, used to minimize the influence of outliers.
Figure 6.
Figure 6.
Slow oscillation-spindle coupling. A, Topography of coupled fast (first column) and slow (second column) spindle density, and the difference between them (third column). Cluster statistics presented above topography. Pink dots represent significant electrodes in cluster. Far right, the percentage of participants who exhibited a significantly higher rate of coupling than would be expected by chance. B, Coupling phase. Columns 1 and 2, Preferred coupling phase of fast and slow spindles at each electrode. Pink dots represent electrodes exhibiting significant nonuniformity (Rayleigh tests) at p < 0.05 (adjusted for multiple comparisons using the false discovery rate). Column 3, A circular phase plot displaying phase distributions of fast and slow spindles across participants at electrode FCz (ringed electrode in topographies). Each line indicates the preferred coupling phase of individual participants. The direction of the arrow indicates the average phase across participants, with the length of the arrow indicating the coupling strength across participants. A coupling of phase of 0° indicates preferential coupling of spindles at the positive peak of the slow oscillation. A coupling phase of 180° indicates preferential spindle coupling at the negative trough of the slow oscillation. C, Temporal dynamics of slow oscillation-spindle coupling events. Left, Top, The average time-frequency response of all slow oscillations coupled to a fast spindle (−1200 to 1200 ms, centered on the trough of the slow oscillation), with the time-domain averaged slow oscillation overlaid. Bottom, Histogram indicating the distribution of coupled fast spindles, displayed as percentage of coupled fast spindles, averaged across participants, binned into 100 ms intervals. Right, The same information, but for slow spindle coupling. All analyses performed on electrode FCz (ringed electrode in topographies of B).
Figure 7.
Figure 7.
Fast spindle coupling and memory consolidation of 1PRES items. Top row, Univariate correlations between fast coupled spindle density (left plot) and fast uncoupled spindle density (right plot) with 1PRES change in recall. Cluster statistics presented above topographies. Pink dots represent significant electrodes in cluster. Bottom row, Partial robust regression plots. Left plot visualizes the relationship between coupled fast spindle density and 1PRES change in recall, after accounting for uncoupled spindles. Right plot visualizes the relationship between uncoupled fast spindle density and 1PRES change in recall, after accounting for coupled spindles.
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