The Cognitive Psychology of Sleep and MEMORY

2.
31 The Cognitive Psychology of Sleep and Memory

Sara E Alger, Enmanuelle Pardilla-Delgado, Stephen M Mattingly, Tony J Cunningham, and Jessica D Payne, The University of
Notre Dame, Notre Dame, IN, United States
Ó 2017 Elsevier Ltd. All rights reserved.
2.31.1 Introduction 571

2.31.2 An Introduction to the Stages of Sleep 571
2.31.2.1 Stage 1 Sleep 572
2.31.2.2 Stage 2 Sleep 572
2.31.2.3 Slow-Wave Sleep 573
2.31.2.4 Rapid Eye Movement Sleep 573
2.31.3 Classification and Phases of Memory 573
2.31.3.1 Phases of Memory 574
2.31.4 General Theories Regarding Memory Advantages From Sleep 574
2.31.5 Sleep During Consolidation Benefits Memory 576
2.31.5.1 Sleep Facilitates Procedural Memory 576
2.31.5.2 Sleep Facilitates Declarative Memory 577
2.31.5.2.1 Overnight Sleep 577
2.31.5.2.2 Daytime Napping Benefits Memory 578
2.31.5.3 Manipulations of Sleep Physiology and Memory During Sleep 580
2.31.5.3.1 Manipulation of Sleep Physiology 580
2.31.5.3.2 Reactivation of Memory During Sleep 581
2.31.5.4 Sleep and Emotional Memory 582
2.31.5.4.1 Selective Consolidation of Complex Emotional Memories 583
2.31.6 Sleep Deprivation Impairs Memory 584
2.31.6.1 Recent Work on Sleep Deprivation 584
2.31.6.1.1 Functional Imaging and Sleep Deprivation 585
2.31.7 Sleep Prior to Encoding Primes for New Learning 586
2.31.8 Sleep Aids Memory Transformation: Generalization, Integration, and Reorganization 587
2.31.8.1 Preferential Consolidation of Prospective Information 587
2.31.8.2 Integration of New Information Into Existing Stores 588
2.31.8.3 Extraction of Gist 588
2.31.8.4 Inferential Associations 589
2.31.8.5 Creativity 590
2.31.8.6 Gain of Insight 590
2.31.8.7 A Theory of Memory Transformation During Sleep 590
2.31.9 Future Directions and Conclusions 591
References 592
2.31.1 Introduction
We are our memories, formed from our experiences, our knowledge, and our skills. Memories guide our behavior and our
personality and influence our preferences. There is still much to be discovered regarding how we make and store these life-shaping details,
but a myriad of studies point to sleep as a state ideal to both prepare to take on new information and store the material we have already
learned. Unlike the common misconception that the brain shuts down during sleep, this chapter will provide evidence that sleep involves
a highly active collection of brain states with unique electrochemical and neurophysiological properties that support the stabilization and
protection of learned information. We will discuss the impact of both overnight and daytime sleep, as well as the lack of sleep, on both
procedural and declarative memory formation, although focusing primarily on neutral and emotional episodic memories. Beyond this,
we consider the role of sleep in the transformation of memory, including the selective consolidation of elements of our experience that are
most important to remember and the flexible recombination of that information, which better serves us in the future.
2.31.2 An Introduction to the Stages of Sleep
For centuries sleep was considered to be an inactive state in which the brain went silent, allowing the body and mind to restore their
energy through quiet rejuvenation. It was only through the development of polysomnography (PSG) within the last 60 years that
Learning and Memory: A Comprehensive Reference, 2nd edition, Volume 2 http://dx.doi.org/10.1016/B978-0-12-809324-5.21062-6 571
researchers discovered how active the brain truly is during sleep. Rather than shutting down or remaining in a single, unified state for
the night, the sleeping brain progresses through several cycles of distinctive sleep stages, each cycle lasting approximately 90 min
and characterized by idiosyncratic brain activity and neurochemical properties. Knowledge of the electrophysiological and neuro-
chemical makeups of each of these stages allows for a deeper understanding of the role that sleep plays in various forms of memory
consolidation.
