Abstract
Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, conversely, normal sleep promotes the strengthening of the already encoded memories. However, whether sleep can strengthen deteriorated memories caused by insufficient sleep remains unknown. Here, we showed that sleep restriction in a group of participants caused a reduction in the stability of EEG activity patterns across multiple encoding of the same event during awake, compared with a group of participants that got a full night’s sleep. The decrease of neural stability patterns in the sleep-restricted group was associated with higher slow oscillation-spindle coupling during a subsequent night of normal sleep duration, thereby suggesting the instantiation of restorative neural mechanisms adaptively supporting cognition and memory. Importantly, upon awaking, the two groups of participants showed equivalent retrieval accuracy supported by subtle differences in the reinstatement of encoding-related activity: it was longer lasting in sleep-restricted individuals than in controls. In addition, sustained reinstatement over time was associated with increased coupling between spindles and slow oscillations. Taken together, these results suggest that the strength of prior encoding might be an important moderator of memory consolidation during sleep. Supporting this view, spindles nesting in the slow oscillation increased the probability of correct recognition only for weakly encoded memories. Current results demonstrate the benefit that a full night’s sleep can induce to impaired memory traces caused by an inadequate amount of sleep.
Highlights
Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, normal sleep promotes the strengthening of the already encoded memories
While some of the studies indicate that sleep disruption reduces hippocampal activation during encoding in the awake period, leading to impaired memory retrieval after one night of recovery sleep[1,2]; other studies show that sleep mostly facilitates the consolidation of weaker memories[3,4,5,6,7,8,9,10,11,12], thereby suggesting that memory consolidation during sleep is adaptive and prioritizes memories most vulnerable to forgetting
We focused on fast SPs (13–16 Hz) because they have been more consistently related to memory consolidation than slow SPs (9–12 Hz)[45,46], and have shown strong phase synchronization with the depolarizing up-state of SOs21–24,47,48
Summary
Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, normal sleep promotes the strengthening of the already encoded memories. The decrease of neural stability patterns in the sleep-restricted group was associated with higher slow oscillation-spindle coupling during a subsequent night of normal sleep duration, thereby suggesting the instantiation of restorative neural mechanisms adaptively supporting cognition and memory. We examined whether the interplay of neural oscillations supporting memory consolidation during sleep is associated with participants’ ability to elicit stable EEG activity patterns across encoding repetitions and with their capacity of correctly recognizing learned associations the day To this aim, we analyzed the temporal grouping of fast spindles (SPs; 13–16 Hz) by the depolarized up-state of slow oscillations (SOs; 0.5–4 Hz) during slow-wave sleep (SWS), which has been proposed as a key mechanism of overnight memory consolidation[20,21,22,23,24]. Based on the assumption that sleep preferentially consolidates memories that have been poorly encoded during the previous waking period[3,4,7,8], we hypothesized that the capacity of SO-SP coupling to predict memory recognition would be a function of prior encoding strength
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