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. 2019 Jan;22(1):e12706.
doi: 10.1111/desc.12706. Epub 2018 Sep 5.

Developmental changes of sleep spindles and their impact on sleep-dependent memory consolidation and general cognitive abilities: A longitudinal approach

Michael Hahn  1 , Ann-Kathrin Joechner  1 , Judith Roell  1 , Manuel Schabus  1 , Dominik Pj Heib  1 , Georg Gruber  2   3 , Philippe Peigneux  4 , Kerstin Hoedlmoser  1
Affiliations

Developmental changes of sleep spindles and their impact on sleep-dependent memory consolidation and general cognitive abilities: A longitudinal approach

Michael Hahn et al. Dev Sci. 2019 Jan.

Abstract

Sleep spindles are related to sleep-dependent memory consolidation and general cognitive abilities. However, they undergo drastic maturational changes during adolescence. Here we used a longitudinal approach (across 7 years) to explore whether developmental changes in sleep spindle density can explain individual differences in sleep-dependent memory consolidation and general cognitive abilities. Ambulatory polysomnography was recorded during four nights in 34 healthy subjects (24 female) with two nights (baseline and experimental) at initial recording (age range 8-11 years) and two nights at follow-up recording (age range 14-18 years). For declarative learning, participants encoded word pairs with a subsequent recall before and after sleep. General cognitive abilities were measured by the Wechsler Intelligence Scale. Higher slow (11-13 Hz) than fast (13-15 Hz) spindle density at frontal, central, and parietal sites during initial recordings, followed by a shift to higher fast than slow spindle density at central and parietal sites during follow-up recordings, suggest that mature spindle topography develops throughout adolescence. Fast spindle density increases from baseline to experimental night were positively related to sleep-dependent memory consolidation. In addition, we found that the development of fast spindles predicted the improvement in memory consolidation across the two longitudinal measurements, a finding that underlines a crucial role for mature fast spindles for sleep-dependent memory consolidation. Furthermore, slow spindle changes across adolescence were related to general cognitive abilities, a relationship that could indicate the maturation of frontal networks relevant for efficient cognitive processing. A video abstract of this article can be viewed at: https://www.youtube.com/watch?v=7NXJzm8HbIw and https://www.youtube.com/watch?v=iuMQY1OIJ0s.

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Figures

Figure 1
Figure 1
Study design. Ambulatory PSG recordings were conducted at the participants’ homes. During both nights, participants stayed in bed for 10 hours at initial and 8 hours at follow‐up recordings. At the experimental night, word pair encoding was performed in the evening with subsequent recall one hour before sleep and a delayed recall one hour after sleep. This resulted in a 12 hour retention interval at initial and a 10 hour retention interval at follow‐up recordings. The counterbalanced wake condition was only conducted for follow‐up recordings with encoding and immediate recall in the morning followed by 10 hours of wakefulness prior to the delayed recall in the evening
Figure 2
Figure 2
(a) Means and standard error of correctly recalled word pairs compared between initial and follow‐up recordings before and after a sleep retention interval. Memory performance was higher at follow‐up recordings. At initial recordings, word pair memory decreased after the sleep interval (p = 0.015) but remained stable at follow‐up recordings. (b) Comparison of word pair memory between a sleep and a wake retention interval at follow‐up recordings. Memory did not change after the sleep retention interval but decreased after the wake retention interval (p <0.001)
Figure 3
Figure 3
Topographical plots for mean spindle density at each electrode separated by slow (left column) and fast spindle density (right column) at initial (upper row) and follow‐up recordings (lower row) during experimental nights. Bright colours indicate higher spindle density. Slow spindles were dominant during initial recordings. At follow‐up, slow spindles only remained dominant at frontal derivations, whereas fast spindles became dominant at centro‐parietal derivations. Note that due to the extrapolation of topographical plots, colours that go beyond the measured electrodes do not contain any information
Figure 4
Figure 4
Means and standard error of slow (dark colours) and fast spindle density (bright colours) for memory decliners (dashed line) and maintainers at initial recording (left column, blue) and follow‐up recording (right column, red) at frontal (upper row) and central electrode sites (lower row) during baseline and experimental night. Memory decliner increased slow spindle density from baseline to experimental night at both electrode sites at initial recordings (frontal: p = 0.020; central: p = 0.002). At follow‐up recordings, memory maintainer increased fast spindle density from baseline to experimental night (p = 0.022), whereas memory decliner increased slow spindle density at central electrode sites (p = 0.042). Note: Group composition of memory decliner and memory maintainer is different between initial and follow‐up recordings
Figure 5
Figure 5
Spearman correlations between the development of overnight memory change enhancement and central fast spindle density development. Higher increase in central fast spindle density in the experimental night from initial to follow‐up was related to enhanced overnight memory change relative to initial recordings. Participants who enhance overnight memory change from initial to follow‐up are indicated by triangles, those who decline by circles
Figure 6
Figure 6
Spearman correlations between the mean IQ score at follow‐up recordings and slow spindle density development on frontal sites with linear trend line. An increase in frontal slow spindle density was linked to higher cognitive abilities (IQ)
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