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

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          Abstract

          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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          Most cited references62

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          Theta oscillations in the hippocampus.

          Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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            Memory--a century of consolidation.

            J McGaugh (2000)
            The memory consolidation hypothesis proposed 100 years ago by Müller and Pilzecker continues to guide memory research. The hypothesis that new memories consolidate slowly over time has stimulated studies revealing the hormonal and neural influences regulating memory consolidation, as well as molecular and cellular mechanisms. This review examines the progress made over the century in understanding the time-dependent processes that create our lasting memories.
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              The amygdala modulates the consolidation of memories of emotionally arousing experiences.

              Converging findings of animal and human studies provide compelling evidence that the amygdala is critically involved in enabling us to acquire and retain lasting memories of emotional experiences. This review focuses primarily on the findings of research investigating the role of the amygdala in modulating the consolidation of long-term memories. Considerable evidence from animal studies investigating the effects of posttraining systemic or intra-amygdala infusions of hormones and drugs, as well as selective lesions of specific amygdala nuclei, indicates that (a) the amygdala mediates the memory-modulating effects of adrenal stress hormones and several classes of neurotransmitters; (b) the effects are selectively mediated by the basolateral complex of the amygdala (BLA); (c) the influences involve interactions of several neuromodulatory systems within the BLA that converge in influencing noradrenergic and muscarinic cholinergic activation; (d) the BLA modulates memory consolidation via efferents to other brain regions, including the caudate nucleus, nucleus accumbens, and cortex; and (e) the BLA modulates the consolidation of memory of many different kinds of information. The findings of human brain imaging studies are consistent with those of animal studies in suggesting that activation of the amygdala influences the consolidation of long-term memory; the degree of activation of the amygdala by emotional arousal during encoding of emotionally arousing material (either pleasant or unpleasant) correlates highly with subsequent recall. The activation of neuromodulatory systems affecting the BLA and its projections to other brain regions involved in processing different kinds of information plays a key role in enabling emotionally significant experiences to be well remembered.
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                Author and article information

                Journal
                Cereb Cortex
                cercor
                cercor
                Cerebral Cortex (New York, NY)
                Oxford University Press
                1047-3211
                1460-2199
                May 2009
                1 October 2008
                1 October 2008
                : 19
                : 5
                : 1158-1166
                Affiliations
                [1 ]Sleep and Neuroimaging Laboratory Department of Psychology and Helen Wills Neuroscience Institute, University of California, Berkeley, CA 94702, USA
                [2 ]Section of Psychiatry and Behavioral Science, Tokyo Medical and Dental University Graduate School, 1-5-45 Yushima, Bunkyo, Tokyo, Japan
                [3 ]Department of Psychology, Center for Brain Science, Howard Hughes Medical Institute, Harvard University, Davis, CA 95618, USA
                [4 ]Departments of Psychiatry and Radiology, Anthinoula A. Martinos Center, Massachusetts General Hospital, Boston, MA 02114, USA
                Author notes
                Address correspondence to Matthew P. Walker, PhD, Department of Psychology, Tolman Hall 3331, University of California, Berkeley, CA 94720-1650, USA. Email: mpwalker@ 123456berkeley.edu .
                Article
                10.1093/cercor/bhn155
                2665156
                18832332
                17a8e721-6513-4fd9-b567-6aa8d3cfe487
                © 2008 The Authors

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Categories
                Articles

                Neurology
                memory,prefrontal,theta,emotion,rem,consolidation
                Neurology
                memory, prefrontal, theta, emotion, rem, consolidation

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