A healthy night of sleep typically begins with the transition from wakefulness into the first stage of sleep known as Stage 1
(classically defined by Rechtschaffen and Kales, 1968) or N1 (redefined by the American Academy of Sleep Medicine, Iber
et al., 2007). This is the lightest stage of sleep, and it is quickly followed by the onset of Stage 2, or N2, sleep. Subsequently,
the sleep cycle moves into the deepest stages of sleep known as slow-wave sleep (SWS), which is comprised of Stages 3 and 4,
jointly referred to as N3. Collectively, Stages 1–4 (or N1–N3) are also known as nonrapid eye movement (NREM) sleep. After
a period of deep sleep, the cycle typically moves back up through the lighter stages of sleep before entering rapid eye movement
(REM) sleep. While these 90-min cycles remain largely consistent, the proportion of each stage changes throughout the course of
the night, such that the first half of the night is typically SWS heavy, while the latter half is dominated by REM sleep (see Fig. 1).
Each of these stages is unique and identifiable by their electrophysiological and neurochemical properties.
2.31.2.1 Stage 1 Sleep

Stage 1 sleep is considered a transitory stage between sleep and wakefulness. While a strong alpha rhythm (8–13 Hz) and chaotic eye
movements characterize wakefulness, Stage 1 sleep is marked by a decline in alpha rhythm and the onset of rolling eye movements. A
common visual used to illustrate this stage is a student beginning to nod off in class or while reading a textbook. Individuals in Stage 1
frequently experience brief hallucinations and are easily aroused by external stimuli. Stage 1 sleep is such a slight departure from
wakefulness that people may not report feeling such as they were asleep when awakened.
2.31.2.2 Stage 2 Sleep

Stage 2 is a more noticeable departure from wakefulness (e.g., a student well past the point of nodding off with decreased response
to external stimuli). In Stage 2 sleep, the brain’s background electroencephalogram (EEG) rhythm transitions from primarily alpha
to primarily theta waves (4–8 Hz). The most prominent markers of Stage 2 sleep are K-complexes and sleep spindles. K-complexes
are brief high-amplitude, negative, high-voltage peaks of 100 mV followed by a slower positive complex and a final negative peak.
Sleep spindles are short bursts of sigma activity around the 11–16 Hz range, and two different types of spindles have been identified
based on frequency and regions of generation. Slow spindles originate from frontal brain regions and remain around the 11–14 Hz
range, while fast spindles are generated in centroparietal regions and can reach up to 14–16 Hz. Sleep spindles and K-complexes are
thought to be involved in a variety of roles such as memory reactivation and assimilation (Rosanova and Ulrich, 2005; Tamminen
et al., 2010), learning (Gais et al., 2002; Clemens et al., 2005; Schabus et al., 2004), and increasing arousal thresholds to reduce
external stimulus processing and arousals to protect sleep (Dang-Vu et al., 2011; Schabus et al., 2012). While a great deal more
research is necessary to fully understand the purpose of these neurophysiological phenomena, sleep spindles in particular seem
to play a role in consolidating information, as higher levels of spindle density have been shown to correlate with enhanced memory
performance and increased IQ (see Fogel and Smith, 2011 for review).
Figure 1 The first half of the night is rich in slow-wave sleep, but during the latter half, REM sleep dominates. REM, rapid eye movement; SWS,
slow-wave sleep. From Payne, J.D., 2011a. Learning, memory, and sleep in humans. Sleep. Med. Clin. 6 (1), 15–30.
The Cognitive Psychology of Sleep and Memory 573
2.31.2.3 Slow-Wave Sleep

SWS represents the greatest divergence in brain state from wakefulness. In SWS, there is an overall decrease in activation compared to
the waking brain, including in the limbic regions, areas of the midbrain, and higher cortical areas such as the dorsolateral prefrontal
cortex (Braun et al., 1997). During SWS, it is extremely difficult for external stimuli to penetrate into the processing centers of the
brain, further decreasing the likelihood of arousal (e.g., the student is now facing down, snoring, and drooling into her textbook).
