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Sleep, Memory and Emotion G. A. Kerkhof and H. P. A. Van Dongen (Eds.) Progress in Brain Research, Vol. 185 ISSN: 0079-6123 Copyright Ó 2010 Elsevier B.V. All rights reserved. CHAPTER 4 Sleep, memory and emotion Matthew P. Walker* Sleep and Neuroimaging Laboratory, Department of Psychology, Helen Wills Neuroscience Institute, University of California, Berkeley, CA, USA Abstract: As critical as waking brain function is to cognition, an extensive literature now indicates that sleep supports equally important, different, yet complementary operations. This review will consider recent and emerging findings implicating sleep, and specific sleep-stage physiologies, in the modulation, regulation and even preparation of cognitive and emotional brain processes. First, evidence for the role of sleep in memory processing will be discussed, principally focusing on declarative memory. Second, at a neural level, several mechanistic models of sleep-dependent plasticity underlying these effects will be reviewed, with a synthesis of these features offered that may explain the ordered structure of sleep, and the orderly evolution of memory stages. Third, accumulating evidence for the role of sleep in associative memory processing will be discussed, suggesting that the long-term goal of sleep may not be the strengthening of individually memory items, but, instead, their abstracted assimilation into a schema of generalized knowledge. Forth, the newly emerging benefit of sleep in regulating emotional brain reactivity will be considered. Finally, and building on this latter topic, a novel hypothesis and framework of sleep-dependent affective brain proces- sing will be proposed, culminating in testable predictions and translational implications for mood disorders. Keywords: Sleep; emotion; affect; memory; encoding; consolidation; integration; SWS; REM; reactivation Introduction sleep is a brain phenomenon, and over the past 20 years, an exciting revival has taken place within the Despite the vast amount of time this state takes neurosciences, focusing on the question of why we from our lives, we still lack any consensus function sleep, and specifically targeting the role of sleep in a for sleep. In part, this is perhaps because sleep, like number of cognitive and emotional processes. This its counterpart wakefulness, may serve not one but chapter aims to provide a synthesis of these recent many functions, for brain and body alike. Centrally, findings in humans, with the goal of extracting * Corresponding author. Tel.: (+) 510 642 5292; Fax: (+) 510 642 5293. E-mail: [email protected] DOI:10.1016/B978-0-444-53702-7.00004-X 49 50 consistent themes across domains of brain function that ‘temporal memory’ (memory for when events that appear to be regulated by sleep. ‘Memory pro- occur) was significantly disrupted by a night of pre- cessing and brain plasticity’ section will explore the training sleep loss. These findings have been revis- role of sleep in memory and brain plasticity, and ited in a more rigorous study by Harrison and also examine competing models of sleep-dependent Horne (2000), again using the temporal memory learning. ‘Association, integration and creativity’ paradigm. Significant impairments in retention section will address the role of sleep beyond mem- were evident in a group of subjects deprived of ory consolidation, in processes of association, inte- sleep for 36 h, scoring significantly lower than con- gration and creativity. Finally, ‘Emotional regula- trols, even in a subgroup that received caffeine to tion’ section will discuss the more recent and overcome non-specific effects of lower alertness. emerging role for sleep in emotional and affective Furthermore, the sleep-deprived subjects dis- brain regulation. played significantly worse insight into their mem- ory encoding performance, resulting in lower pre- dictive ability of performance. Memory processing and brain plasticity Pioneering work by Drummond and colleagues has examined the neural basis of similar memory When considering the role of sleep in memory impairments using fMRI, investigating the effects processing, it is pertinent to appreciate that mem- of 35 h of total sleep deprivation on verbal learning ories evolve (Walker and Stickgold, 2006). (Drummond et al., 2000). In those who were sleep Specifically, memories pass through discrete stages deprived, regions of the medial temporal lobe in their ‘lifespan’. The conception of a memory (MTL) were significantly less active during learn- begins with the process of encoding, resulting in ing, relative to a control group that had slept, while an initial stored representation of an experience the prefrontal cortex actually expressed greater within the brain. However, it is now understood activation. Most interesting, the