REM Sleep, Prefrontal Theta, and the Consolidation of Human Emotional Memory

Sleep and Neuroimaging Laboratory Department of Psychology and Helen Wills Neuroscience Institute, University of California, Berkeley, CA 94702-1650, USA.
Cerebral Cortex (Impact Factor: 8.67). 11/2008; 19(5):1158-66. DOI: 10.1093/cercor/bhn155
Source: PubMed


Both emotion and sleep are independently known to modulate declarative memory. Memory can be facilitated by emotion, leading to enhanced consolidation across increasing time delays. Sleep also facilitates offline memory processing, resulting in superior recall the next day. Here we explore whether rapid eye movement (REM) sleep, and aspects of its unique neurophysiology, underlie these convergent influences on memory. Using a nap paradigm, we measured the consolidation of neutral and negative emotional memories, and the association with REM-sleep electrophysiology. Subjects that napped showed a consolidation benefit for emotional but not neutral memories. The No-Nap control group showed no evidence of a consolidation benefit for either memory type. Within the Nap group, the extent of emotional memory facilitation was significantly correlated with the amount of REM sleep and also with right-dominant prefrontal theta power during REM. Together, these data support the role of REM-sleep neurobiology in the consolidation of emotional human memories, findings that have direct translational implications for affective psychiatric and mood disorders.

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Available from: Masaki Nishida, Oct 11, 2015
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    • "Several studies have suggested that emotional memories are preferentially consolidated during sleep (Wagner et al. 2001, 2006; Hu et al. 2006; Payne et al. 2008), and that the brain regions supporting such memories undergo distinct changes overnight, when compared with their neutral counterparts (Sterpenich et al. 2007, 2009; Lewis et al. 2011; Payne and Kensinger 2011). Although some work has implicated REM in emotional memory consolidation (Wagner et al. 2001; Nishida et al. 2009; Payne et al. 2012; Groch et al. 2013), other studies have failed to demonstrate such a relationship (Baran et al. 2012), and research addressing the role of SWS in this process is particularly limited (Groch et al. 2011). Moreover, since recent work has suggested that highly salient memories are selectively supported by slow oscillation activity (Wilhelm et al. 2011), it is possible that SWS may facilitate the consolidation of inherently salient emotional information. "
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    ABSTRACT: Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation, the role of slow-wave sleep (SWS) in this process is largely uncharacterized. In the present study, we investigated the relative impacts of nocturnal SWS and REM upon the consolidation of emotional memories using functional magnetic resonance imaging (fMRI) and polysomnography (PSG). Participants encoded emotionally positive, negative, and neutral images (remote memories) before a night of PSG-monitored sleep. Twenty-four hours later, they encoded a second set of images (recent memories) immediately before a recognition test in an MRI scanner. SWS predicted superior memory for remote negative images and a reduction in right hippocampal responses during the recollection of these items. REM, however, predicted an overnight increase in hippocampal–neocortical connectivity associated with negative remote memory. These findings provide physiological support for sequential views of sleep-dependent memory processing, demonstrating that SWS and REM serve distinct but complementary functions in consolidation. Furthermore, these findings extend those ideas to emotional memory by showing that, once selectively reorganized away from the hippocampus during SWS, emotionally aversive representations undergo a comparably targeted process during subsequent REM.
    Cerebral Cortex 06/2015; DOI:10.1093/cercor/bht349 · 8.67 Impact Factor
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    • "Strong emotional tone strengthens memory associations (Cahill, Haier et al. 1996; Hamann, Ely et al. 1999). REM sleep enhances 'emotional memory' (Cahill and McGaugh 1998; Wagner, Gais et al. 2001; Nishida, Pearsall et al. 2009). Although, the category 'emotional memory' may be redundant in the sense that, " Without emotion, there would be no remembering. "
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    ABSTRACT: This article argues both rapid eye movement (REM) and non-rapid eye movement (NREM) sleep contribute to overnight episodic memory processes but their roles differ. Episodic memory may have evolved from memory for spatial navigation in animals and humans. Equally, mnemonic navigation in world and mental space may rely on fundamentally equivalent processes. Consequently, the basic spatial network characteristics of pathways which meet at omnidirectional nodes or junctions may be conserved in episodic brain networks. A pathway is formally identified with the unidirectional, sequential phases of an episodic memory. In contrast, the function of omnidirectional junctions is not well understood. In evolutionary terms, both animals and early humans undertook tours to a series of landmark junctions, to take advantage of resources (food, water and shelter), whilst trying to avoid predators. Such tours required memory for emotionally significant landmark resource-place-danger associations and the spatial relationships amongst these landmarks. In consequence, these tours may have driven the evolution of both spatial and episodic memory. The environment is dynamic. Resource-place associations are liable to shift and new resource-rich landmarks may be discovered, these changes may require re-wiring in neural networks. To realise these changes, REM may perform an associative, emotional encoding function between memory networks, engendering an omnidirectional landmark junction which is instantiated in the cortex during NREM Stage 2. In sum, REM may preplay associated elements of past episodes (rather than replay individual episodes), to engender an unconscious representation which can be used by the animal on approach to a landmark junction in wake. Copyright © 2015. Published by Elsevier Inc.
    Neurobiology of Learning and Memory 04/2015; 122. DOI:10.1016/j.nlm.2015.04.005 · 3.65 Impact Factor
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    • "All three of these studies compared the effects of SWS-rich sleep in the first half of the night with REM-sleep-rich sleep in the second half (split-night design) and revealed that REM-sleep-rich late sleep selectively fostered the consolidation of emotional memories. Furthermore, the study by Nishida et al. (2009) matches our results. The authors compared the effects of a short nap and an interval spent awake (nap-design) on emotional memory consolidation. "
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    ABSTRACT: Emotion boosts the consolidation of events in the declarative memory system. Rapid eye movement (REM) sleep is believed to foster the memory consolidation of emotional events. On the other hand, REM sleep is assumed to reduce the emotional tone of the memory. Here, we investigated the effect of selective REM-sleep deprivation, SWS deprivation, or wake on the affective evaluation and consolidation of emotional and neutral pictures. Prior to an 9-hour retention interval, sixty-two healthy participants (23.5 ± 2.5 years, 32 female, 30 male) learned and rated their affect to 80 neutral and 80 emotionally negative pictures. Despite rigorous deprivation of REM sleep or SWS, the residual sleep fostered the consolidation of neutral and negative pictures. Furthermore, emotional arousal helped to memorize the pictures. The better consolidation of negative pictures compared to neutral ones was most pronounced in the SWS-deprived group where a normal amount of REM sleep was present. This emotional memory bias correlated with REM sleep only in the SWS-deprived group. Furthermore, emotional arousal to the pictures decreased over time, but neither sleep nor wake had any differential effect. Neither the comparison of the affective ratings (arousal, valence) during encoding and recognition, nor the affective ratings of the recognized targets and rejected distractors supported the hypothesis that REM sleep dampens the emotional reaction to remembered stimuli. The data suggest that REM sleep fosters the consolidation of emotional memories but has no effect on the affective evaluation of the remembered contents. Copyright © 2015. Published by Elsevier Inc.
    Neurobiology of Learning and Memory 02/2015; 122. DOI:10.1016/j.nlm.2015.02.008 · 3.65 Impact Factor
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