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Sleep's Role in the Consolidation of Emotional Episodic Memories

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Sleep's Role in the Consolidation of Emotional Episodic Memories Current Directions in Psychological Science Sleep’s Role in the Consolidation of 19(5) 290-295 ª The Author(s) 2010 Reprints and permission: Emotional Episodic Memories sagepub.com/journalsPermissions.nav DOI: 10.1177/0963721410383978 http://cdps.sagepub.com Jessica D. Payne1 and Elizabeth A. Kensinger2 1 University of Notre Dame and and 2 Boston College Abstract Emotion has a lasting effect on memory, encouraging certain aspects of our experiences to become durable parts of our memory stores. Although emotion exerts its influence at every phase of memory, this review focuses on emotion’s role in the consolidation and transformation of memories over time. Sleep provides ideal conditions for memory consolidation, and recent research demonstrates that manipulating sleep can shed light on the storage and evolution of emotional memories. We provide evidence that sleep enhances the likelihood that select pieces of an experience are stabilized in memory, leading memory for emotional experiences to home in on the aspects of the experience that are most closely tied to the affective response. Keywords affect, amygdala, consolidation, emotion, memory, fMRI, hippocampus, sleep, stabilization, trade-off Episodic memory refers to the long-term retention of contex- consolidated, and affect how events are re-experienced at tually rich representations of past experiences. When we retrieval (see Kensinger, 2009 and McGaugh, 2004 for remember specific events from our past, recalling their spatial reviews). Although emotion’s influence during each of these and temporal context or recollecting perceptual or conceptual phases is critically important, this review focuses on emotion’s details of those events, our memory is considered to be episodic effect on memory consolidation. in nature. Although our experience of episodic memory occurs at the moment of retrieval, when information about the initial experience enters conscious awareness, successful retrieval is Emotional Memory Consolidation: contingent upon the successful completion of at least two ear- A Brief Introduction lier stages of memory formation. First, the experience must be A long-standing question in cognitive neuroscience is how properly encoded. Encoding involves transforming new infor- memory for emotional experience is consolidated over time. mation into a representation capable of being stored in mem- This issue is key to understanding basic mechanisms giving rise ory, just as the key presses we make on keyboard must be to long-lasting emotional memories and for appreciating how converted to a format that can be stored in a computer. Second, those mechanisms may be altered in affective disorders. The the information must be durably stored in a manner that can occurrence of an emotional reaction enhances the likelihood withstand the passage of time, a process known as memory con- that an experience will become consolidated. When an emo- solidation. Only if these processes occur successfully will it be tional reaction occurs, stress hormones (e.g., cortisol, norepi- possible for information from the initial event to be retrieved nephrine) are released, which in turn leads to increased later in time. activation of the amygdala, an almond-shaped region situated The events we care most about remembering are often accompanied by an emotional response, including cognitive, physiological, and somatic reactions. The examination of Corresponding Author: memory for these experiences—the study of ‘‘emotional mem- Elizabeth A. Kensinger, Department of Psychology, Boston College, McGuinn ory’’—has made clear that emotion can intervene at each of the 510, 140 Commonwealth Ave., Chestnut Hill, MA 02467; or Jessica D. memory phases noted above. Emotion has a powerful influence Payne, Department of Psychology, University of Notre Dame, Haggar Hall, on memories. It can alter the likelihood that an experience will Room 122B, Notre Dame, IN 56556 be encoded in memory, influence how memories are E-mail: [email protected] or [email protected] Sleep and Episodic Memory Consolidation 291 in the interior portion of the brain at the level of the ears. The phase of sleep may be particularly important for modulatory amygdala has strong connections with a region that sits just effects on emotional memory (Wagner, Gais, & Born, 2001). behind it: the hippocampus, a seahorse-shaped structure that In humans, medial temporal regions, including the amygdala is critical for the consolidation of episodic memories (reviewed and hippocampus, are more active during REM sleep than dur- by Moscovitch & Nadel, 1998). Because of the strong connec- ing wakefulness, and several studies have correlated features of