In this stage, the theta waves slow further into high-amplitude, low-frequency oscillations, or delta waves (0.5–4 Hz). Along with
these waves, the hippocampus produces sharp-wave ripples (SWR, 150–250 Hz), occurring in clusters during the transitions between
the up-states of the slow oscillations (SOs) (Steriade et al., 1993; De Gennaro and Ferrara, 2003; Battaglia et al., 2004; Mölle et al.,
2006). These hippocampal ripples are particularly pertinent for the discussion of sleep and memory, as they have been reported to be
temporally related to sleep spindles, which continue throughout SWS (Siapas and Wilson, 1998; Sirota et al., 2003), and reactivate
the areas of the brain that were the most active during learning in the awake state (Pavlides and Winson, 1989; Skaggs and McNaugh-
ton, 1996; Kudrimoti et al., 1999; Nádasdy et al., 1999; Ji and Wilson, 2007). As we will discuss in more detail later (section General
Theories Regarding Memory Advantages From Sleep), research suggests that this reactivation is crucial for declarative memory pro-
cessing and consolidation through durable changes in brain plasticity and long-term potentiation (LTP) (Wilson and McNaughton,
1994; Sirota et al., 2003; Brehens et al., 2005; Whitlock et al., 2006; Diba and Buzsaki, 2007).
The neurochemistry of the brain during SWS is also starkly different from that of wakefulness. Serotonin and norepinephrine
(NE) are at low concentration levels, similar to those during quiet wake. NE is released in bursts from the locus coeruleus during
NREM sleep, particularly during SWS, modulating activity in the neocortex and the hippocampus (Aston-Jones, 2004). These
bursts correlate with sleep spindles and slow oscillations and may be associated with memory consolidation (Gais et al.,
2011). After a period of learning, NE levels have been shown to transiently increase during SWS (Eschenko and Sara, 2008;
Sara, 2009). Furthermore, blocking NE activity with clonidine during NREM sleep results in a reduction of sleep-dependent facil-
itation of memory using an odor recognition task, while an NE reuptake inhibitor increases memory consolidation (Gais et al.,
2011). Meanwhile, the firing rate of acetylcholine (ACh) is nearly negligible at levels less than one-third of that found during active
wake. These reduced ACh levels facilitate feedback from the hippocampus to the neocortex by releasing the suppression of most
glutamatergic synapses, which is theorized to facilitate systems consolidation (see later in section General Theories Regarding
Memory Advantages From Sleep) for declarative memories (Rovira et al., 1983; Herreras et al., 1988; Hasselmo, 1999; Hasselmo
and McGaughy, 2004). We see the importance of ACh when looking at the findings from studies that experimentally increased
ACh during SWS-rich sleep early in the night. The resulting performance on a word associates task, which typically improves
following SWS, is weakened (Gais and Born, 2004). These changes in neurohormonal levels are thought to add further benefit
to memory consolidation during sleep, as they collectively enhance connectivity between hippocampal and neocortical regions.
2.31.2.4 Rapid Eye Movement Sleep

After sustained periods of these deepest stages of sleep, the brain moves briefly back up through the lighter stages of sleep before
entering REM sleep. Interestingly, brain activity during REM sleep bears a striking resemblance to that of the waking brain with low-
amplitude, high-frequency predominantly beta and theta activity in the 13–30 Hz range, often described as “saw-tooth waves.” REM
sleep can also be identified by a drastic reduction in electromyogram muscle tone and the appearance of periodic REMs in electro-
oculogram recordings (Carskadon and Dement, 1989). Another notable component of REM sleep includes the phasic ponto-
geniculo-occipital (PGO) waves or bursts of activity between the pons, lateral geniculate nucleus of the thalamus, and occipital
lobe. These waves may play a role in moderating the timing of the REMs (McCarley, 2007). REM sleep is typically associated
with experiencing the most active and vivid dreams, and the reduction in muscle tone is necessary to prevent us from physically
acting out our dreams. Importantly, the limbic region and other brain areas associated with the experience of emotion and memory
reach activity levels even higher than wake.
The neurochemistry of the brain in REM sleep involves the interplay between “REM-off” and “REM-on” cells, again primarily
involving the neuromodulators NE, serotonin, and ACh. ACh levels go from a low during SWS to their highest levels during
REM sleep, with concentrations more than 1.5 times greater than those found during the waking state in brain areas such as the
hippocampus and surrounding regions (Maquet et al., 1996; Rosenthal, 1998; Hasselmo, 1999). NE and serotonergic levels,
however, drop to near negligible levels. The resulting suppression of glutamatergic receptors again shuts down the flow of informa-
tion from the hippocampus to the neocortex (Hasselmo, 1999) and inhibits GABAergic, spindle-generating neurons in the reticular
nucleus of the thalamus that are typically active during Stage 2 sleep and SWS. These conditions foster intracortical communication
and are conducive to the integration of newly learned information into existing neocortical stores, semanticization of information,
and promotion of flexible use of information throughout the cortex without hippocampal interference (Payne, 2011a). It has been
theorized that the conditions of REM sleep may be ideal for processing and consolidating emotional experiences, allowing for the
integration of these memories without lasting physiological emotional responses (Walker, 2009; McGaugh, 2004). Others,
however, suggest that SWS is also important for emotional memory processing (Groch et al., 2011; Payne et al., 2015).
