The reciprocal relation between sleep and memory in infancy: Memory‐dependent adjustment of sleep spindles and spindle‐dependent improvement of memories

Abstract

Sleep spindle activity in infants supports their formation of generalized memories during sleep, indicating that specific sleep processes affect the consolidation of memories early in life. Characteristics of sleep spindles depend on the infant's developmental state and are known to be associated with trait-like factors such as intelligence. It is, however, largely unknown which state-like factors affect sleep spindles in infancy. By varying infants' wake experience in a within-subject design, here we provide evidence for a learning- and memory-dependent modulation of infant spindle activity. In a lexical-semantic learning session before a nap, 14- to 16-month-old infants were exposed to unknown words as labels for exemplars of unknown object categories. In a memory test on the next day, generalization to novel category exemplars was tested. In a nonlearning control session preceding a nap on another day, the same infants heard known words as labels for exemplars of already known categories. Central-parietal fast sleep spindles increased after the encoding of unknown object-word pairings compared to known pairings, evidencing that an infant's spindle activity varies depending on its prior knowledge for newly encoded information. Correlations suggest that enhanced spindle activity was particularly triggered, when similar unknown pairings were not generalized immediately during encoding. The spindle increase triggered by previously not generalized object-word pairings, moreover, boosted the formation of generalized memories for these pairings. Overall, the results provide first evidence for a fine-tuned regulation of infant sleep quality according to current consolidation requirements, which improves the infant long-term memory for new experiences.

Atypicalities in sleep and semantic consolidation in autism

“…These findings resonate with a recent infant study, in which state‐dependent changes in spindle density predicted generalization of novel object labels 1 day after learning (Friedrich, Mölle, Friederici, & Born, ). Furthermore, a developmental MEG study in children aged 8–12 years found that activity in inferior frontal gyri and medial prefrontal cortex was associated with recall of novel object associations (i.e., semantic learning) following sleep but not wake; whereas the wake group showed significantly greater hippocampal activation (Urbain et al, ).…”

Sleep-dependent memory consolidation in infants protects new episodic memories from existing semantic memories

“…Finally, the correlation of spindle activity over central-parietal brain regions with the N400 effect for words paired with new objects, which had been observed in recent infant studies [28][29][30] , failed to meet statistical significance after correcting for multiple testing (highest correlation with spindle RMS at P4: r = −0.437, P = 0.016, adjusted α = 0.008; overall correlation with mean spindle RMS amplitude over the left and right central and parietal regions: r = −0.174, P = 0.358). This weak relation suggests that infants did not build substantial new semantic memories during their nap.…”

“…NonREM sleep with a substantial amount of central-parietal fast sleep spindles in the 13-15 Hz frequency range supports semantic generalization of memories even in infants [28][29][30] . The amount of central-parietal fast spindle activity, in turn, is affected by an infant's processing of novel experience immediately before a nap.…”

“…The less generalized knowledge is available for novel experience-either in semantic long-term memory or transiently formed during encoding-the higher the central-parietal spindle activity in a subsequent nap. In turn, the higher the spindle activity during the nap, the stronger the semantic generalization of the novel experience in the memory test on a next day 30 .…”

Remembering in the Context of Internal States: The Role of Sleep for Infant Memory

“…Encoding, subsequent sleep, and consolidation are intertwined tightly. In a study of 14‐ to 16‐month‐olds (Friedrich, Mölle, Friederici, & Born, ), hearing unknown labels for exemplars of unknown categories produced more sleep spindle activity during a subsequent nap than hearing known labels for exemplars of known categories. In turn, sleep spindle activity was related to memory performance assessed 24 hr later.…”