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.
Slow oscillations and sleep spindles, the canonical electrophysiological oscillations of non-rapid eye movement sleep, are thought to gate incoming sensory information, underlie processes of sleep-dependent memory consolidation, and are altered in various neuropsychiatric disorders. Accumulating evidence of the predominantly local expression of these individual oscillatory rhythms suggests that their cross-frequency interactions may have a similar local component. However, it is unclear whether locally coordinated sleep oscillations exist across the cortex, and whether and how these dynamics differ between fast and slow spindles, and sleep stages. Moreover, substantial individual variability in the expression of both spindles and slow oscillations raises the possibility that their temporal organization shows similar individual differences. Using two nights of multi-channel electroencephalography recordings from 24 healthy individuals, we characterized the topography of slow oscillation-spindle coupling. We found that while slow oscillations are highly restricted in spatial extent, the phase of the local slow oscillation modulates local spindle activity at virtually every cortical site. However, coupling dynamics varied with spindle class, sleep stage, and cortical region. Moreover, the slow oscillation phase at which spindles were maximally expressed differed markedly across individuals while remaining stable across nights. These findings both add an important spatial aspect to our understanding of the temporal coupling of sleep oscillations and demonstrate the heterogeneity of coupling dynamics, which must be taken into account when formulating mechanistic accounts of sleep-related memory processing.
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