2.31.3 Classification and Phases of Memory
Before we begin to discuss the relationship between sleep and memory, we first need to define how we are using the term
“memory,” as, like sleep, there are different types and different stages of memory. Many choose to define memory in terms of its
content (e.g., emotional memory, spatial memory), its duration (e.g., working, short-term, and long-term memory), its relationship
to the present (e.g., retrospective vs. prospective memory), its modality (e.g., visual or iconic memory, haptic memory), and/or by
conscious (explicit) or unconscious (implicit) access. Additionally, these different types of memory can overlap and subdivide. For
example, emotional memory can be defined both by its affective content and as a form of declarative memory in that it can be
accessed consciously and explicitly talked about. While sleep has been used as a tool to examine many types of memory, we
find it easiest and most relevant to consider memory in terms of long-term memory. For the purposes of this chapter, we primarily
consider procedural memory (implicit memory for skills and actions, such as tracing a shape while looking in a mirror or tapping
fingers in a particular sequence) and declarative memory (explicit memory for facts and experiences that can be stated).
Declarative memory can be further divided to include semantic and episodic memory. Semantic memory is general knowledge,
including facts, such as Paris is the capital of France, as well as features or expectations of things, such as dogs have four legs and fur or
that a birthday party includes cake and balloons. Episodic memory, on the other hand, allows for “mental time travel” (Tulving,
1985) and recollection of an event or experience, as well as autobiographical memory, which combines semantic and episodic
memory. A special category of declarative memory is emotional memory, composed of an episodic experience tied to a physiological
reaction that is associated with the emotional salience of the experience (Hamann, 2001; Kensinger, 2009). Emotionally salient infor-
mation typically evokes feelings of positivity or negativity and often alters levels of arousal, such as the experience and subsequent
memory of the birth of a child or the death of a loved one. Declarative memory also includes spatial memory or the ability to form
a mental map – for example, the ability to describe a route to a specific location and the ability to reverse the route for a return trip.
While memory comes in many forms, sleep has been shown through a variety of manipulations, including full nights, partial nights,
naps, and sleep deprivation, to modulate declarative memory through preservation, enhancement, and/or integration.
Various brain regions are involved in forming and storing memories. Current models of declarative memory emphasize the medial
temporal lobe (MTL), and more specifically, the hippocampus, in the formation and preservation of information (Eichenbaum, 2000;
Davachi, 2004; Moscovitch et al., 2005). The hippocampus acts as a hub that combines different modalities (e.g., remembering both
sound and sight) and organizes this information into a cohesive, temporally ordered representation in neuronal form to create
a memory. The importance of the hippocampus for memory formation and memory access becomes especially apparent in people
with hippocampal damage who exhibits difficulty forming new memories, as well as graded memory for prior experiences, with more
recent memories lost and more remote memories still relatively accessible (Scoville and Milner, 1957). In addition to the central role
of the hippocampus, other brain regions devoted to different elements of memory can support and strengthen memory through
modulation of hippocampal activity (Lang et al., 1997; Abe, 2001). For instance, emotional memories are typically better remem-
bered than neutral memories, and emotion has been strongly linked to activity in the amygdala (Hamann et al., 1999, 2002;
Kensinger and Schacter, 2006; McGaugh, 2004). Amygdalar activity can influence hippocampal and caudate nucleus reactivity to
epinephrine and cortisol (McGaugh, 2000, 2004), and this amygdalar influence on the hippocampus has been shown via functional
magnetic resonance imaging (fMRI) to predict subsequent emotional memory (Ritchey et al., 2008). While these benefits are apparent
after a few minutes (Kensinger and Corkin, 2003), emotional effects are most apparent over longer consolidation delays that can take
a day or more (Sharot and Yonelinas, 2008; Payne and Kensinger, 2010 for review) and can be further enhanced if the delay contains
sleep (Wagner et al., 2001; Hu et al., 2006; Payne et al., 2008).
