It is widely agreed that rhythmic neuronal activity during sleep supports declarative memory consolidation (Diekelmann & Born, 2010;Watson & Buzsáki, 2015). Compelling evidence suggests that the underlying key mechanism is the reactivation of initially labile, learning-related neuronal activity in the hippocampus and its integration into cortical networks (Peyrache et al., 2009;Wilson & McNaughton, 1994). This system consolidation results in more durable and integrated mnemonic representations (Diekelmann & Born, 2010). However, given profound developmental changes in rhythmic neuronal activity,
In young adults, memory consolidation during sleep is supported by a time-coordinated interplay of sleep spindles and slow oscillations. However, given tremendous developmental changes in sleep spindle and slow oscillation morphology, it remains elusive whether the same mechanisms as identified in young adults are comparably functional across childhood. Here, we characterise slow and fast sleep spindles and their temporal coupling to slow oscillations in 24 pre-school children. Further, we ask whether slow and fast sleep spindles and their modulation during slow oscillations are similarly associated with behavioural indicators of declarative memory consolidation as suggested from adult literature. Employing a development-sensitive, individualised approach, we reliably identify an inherent, development-specific fast sleep spindle type, though nested in the adult-like slow sleep spindle frequency range, along with a dominant slow sleep spindle type. Further, we provide evidence for the modulation of fast sleep spindles during slow oscillations, already in pre-school children. However, the temporal coordination between fast sleep spindles and slow oscillations is weaker and less precise than expected from adult research. While we do not find evidence for a critical contribution of the pattern of fast sleep spindle modulation during slow oscillations for memory consolidation, crucially, both inherent slow and fast sleep spindles separately are differentially related to sleep-associated consolidation of items of varying quality. While a higher number of slow sleep spindles is associated with stronger maintenance of medium-quality memories, more fast sleep spindles are linked to higher gain of low-quality items. Our results provide evidence for two functionally relevant inherent sleep spindle types in pre-school children despite not fully matured sleep spindle - slow oscillation coupling.
Adaptive memories are formed in the face of a fundamental tension: extracting commonalities across experiences to generate novel inferences (i.e., generalization), while simultaneously forming separate representations of similar events (i.e., memory specificity). Theoretical memory models suggest that specific experiences are initially encoded as hippocampus-dependent episodic memories and slowly become amenable to generalization through consolidation. Post-learning sleep facilitates such consolidation processes. However, generalization can also occur rapidly during wakefulness. Contemporary models propose that rapid generalization relies on the retrieval of specific episodes. In a sample of 141 four- to eight-year-old children, we investigated whether (i) age differentially relates to generalization and memory specificity, (ii) generalization is contingent on different aspects of past experiences, and (iii) the effect of a sleep-filled delay on generalization and memory specificity differs across age. We found age-related differences in generalization and memory specificity, with improvements with age being more pronounced in generalization than in memory specificity. Unlike prior evidence in adults, children’s generalization success was contingent on retrieving specific object conceptual properties and on inter-object semantic proximity, but not on perceptual attributes or surrounding contexts. Further, older children were more likely to retain general and specific aspects of memory after an overnight delay. However, age-related gains differed across memory functions: Compared to younger children, older children showed greater gains in generalized, but not in specific memories. These findings reveal those aspects of past experiences upon which children draw when creating inferences, and suggest that the effects of sleep on generalization and memory specificity interact with age.
The synchronization of canonical fast sleep spindle activity (12.5-16 Hz) precisely during the slow oscillation up peak is considered an essential feature of adult non-rapid eye movement sleep. However, there is little knowledge on how this well-known coalescence between slow oscillations and sleep spindles develops. Leveraging individualized detection of single events, we first provide a detailed cross-sectional characterization of age-specific patterns of slow and fast sleep spindles, slow oscillations, and their coupling in children aged 5 to 6, 8 to 11, and 14 to 18 years. Critically, based on this, we then investigated how spindle and slow oscillation maturity substantiate age differences in their precise orchestration. While the predominant type of fast spindles was development-specific in that it was still nested in a frequency range below the canonical fast spindle range for the majority of children, the well-known slow oscillation-spindle coupling pattern was evident for sleep spindles in the canonical (adult-like) fast spindle range in all three age groups - but notably less precise in children. To corroborate these findings, we linked personalized measures of fast spindle maturity, which indicate the similarity between the prevailing development-specific and adult-like fast spindles, and slow oscillation maturity, which reflects the extent to which slow oscillations show frontal dominance, with individual slow oscillation-spindle coupling patterns. Importantly, we found that fast spindle maturity was uniquely associated with enhanced slow oscillation-spindle coupling strength and precision. Taken together, our results suggest that the increasing ability to generate canonical fast sleep spindles actuates precise slow oscillation-spindle coupling patterns across child and adolescent development.
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