Sleep Electroencephalogram (EEG) Oscillations and Associated Memory Processing During Childhood and Early Adolescence

The architecture of sleep undergoes distinct changes during childhood and early adolescence. Slow wave sleep is involved in memory processing and may support active consolidation of newly encoded representations to support the formation of abstracted gist memories. Here, we examined sleep and overnight memory formation in German school children (n = 33) between 7 and 15 years of age, after the encoding phase of a verbal Deese-Roediger-McDermott (DRM) task. Effects of age were analyzed on sleep electroencephalogram (EEG) signatures of memory processing during nonrapid eye movement (NonREM) sleep, and the overnight formation of veridical and gist-based memories. Increasing age decreases time spent in slow wave sleep, and slow wave activity, whereas density and amplitude of fast sleep spindles in NonREM sleep were increased. Moreover, fast spindles were more consistently and more closely coupled to the upstate of the slow oscillation in the older children. Also, veridical and gist-based recall of words after sleep increased with age. Notably, a closer slow oscillation upstate-fast spindle coupling predicted veridical recall of words, and this relationship was found independent of age. Memory performance in the sleeping children did not differ from that of an age-matched control group (n = 32) tested over a daytime wake retention interval, with adolescents even showing superior veridical recall after wake. Our findings suggest that slow oscillation-spindle coupling as a mechanism of sleep-dependent memory formation becomes increasingly relevant during childhood and early adolescence. However, wake-associated mechanisms similarly effective in forming medium-term memory exist in this age as well. Public Significance Statement The recall of veridical and gist-based memories increases with age in children between 7 to 15 years of age. Whereas sleep compared with wakefulness did not generally alter memory performance, consolidation of veridical memory was connected to a more precise coupling of spindles to slow oscillations, two cardinal nonrapid eye movement sleep oscillations.

Automated summary

The architecture of sleep undergoes distinct changes during childhood and early adolescence. Slow wave sleep is involved in memory processing and may support the formation of abstracted gist memories. The coupling of slow oscillations and fast sleep spindles becomes increasingly important for memory formation in children and adolescents, while wake-associated mechanisms are also effective in forming medium-term memory in this age group.