Abstract
Precise temporal coordination of slow oscillations (SO) and sleep spindles is a fundamental mechanism of sleep-dependent memory consolidation. SO and spindle morphology changes considerably throughout development. Critically, it remains unknown how the precise temporal coordination of these two sleep oscillations develops during brain maturation and whether their synchronization indexes the development of memory networks. Here, we use a longitudinal study design spanning from childhood to adolescence, where participants underwent polysomnography and performed a declarative word-pair learning task. Performance on the memory task was better during adolescence. After disentangling oscillatory components from 1/f activity, we found frequency shifts within SO and spindle frequency bands. Consequently, we devised an individualized cross-frequency coupling approach, which demonstrates that SO-spindle coupling strength increases during maturation. Critically, this increase indicated enhanced memory formation from childhood to adolescence. Our results provide evidence that improved coordination between SOs and spindles indexes the development of sleep-dependent memory networks.
Highlights
We assessed the relationship of sleep-dependent memory consolidation between childhood and adolescence and found no correlation between the two maturational stages (Figure 1—figure supplement 1A; for a direct comparison of sleepdependent memory consolidation see Figure 1—figure supplement 1B)
In a longitudinal sleep and memory study, we show that slow oscillations (SO) and spindles become more precisely coupled during brain maturation from childhood to adolescence
Our findings suggest that the emergence of precise temporal SO-spindle coordination might index the development of hippocampal-neocortical memory systems
Summary
Active system memory consolidation theory proposes that sleep-dependent memory consolidation is orchestrated by three cardinal sleep oscillations (Diekelmann and Born, 2010; Helfrich et al, 2019; Klinzing et al, 2019; Molle et al, 2011; Piantoni et al, 2013; Rasch and Born, 2013; Staresina et al, 2015): (1) Hippocampal sharp-wave ripples represent the neuronal substrate of memory reactivation (Vaz et al, 2019; Wilson and McNaughton, 1994; Zhang et al, 2018), (2) thalamo-cortical sleep spindles are thought to promote long-term potentiation (Antony et al, 2018; De Gennaro and Ferrara, 2003; Rosanova and Ulrich, 2005; Schonauer, 2018; Schonauer and Pohlchen, 2018), while (3) neocortical SOs provide temporal reference frames where memory can be replayed, potentiated and eventually transferred from the short-term storage in the hippocampus to the long-term storage in the neocortex, rendering memories increasingly more stable (Chauvette et al, 2012; Diekelmann and Born, 2010; Frankland and Bontempi, 2005; Rasch and Born, 2013).
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