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.

Keywords: consolidation; generalization; learning; memory; sleep; sleep spindles.

Figure 1

Experimental design. In the learning session on the first day, infants heard unknown pseudowords as names for exemplars of unknown similarity‐based object categories. In the memory test on the following day, generalization was tested by presenting novel category exemplars in both correct and incorrect pairings, that is, in same category–word pairings as in the learning session or in different pairings. In the nonlearning control session about a week later, infants heard known words as names for exemplars of known categories. Subsequent to the learning and control sessions infants napped. (For a detailed description, see Section 1)

Figure 2

Sleep spindle activity and its increase after learning. (a) EEG power spectra during NonREM sleep (at CZ) and (above) sleep spindles averaged across frontal (F3, FZ, and F4) and across central–parietal (C3, CZ, C4, P3, PZ, and P4) brain regions for the nap after the learning session and the control nap after the nonlearning session (mean ± SEM). (b) Spindle numbers (left panels) and spindle density (right panels) in nonlearning control nap and postlearning nap for spindles over frontal (upper panels) and central–parietal (lower panels) cortex. Learning‐induced increases in spindle number and density were significant only for central–parietal spindles but not for frontal spindles. (c) Correlation between the learning‐induced increase in time spent in stage 2 NonREM sleep and the learning‐induced increase in spindle number (left: r = 0.836, p < 0.0001) and spindle density (right: r = 0.054, p = 0.777). Learning‐induced increases are determined by the individual infant's difference in respective parameters between the postlearning nap and the nonlearning control nap

Figure 3

ERPs of the memory test on the day after encoding. (a) The ERP responses to the same words in correct pairings and incorrect pairings averaged across all infants. Negativity is plotted upward. (b) Early N200–500 memory effect (over the left fronto‐temporal region) and late N400 memory effect (at PZ) in the infants with strong spindle increase during the postencoding nap

Figure 4

Comparison between the generalization effects of the spindle subgroups. Mean ERP responses with error bars (±2 SEM) in the subgroup with substantial learning‐related increase in spindle density (above the median of the whole group) and in the subgroup without substantial spindle density increase (below the median), (a) during encoding and (b) during the memory test. Upper panels: early N200–500 effect, lower panels: late N400 effect. *p < 0.05, **p < 0.01

Figure 5

The relations between spindle density increase and generalization. (a) Relation between the increase in central–parietal spindle density and the N400 effect of immediate generalization during the second half of the learning phase (r = 0.444, p = 0.023). Due to the negative potential shift of the N400, the positive sign of the correlation coefficient reflects a negative dependency. (b) Positive relation between the increase in central–parietal spindle density and the negative N400 generalization effect in the memory test (r = −0.568, p = 0.001). (c) Positive relation between the increase in central–parietal spindle density and the increase in the N400 generalization effect from learning to memory test (r = −0.707, p = 0.00005)

Figure 6

Comparison between the N400 generalization effect of the comprehension subgroups. Mean late N400 effect with error bars (±2 SEM) in the subgroup with lower word comprehension and in the subgroup with higher word comprehension, (a) during encoding and (b) during the memory test. *p < 0.05