2.31.3.1 Phases of Memory

Events do not just become memories in our mental stores immediately as they are experienced. Rather, information goes through
several stages of processing to become long-term, accessible memory, including encoding, consolidation/storage, and retrieval. First,
information must be encoded, a term that encompasses both the initial acquisition of new information and the transformation of
this information into mental representations in the brain. All the external input filtering through the individual sensory cortices,
influenced by the current internal physiological state, are held temporarily together as a representation of that particular experience
by the structures in the MTL, namely the hippocampus. In this state, the memory would quickly decay if no further processing
occurred. Thus, the next stage of memory, consolidation, must ensue for long-term storage to occur. Over the subsequent hours,
days, and even years, these neural representations are stabilized and further protected from interference from competing informa-
tion. This crucial stage is still not fully understood, with suggestions that it will be broken down into substages of stabilization and
enhancement (Walker and Stickgold, 2006), or that it goes beyond simple stabilization and enhancement to produce qualitative
changes in memory representations, especially as these memories are reconsolidated (for review, see Payne and Kensinger, 2010;
Payne, 2011a,b). Finally, to access a memory, the final stage of memory, retrieval, must occur.
Much of the sleep and memory literature focuses on the consolidation phase of memory and we will spend the majority of the
chapter discussing these findings, primarily as they apply to declarative memory. We will also consider the evidence of a role for
sleep prior to encoding new information, both examining healthy sleep as well as sleep deprivation procedures. Finally, we consider
how sleep aids the integration and transformation of memory in a way that optimally preserves the most useful and relevant
elements contained in the information stream. First, however, we consider the widely held theories and models explaining the
cognitive neuroscience of sleep and memory processing.
2.31.4 General Theories Regarding Memory Advantages From Sleep
While it is not conclusive, there is an overwhelming amount of evidence that points to an active role for sleep in memory process-
ing. Those who argue against active processes suggest that memories benefit from a period of sleep compared to remaining awake
simply due to the fact that sleep provides a state that attenuates external stimulation that could potentially interfere with the
memory trace. Early research, such as the seminal study by Jenkins and Dallenbach (1924), provides findings in line with this
theory, demonstrating that once the sleep period is over, the memory is once again susceptible to interference (Vertes and Siegel,
2005). Conversely, the active hypothesis postulates that there are attributes of sleep, such as particular sleep stages, oscillatory
activity, and other sleep-based phenomena that actively facilitate memory consolidation via plastic changes in the brain. Activities
such as SWRs and sleep spindles (discussed later) are theorized to be examples of these active processes. As we will also discuss,
evidence such as changes in hippocampal activation and reorganization of brain circuitry after sleep, changes in spindle density
and slow-wave activity (SWA) following learning, and alterations in memory following manipulations of sleep physiology and
reactivation of memory during sleep support this active role. We note here that while we will focus on these active processes during
sleep, we acknowledge the literature that provides evidence of consolidation during quiet rest, possibly through active processes
similar to those seen during sleep (e.g., neural reactivation, facilitated connectivity between hippocampus and neocortex). The
opportunistic theory suggests that consolidation might not depend on sleep, but rather, that the brain opportunistically consoli-
dates previously encoded memories whenever the hippocampus is not occupied by encoding new memories, such as during quiet
wake (Wixted, 2004; Tambini et al., 2010; van Kesteren et al., 2010; Staresina et al., 2013; Schlichting and Preston, 2014; Brokaw
et al., 2016; Hermans et al., 2016).
