Sleep loss disrupts the neural signature of successful learning.

Anna Á V Guttesen, M Gareth Gaskell, Emily V Madden, Gabrielle Appleby, Zachariah R Cross, Scott A Cairney

Journal: Cerebral cortex (New York, N.Y. : 1991) 2023;33(5):1610-1625

PMID: 35470400

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Plain Language Summary

Understanding how sleep disturbances impair learning and memory is increasingly important in modern society, where many people fail to regularly obtain an adequate amount of sleep. The aim of this study was to investigate the relationship between sleep-associated consolidation and next-day learning and how suppressing slow-wave activity (SWA) [during slow-wave sleep, electrical activity in the brain changes while the body relaxes into deep and restorative rest] contributes to this relationship. This study was a within-subjects (n = 30), crossover design which showed that sleep improved both memory retention and next-day learning however, there was no evidence of a relationship between these measures or with SWA. Furthermore, an absence of sleep disrupts the neural operations underpinning memory encoding, leading to suboptimal performance. Authors conclude that an extended lack of sleep might disrupt the ability to draw upon semantic knowledge when encoding novel associations, necessitating the use of more surface-based and ultimately suboptimal routes to learning.

Abstract

Sleep supports memory consolidation as well as next-day learning. The influential "Active Systems" account of offline consolidation suggests that sleep-associated memory processing paves the way for new learning, but empirical evidence in support of this idea is scarce. Using a within-subjects (n = 30), crossover design, we assessed behavioral and electrophysiological indices of episodic encoding after a night of sleep or total sleep deprivation in healthy adults (aged 18-25 years) and investigated whether behavioral performance was predicted by the overnight consolidation of episodic associations from the previous day. Sleep supported memory consolidation and next-day learning as compared to sleep deprivation. However, the magnitude of this sleep-associated consolidation benefit did not significantly predict the ability to form novel memories after sleep. Interestingly, sleep deprivation prompted a qualitative change in the neural signature of encoding: Whereas 12-20 Hz beta desynchronization-an established marker of successful encoding-was observed after sleep, sleep deprivation disrupted beta desynchrony during successful learning. Taken together, these findings suggest that effective learning depends on sleep but not necessarily on sleep-associated consolidation.

Address: Department of Psychology, University of York, Heslington, York, YO10 5DD, UK.; York Biomedical Research Institute, University of York, Heslington, York, YO10 5DD, UK.; Cognitive Neuroscience Laboratory, Australian Research Centre for Interactive and Virtual Environments, Mawson Lakes Campus, Mawson Lakes, South Australia 5095, Australia.

DOI: 10.1093/cercor/bhac159