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. 2024 Jul 11;47(7):zsae072.
doi: 10.1093/sleep/zsae072.

Spindle-slow wave coupling and problem-solving skills: impact of age

Daniel Baena  1   2 , Balmeet Toor  1 , Nicholas H van den Berg  1 , Laura B Ray  1 , Stuart M Fogel  1   2   3
Affiliations

Spindle-slow wave coupling and problem-solving skills: impact of age

Daniel Baena et al. Sleep. .

Abstract

We examined how aging affects the role of sleep in the consolidation of newly learned cognitive strategies. Forty healthy young adults (20-35 years) and 30 healthy older adults (60-85 years) were included. Participants were trained on the Tower of Hanoi (ToH) task, then, half of each age group were assigned to either the 90-minute nap condition, or stayed awake, before retesting. The temporal co-occurrence between slow waves (SW) and sleep spindles (SP) during non-rapid eye movement sleep was examined as a function of age in relation to memory consolidation of problem-solving skills. We found that despite intact learning, older adults derived a reduced benefit of sleep for problem-solving skills relative to younger adults. As expected, the percentage of coupled spindles was lower in older compared to younger individuals from control to testing sessions. Furthermore, coupled spindles in young adults were more strongly coupled to the SW upstate compared to older individuals. Coupled spindles in older individuals were lower in amplitude (mean area under the curve; μV) compared to the young group. Lastly, there was a significant relationship between offline gains in accuracy on the ToH and percent change of spindles coupled to the upstate of the slow wave in older, but not younger adults. Multiple regression revealed that age accounted for differences in offline gains in accuracy, as did spindle coupling during the upstate. These results suggest that with aging, spindle-slow wave coupling decreases. However, the degree of the preservation of coupling with age correlates with the extent of problem-solving skill consolidation during sleep.

Keywords: EEG; aging; coupling; procedural memory; sleep; slow waves; spindles.

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Figures

Graphical Abstract
Graphical Abstract
Figure 1.
Figure 1.
Study design. Overview of experimental protocol. Acclimatization and screening: all participants underwent an initial acclimatization and screening polysomnographic (PSG) recording. Following this, each group (young nap (YN), young wake (YW), older nap (ON), older wake (OW)) underwent both a testing and a control day. Testing Day: Participants arrived at the lab at 09:00 am. Beginning at 10:00 am, participants completed the Tower of Hanoi (ToH) task. Those in the Nap condition then slept in the laboratory from 1:00 pm to 2:30 pm. Those in the Wake condition remained awake. Following this, all participants were retested on the ToH task at 5:00 pm. In addition, participants completed the Stanford Sleepiness Scale (SSS) and Psychomotor Vigilance Test (PVT) before and after each session. Control Day: The same procedure was used, except there was no learning possible with the CTRL version of the ToH task.
Figure 2.
Figure 2.
ToH performance. Mean percent improvement for speed and accuracy on the ToH from Training to Retest in young and older participants. Young adults benefited from a daytime nap as compared to wake, whereas older adults did not. Error bars represent the standard error of the mean. Figure adapted from Toor, B.A., et al., (2022), Neurobiology of Aging, 116, p. 60.
Figure 3.
Figure 3.
Percentage of coupled spindles for older and young participants during control and testing sessions. Each bar represents the number of coupled spindles divided by the total number of spindles. Coupling percentage was lower in older compared to young individuals both at control and testing sessions.
Figure 4.
Figure 4.
Percentage of coupled spindles during the upstate for older and young participants correlated to offline gains in performance (accuracy scores). There was a significant relationship between offline gains in accuracy and coupled spindle percent change during the upstate in older, but not younger adults.
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