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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    • "Sleep alterations directly affect quality of life and interfere with emotional regulation in BD (Giglio et al., 2009; Michalak et al., 2007). Evidence exists for a relationship between the state of mood prior to sleep and EEG parameters during REM sleep, which seems to play an important role in emotional processing (Nishida et al., 2009). In a systematic review that investigated symptoms prior to outbreaks of manic or depressive episodes in bipolar patients, Jackson and colleagues concluded that changes in sleep patterns were the most common symptom predictor for mania (Jackson et al., 2003). "
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    ABSTRACT: Aim: To compare patterns of sleep and the presence of sleep disturbances in individuals in at-risk mental states (ARMS) for psychosis and bipolar disorder (BD) with a healthy control (HC) group. Methods: This was a comparative study involving 20 individuals in ARMS for psychosis or BD, according to the Comprehensive Assessment of At-Risk Mental States, and 20 age- and sex-matched healthy controls. Quality of sleep in the previous month was assessed using the Pittsburgh Sleep Quality Index, diurnal somnolence was evaluated using The Epworth Sleepiness Scale, and chronotype was determined using the Questionnaire of Morningness/Eveningness (QME). All of the participants underwent polysomnography (PSG) during the entire night for two consecutive nights. The first night aimed to adapt the subject to the environment, and only the data from the second night were used for the analysis. Results: Compared with the HC group, individuals in the ARMS group reported significantly worse sleep quality, as measured by the Pittsburgh Sleep Quality Index. Both groups had scores consistent with daytime sleepiness on the Epworth Sleepiness Scale, and there were no differences with regard to chronotype between the groups, with a predominance of the indifferent type in both groups. In the PSG assessment, we observed increased Sleep Latency (SL) and increased Rapid Eye Movement Sleep Onset Latency (REMOL) in the ARMS group, compared to the HC group. Conclusion: The results of this study indicated that sleep abnormalities could be found early in the course of mental diseases, even in at-risk stages, and support the further investigation of their predictive value in the transition to psychosis and BD.
    Schizophrenia Research 09/2015; DOI:10.1016/j.schres.2015.08.023 · 3.92 Impact Factor
    • "Moreover , subjects with a weak first-night effect did not differ from those with a strong first-night effect with regard to the proportion or absolute amount of SWS. Furthermore, REM sleep has been reported to be critical to the consolidation of memory if the processed information is emotionally salient (Wagner et al., 2001, 2007; Nishida et al., 2009). Along these lines, it has been proposed that during wake state, hippocampal-bound information is encoded within cortical modules. "

    Pharmacopsychiatry; 09/2015
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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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