There are two widely investigated theoretical models that detail the mechanisms behind how sleep actively facilitates memory
formation (see Fig. 2). The first theory, the two-stage model of memory consolidation (Buzsaki et al., 1983; Buzsaki, 1989; McClel-
land et al., 1995; see Fig. 2B), proposes that memory is rapidly encoded from the environment and relies on the hippocampus for its
initial storage. During SWS, SWR complexes trigger the reactivation of neural networks representing learned information (Pavlides
and Winson, 1989; Wilson and McNaughton, 1994; Ji and Wilson, 2007), as those networks are typically the more recent and/or
more potentiated synaptic connections. This replay is thought to lead to LTP, resulting eventually in pre- and postsynaptic changes
(Sirota et al., 2003; Brehens et al., 2005; Whitlock et al., 2006; Diba and Buzsaki, 2007). These changes due to LTP strengthen the
connection between the cells in the network, making them more likely to fire together in the future (Hebb, 1949; Bliss and
Figure 2 Theories of sleep benefits to memory. (A) The synaptic homeostasis hypothesis theorizes that as synapses become potentiated during
waking activity (large yellow nerve ending), this results in net increases in synaptic strength (W ¼ synaptic weight). New synapses (small yellow) and
inactive synapses (small unfilled) do not increase in strength. During subsequent SWS, slow oscillations globally downscale synaptic strength
(burgundy nerve endings) resulting in the weaker connections being eliminated. The relative strength of the remaining connections is preserved.
Through an increase in signal-to-noise ratio, the memory is enhanced. (B) The active system consolidation model presumes that waking experiences
are encoded in both neocortical and hippocampal networks. Slow oscillations during subsequent SWS participate in repeatedly reactivating these
representations in the hippocampus, synchronized with sharp-wave ripples and spindles. This enables systems consolidation, which stabilizes the
memory in the neocortex through persistent synaptic plastic changes [e.g., expression of immediate early genes (IEG) through Ca2þ/calmodulin-
dependent protein kinase II (CaMKII) and protein kinase A (PKA) activation] supported primarily by subsequent REM sleep. AMPAR, amino-3-hydroxy-
5-methyl-4-isoxazole propionic acid receptor; LTP, long-term potentiation; NMDAR, N-methyl-D-aspartate receptor; REM, rapid eye movement; SWS,
slow-wave sleep. From Diekelmann, S., Born, J., 2010. The memory function of sleep. Nat. Rev. Neurosci. 11 (2), 114–126
Lomo, 1973). With sufficient initial strength and reactivation, connections between regions of the neocortex involved in the experi-
ence are strengthened, leading to systems consolidation, where future reactivation of the memory is no longer entirely dependent on
the hippocampus (Buzsaki, 1989; see also Nadel et al., 2000).
Several studies have demonstrated increased hippocampal SWR complexes during SWS after a period of learning, which were
correlated with successful subsequent memory retrieval (Eschenko et al., 2008; Ramadan et al., 2009). As mentioned earlier, sleep
spindles are temporally correlated with SWRs (Siapas and Wilson, 1998; Sirota et al., 2003) as well as with SOs (Steriade and
Timofeev, 2003; Mölle et al., 2009) and can be considered plastic events themselves (Rosanova and Ulrich, 2005). Therefore,
it is not surprising that they play a role in this type of memory consolidation. Many studies have found increased sleep spindle
density, compared to baseline activity, during sleep following a learning session. In turn, this increase is often correlated with
better performance, demonstrating the involvement of sleep spindles in the reactivation and stabilization of memory (Gais
et al., 2002; Schabus et al., 2004; Clemens et al., 2005; Eschenko et al., 2006).
Another prominent theory, the synaptic homeostasis hypothesis, proposes that sleep, especially SWS, is optimally suited to reduce
neuronal drain on resources by lowering membrane potentials across the whole brain (Tononi and Cirelli, 2003; such a see Fig. 2A).
As the waking day progresses, synapses are continuously potentiated, neural resources are depleted, and the firing threshold is raised,
eventually reducing the plastic capabilities of neurons. This means that as the potentiation increases, the possibility of learning new
information decreases. In relation to this potentiation, the homeostatic need for SWS increases, as SWS facilitates the “resetting” of the
synaptic potential and neural resources. As the need for SWS increases, more SWS is obtained closely following sleep onset, but then
gradually decreases over the sleeping period. The synchronous hyperpolarization and depolarization that occurs during SWS changes
the membrane potential, serving to globally downscale, or reduce synaptic potentials, bringing them back to baseline levels. Inter-
estingly, regionally specific increases in SWA have been shown to correlate with the location of activation during intensive learning,
showing that SWS can locally and globally return the brain to baseline (Huber et al., 2004). By this theory, memory is a by-product of
this active process. Synapses involved in a learning experience are potentiated to a greater degree than those spontaneously firing or
firing in response to everyday experiences. Downscaling reduces the latter below firing threshold while the stronger memory connec-
tions remain above threshold, benefitting a memory through an increase in the signal-to-noise ratio. It is unclear, however, if down-
scaling benefits memory by occurring in the hippocampus proper, which has conflictingly been shown to maintain firing rate over
time (Buzsaki et al., 2002), or only the cortical areas potentiated by learning and associated with the memory trace.
