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About Sleep's Role in Memory Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2013 About sleep’s role in memory Rasch, Björn ; Born, Jan Abstract: Over more than a century of research has established the fact that sleep benefits the retention of memory. In this review we aim to comprehensively cover the field of ”sleep and memory” research by providing a historical perspective on concepts and a discussion of more recent key findings. Whereas ini- tial theories posed a passive role for sleep enhancing memories by protecting them from interfering stimuli, current theories highlight an active role for sleep in which memories undergo a process of system con- solidation during sleep. Whereas older research concentrated on the role of rapid-eye-movement (REM) sleep, recent work has revealed the importance of slow-wave sleep (SWS) for memory consolidation and also enlightened some of the underlying electrophysiological, neurochemical, and genetic mechanisms, as well as developmental aspects in these processes. Specifically, newer findings characterize sleep as abrain state optimizing memory consolidation, in opposition to the waking brain being optimized for encoding of memories. Consolidation originates from reactivation of recently encoded neuronal memory represen- tations, which occur during SWS and transform respective representations for integration into long-term memory. Ensuing REM sleep may stabilize transformed memories. While elaborated with respect to hippocampus-dependent memories, the concept of an active redistribution of memory representations from networks serving as temporary store into long-term stores might hold also for non-hippocampus- dependent memory, and even for nonneuronal, i.e., immunological memories, giving rise to the idea that the offline consolidation of memory during sleep represents a principle of long-term memory formation established in quite different physiological systems. DOI: https://doi.org/10.1152/physrev.00032.2012 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-77770 Journal Article Originally published at: Rasch, Björn; Born, Jan (2013). About sleep’s role in memory. Physiological reviews, 93(2):681-766. DOI: https://doi.org/10.1152/physrev.00032.2012 Physiol Rev 93: 681–766, 2013 doi:10.1152/physrev.00032.2012 ABOUT SLEEP’S ROLE IN MEMORY Björn Rasch and Jan Born Division of Biopsychology, Neuroscience Center Zurich and Zurich Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland; and Institute of Medical Psychology and Behavioral Neurobiology, and Center for Integrative Neuroscience, University of Tuebingen, Tuebingen, Germany Rasch B, Born J. About Sleep’s Role in Memory. Physiol Rev 93: 681–766, 2013; doi:10.1152/physrev.00032.2012.—Over more than a century of research has established the fact that sleep benefits the retention of memory. In this review we aim to comprehensively cover the field of “sleep and memory” research by providing a historical perspective on concepts and a discussion of more recent key findings. LWhereas initial theories posed a passive role for sleep enhancing memories by protecting them from interfering stimuli, current theories highlight an active role for sleep in which memories undergo a process of system consolidation during sleep. Whereas older research concentrated on the role of rapid-eye-movement (REM) sleep, recent work has revealed the importance of slow-wave sleep (SWS) for memory consolidation and also enlightened some of the underlying electrophysio- logical, neurochemical, and genetic mechanisms, as well as developmental aspects in these processes. Specifically, newer findings characterize sleep as a brain state optimizing memory consolidation, in opposition to the waking brain being optimized for encoding of memories. Consol- idation originates from reactivation of recently encoded neuronal memory representations, which occur during SWS and transform respective representations for integration into long-term mem- ory. Ensuing REM sleep may stabilize transformed memories. While elaborated with respect to hippocampus-dependent memories, the concept of an active redistribution of memory represen- tations from networks serving as temporary store into long-term stores might hold also for non-hippocampus-dependent memory, and even for nonneuronal, i.e., immunological memories, giving rise to the idea that the offline consolidation of memory during sleep represents a principle of long-term memory formation established in quite different physiological systems. I. INTRODUCTION 681 A. Sleep II. OVERVIEW OF APPROACHES AND... 684 III. MEMORY REACTIVATIONS DURING... 695 Sleep is defined as a natural and reversible state of reduced IV. SLEEP-SPECIFIC ELECTRICAL... 