tions between these regions, amygdala activation by stress hor- REM sleep with memory for emotional information (see mones during or after an emotional experience increases Walker, 2009, for review). REM-rich sleep is also associated activity in the hippocampus, thereby facilitating memory con- with marked increases in cortisol, a stress hormone important solidation, particularly for emotional events (McGaugh, 2004). for the modulation of emotional memory via interactions Neuroimaging studies demonstrate coactivation of the between the amygdala and the hippocampus (Payne & Nadel, amygdala and hippocampus during emotional experiences and 2004). Together, these findings suggest that although sleep is demonstrate that the simultaneous activity of these two regions a state of behavioral quiescence, it is associated with intense increases the likelihood that an emotional experience will be neuronal activity and functional increases in brain regions nec- remembered (reviewed by Strange & Dolan, 2006). A diffi- essary for emotion and memory processing. culty with neuroimaging studies, however, is that they cannot Given this evidence, a growing number of studies have uti- isolate activity during consolidation, because it occurs over lized sleep manipulations to examine memory consolidation. many hours, days, and months, and thus cannot be captured These studies overwhelmingly support a role for sleep in the in a single snapshot of neural activity. Therefore, the correla- long-term storage of episodic information. Many demonstrate tions between amygdala and hippocampal activity could reflect that sleep benefits memory for neutral episodic memory mate- effects during the initial encoding phase of memory rather than rials across various modalities (see Payne, Ellenbogen, et al., during the later consolidation phase. 2008, for review). Interestingly, however, when emotional Stronger evidence to pinpoint an influence of emotion—and (especially emotionally negative) items are intermixed with of amygdala activation more specifically—in memory consoli- neutral items at study, sleep disproportionately benefits the dation comes from studies examining how emotional memories consolidation of emotional relative to neutral memories. For evolve over time. While the initial effects of emotional arousal example, Wagner et al. (2001) reported that memory for nega- on memory can be small or even nonexistent, the effects of tively arousing relative to neutral narratives was facilitated emotional arousal sometimes become more apparent when after 3 hours of late-night, REM-rich sleep known to activate memory is tested after longer delays (see Kensinger, 2009, for the hippocampus and amygdala, but not following equivalent review). In patients with damage to the amygdala, however, amounts of time spent awake or in early-night, slow-wave- these effects of time do not emerge, and patients show no exag- rich sleep. Similarly, others have demonstrated that a full night gerated effect of emotional arousal on memories assessed after of sleep preferentially improves memory accuracy for recogni- a long delay as compared to a short one (LaBar & Phelps, tion of negatively arousing pictures relevant to an equivalent 1998). These findings suggest that interactions between the period of daytime wakefulness (reviewed in Walker, 2009). amygdala and hippocampus influence how emotional mem- These findings strongly suggest a role for sleep in the process- ories develop over time. However, none of these studies can ing of memory for emotional experiences. More broadly, they unambiguously isolate the consolidation phase; it is always provide compelling evidence for the traditional view of mem- possible that patients encode or retrieve emotional information ory consolidation, as a process that solidifies memories in a differently than healthy individuals, or that the compounding veridical manner, true to their form at initial encoding (see effects of amygdala activation on encoding, consolidation, and Payne, Ellenbogen, et al., 2008, for review). retrieval lead to these effects. Sleep provides a means of manip- ulating consolidation-related processes that avoids such Sleep Transforms Memories in difficulties. Useful and Adaptive Ways Sleep’s Role in Emotional It has long been known that memories change with the passage of time, suggesting that the process of consolidation does not Memory Consolidation always yield exact representations of past experiences. On the Converging evidence from many levels of analysis suggests face of it, this may seem strikingly maladaptive, yet such flex- that the sleeping brain provides ideal conditions for memory ibility in memory representation allows the emergence of key consolidation. For example, activation patterns seen during cognitive abilities, such as generalization and inference (Ellen- daytime task training are
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