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.

Memory consolidation during sleep does not benefit all memories equally. Initial encoding strength appears to play a role in governing where sleep effects are seen, but it is unclear whether sleep preferentially consolidates weaker or stronger memories. We manipulated encoding strength along two dimensions-the number of item presentations, and success at visualizing each item, in a sample of 82 participants. Sleep benefited memory of successfully visualized items only. Within these, the sleep-wake difference was largest for more weakly encoded information. These results suggest that the benefit of sleep on memory is seen most clearly for items that are encoded to a lower initial strength.

Sleep plays a critical role in the consolidation of memories. But this process is selective, with only some memories benefiting. One component of this selection process is encoding strength. The role that initial encoding strength plays in the prioritization for consolidation during sleep is currently unclear, with some studies suggesting that weaker memories are prioritized and others arguing that stronger memories are prioritized. One possible reason for this discrepancy is the wide variety of manipulations employed to induce weak vs. strong encoding. Here, we employed a novel within-subject word pairs paradigm in N = 82 individuals to manipulate encoding strength along two different dimensions—by the number of presentations of an item, and by the participants’ visualization of each item. In this protocol, we found that the sleep benefits were only seen for items that had been successfully visualized during encoding. Within these visualized items, after either a 12- or 24-hour delay including a night of sleep, there was significantly less forgetting of those items that had been presented the fewest times during encoding. Together these results highlight the fact that multiple factors present at the moment of encoding influence whether the brain selects a particular memory for further processing during sleep. Prioritization mechanisms may operate in a hierarchy, with successful visualization prioritized over the impact of repeated item exposure.

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.