parietal lobes, that a vast number of post-encoding memory pro- which were not activated in the control group dur- cesses can take place. For memories to persist over ing learning, were significantly active in the depri- the longer time course of minutes to years, an off- vation group. Such findings suggest that inade- line, non-conscious operation of consolidation quate sleep (at least following one night) prior to appears to be necessary, affording memories learning produces bi-directional changes in epi- greater resistance to decay (a process of stabiliza- sodic encoding activity, involving the inability of tion), or even improved recollection (a process of the MTL to engage normally during learning, com- enhancement). Sleep has been implicated in both bined with potential compensation attempts by the encoding and consolidation of memory. prefrontal regions, which in turn may facilitate recruitment of parietal lobe function (Drummond and Brown, 2001). Sleep and memory encoding The impact of sleep deprivation on memory for- mation may be especially pronounced for emo- In contrast to the role of sleep after learning pro- tional material. We have investigated the impact moting offline consolidation (discussed below), of sleep deprivation on the encoding of emotion- emerging evidence indicates an important need ally negative, positive and neutral words (Walker for sleep before learning in preparing specific brain and Stickgold, 2006). When combined across all networks for initial encoding of information. One stimulus types, subjects in the sleep-deprived con- of the earliest human studies to report the effects of dition exhibited a striking 40% reduction in the sleep and sleep deprivation on declarative memory ability to form new human memories under condi- encoding was by Morris et al. (1960), indicating tions of sleep deprivation. When these data were 51 separated into the three affective categories (neg- phylogeny. Perhaps the earliest reference to the ative, positive or neutral), the magnitude of encod- beneficial impact of sleep on memory is by the ing impairment differed. In those that had slept, Roman rhetoritician, Quintilian, stating that both positive and negative stimuli were associated with superior retention levels relative to the neu- ...[it] is a curious fact, of which the reason is tral condition, consonant with the notion that emo- not obvious, that the interval of a single night tion facilitates memory encoding. However, there will greatly increase the strength of the mem- was severe disruption of encoding and hence later ory... Whatever the cause, things which retention for neutral and especially positive emo- could not be recalled on the spot are easily tional memory in the sleep-deprived group. In con- trast, a relative resistance of negative emotional coordinated the next day, and time itself, memory was observed in the deprivation group. which is generally accounted one of the These data suggest that, while the effects of sleep causes of forgetfulness, actually serves to deprivation are directionally consistent across strengthen the memory. memory sub-categories, the most profound impact is on the encoding of positive emotional stimuli, A robust and consistent literature has demon- and to a lesser degree, emotionally neutral stimuli. strated the need for sleep after learning in the In contrast, the encoding of negative memory subsequent consolidation and enhancement of appears to be more resistant to the effects of prior procedural memories; the evidence for which has sleep loss, at least following one night. recently been reviewed elsewhere (Walker and The impact of sleep deprivation on the neural Stickgold, 2006). Early work focusing on the role dynamics associated with declarative memory for sleep in declarative memory processing was encoding has recently been examined using somewhat less consistent, but more recent find- event-related fMRI (Yoo et al., 2007a). In addition ings have now begun to reveal a robust beneficial to performance impairments under condition of effect of sleep on the consolidation of declarative sleep deprivation, and relative to a control group memory – our focus here. that slept, a highly significant and selective deficit Several reports by Born and his colleagues have was identified in bilateral regions of the hippocam- shown offline improvement on a word-pair associ- pus – a structure known to be critical for learning ates task following sleep, attributed to early night new episodic information. When taken together, sleep, rich in SWS (Diekelmann and Born, 2010). this collection of findings indicate the critical need More recently, the same group has demonstrated for sleep before learning in preparing key neural that, in addition to classically defined slow delta structures
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