702 responsiveness to external stimuli and relative inactivity, V. NEUROCHEMICAL SIGNALING... 713 accompanied by a loss of consciousness. Sleep occurs in VI. GENETIC APPROACHES TO... 719 regular intervals and is homeostatically regulated, i.e., a loss VII. DEVELOPMENTAL ASPECTS OF... 726 or delay of sleep results in subsequently prolonged sleep VIII. SLEEP-DEPENDENT MEMORY... 733 (113). Sleep deprivation and sleep disruptions cause severe IX. CONCLUDING REMARKS 736 cognitive and emotional problems (142, 634, 1243), and animals deprived of sleep for several weeks show tempera- I. INTRODUCTION ture and weight dysregulation and ultimately die of infec- tions and tissue lesions (973). Sleep probably occurs in all The capability to form memory is critical to the strategic vertebrates, including birds, fishes, and reptiles, and adaptation of an organism to changing environmental de- sleeplike states are similarly observed in invertebrates like mands. Observations indicating that sleep benefits memory flies, bees, and cockroaches (209). date back to the beginning of experimental memory re- search, and since then have been fitted with quite different Sleep in mammals consists of two core sleep stages: slow- concepts. This review targets this field of “sleep and mem- wave sleep (SWS) and rapid-eye-movement (REM) sleep, ory” research, which has experienced a unique renaissance which alternate in a cyclic manner (FIGURE 1A). In human during the last three decades. Although we have aimed at nocturnal sleep, SWS is predominant during the early part comprehensively covering the field, we might have missed and decreases in intensity and duration across the sleep out or overlooked some aspects, owing to the vast progress period, whereas REM sleep becomes more intense and exten- achieved in the last years. Before we begin, we will briefly sive towards the end of the sleep period. SWS is hallmarked by introduce the core concepts of sleep and memory, respec- slow high-amplitude EEG oscillations (slow wave activity, tively. SWA), whereas REM sleep (also termed paradoxical sleep) is 0031-9333/13 Copyright © 2013 the American Physiological Society 681 BJÖRN RASCH AND JAN BORN Sleep stages A W REM sleep REM N1 N2 N3 Slow wave sleep Early sleep Late sleep 23.00 0.00 1.00 2.00 3.00 4.00 5.00 6.00 7.00 h B Field potential oscillations Slow oscillationSpindle Sharp wave-ripple PGO wave Theta activity up-state down-state C Neuromodulators Acetylcholine Acetylcholine Noradrenaline/ Noradrenaline/ Serotonin Serotonin Cortisol Cortisol FIGURE 1. Typical human sleep profile and sleep-related signals. A: sleep is characterized by the cyclic occurrence of rapid-eye-movement (REM) sleep and non-REM sleep. Non-REM sleep includes slow-wave sleep (SWS) corresponding to N3, and lighter sleep stages N1 and N2 (591). According to an earlier classification system by Rechtschaffen and Kales (974), SWS was divided into stage 3 and stage 4 sleep. The first part of the night (early sleep) is dominated by SWS, whereas REM sleep prevails during the second half (late sleep). B: the most prominent electrical field potential oscillations during SWS are the neocortical slow oscillations (ϳ0.8 Hz), thalamocortical spindles (waxing and waning activity between 10–15 Hz), and the hippocampal sharp wave-ripples (SW-R), i.e., fast depolarizing waves that are generated in CA3 and are superimposed by high-frequency (100–300 Hz) ripple oscillation. REM sleep, in animals, is characterized by ponto-geniculo- occipital (PGO) waves, which are associated with intense bursts of synchronized activity propagating from the pontine brain stem mainly to the lateral geniculate nucleus and visual cortex, and by hippocampal theta (4–8 Hz) activity. In humans, PGO and theta activity are less readily identified. C: sleep is accompanied by a dramatic change in activity levels of different neurotransmitters and neuromodulators. Compared with waking, cholin- ergic activity reaches a minimum during SWS, whereas levels during REM sleep are similar or even higher than those during waking. A similar pattern is observed for the stress hormone cortisol. Aminergic activity is high during waking, intermediate during SWS, and minimal during REM sleep. [Modified from Diekelmann and Born (293).] 682 Physiol Rev • VOL 93 • APRIL 2013 • www.prv.org SLEEP AND MEMORY characterized by wakelike fast and low-amplitude oscillatory integrate newly encoded memory into a long-term store. brain activity. In addition, REM sleep is characterized by pha- Encoding and consolidation might be mutually exclusive sic REMs and by muscle atonia. Almost 50% of sleep in adult processes inasmuch they draw on overlapping neuronal re- humans is marked by a lighter form of non-REM sleep (stage
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