It is important to note that these two theories are not mutually exclusive. Both consolidation and downscaling processes could
occur simultaneously, with systems consolidation from the hippocampus to the neocortex happening in conjunction with global
downscaling to reset the brain (see iOtA theory in section Extraction of Gist; Lewis and Durrant, 2011; Holz et al., 2012). Notably,
the earlier mentioned theories emphasize the role of SWS in memory consolidation and are primarily describing the consolidation
of declarative memory. While procedural memory is thought to also benefit through reactivation mechanisms, there is little
consensus on which stage of sleep is related to this process. Additionally, while emotional memory is considered declarative, there
is evidence for a relationship between REM sleep and consolidation of information with emotional content, as will be discussed in
section Sleep and Emotional Memory. Moreover, there is evidence that the sequential occurrence of sleep stages may be necessary to
fully consolidate and integrate new information, with early SWS serving to begin consolidation processes that are completed during
REM sleep (i.e., a two-step model of memory consolidation; Stickgold et al., 2000). These findings hint that these suggested models
are not yet comprehensive. It may be that there is a more complex mechanism at play than is described by the two earlier discussed
theories.
2.31.5 Sleep During Consolidation Benefits Memory

2.31.5.1 Sleep Facilitates Procedural Memory
Sleep has time and again been found to confer a robust advantage on procedural memory, which commonly is measured by calcu-
lating the gains in speed and accuracy while performing a task compared to an equal amount of time spent awake. Although the
exact mechanisms by which procedural memories benefit from sleep remain unknown, it may be that, similar to declarative
memory consolidation, reactivation of the memory traces underlies procedural memory consolidation as well, as seen in studies
that use cued reactivation during sleep (Antony et al., 2012; Schönauer et al., 2014). One common procedural task used in these
types of studies is the finger-tapping task. Participants are asked to tap a sequence such as 4-1-3-2-4 with their nondominant hand.
A baseline measure of speed and accuracy is typically measured before a period of sleep or wake during the delay between sessions.
Walker et al. (2002) found that performance on the finger-tapping task significantly improved both speed and accuracy over
a period of overnight sleep compared to daytime wakefulness. Interestingly, these performance gains were related to Stage 2 sleep,
particularly in the late night. Procedural benefits from Stage 2 sleep have also been correlated with sleep spindle activity (Fogel
et al., 2001).
Another commonly used task that evaluates procedural memory is the serial reaction time task (SRTT). This task requires a partic-
ipant to respond to a presented stimulus, such as a visual cue presented at one of the four locations on a screen, by pressing the
appropriate button with his/her finger corresponding to the stimulus location. A hidden sequence underlies this task, a probabilistic
measure of when a cue will fall in a particular position, such as 2-3-1-4-3-2-4-1-3-4-2-1, and this sequence can be learned. The speed
and accuracy that the participant displays when performing the task indicates how well this skill and underlying sequence is being
learned. The SRTT can be learned implicitly or, like the finger-tapping task, begin explicitly, with improvements developing as the
skill becomes more ingrained and implicit. Robertson et al. (2004) found that when participants were not actively practicing the
skill at the computer, performance was benefitted if the offline delay between sessions contained sleep compared to wakefulness.
This improvement correlated positively with the amount of NREM sleep obtained. Interestingly, they found specifically that when
the skill was acquired explicitly, it was shown to preferentially benefit from sleep compared to if it was implicitly learned (Robertson
et al., 2004).
Stickgold et al. (2000) trained participants on a visual perception task by briefly presenting a series of visual displays containing
horizontal bars within which three diagonal bars were present in one visual quadrant, as well as either the letter “T” or “L” in the
central fixation point. Subjects had to indicate trial-by-trial what letter had been presented as well as whether the diagonal lines were
in a horizontal (i.e., next to one another) or vertical (i.e., one on top of the next) array. This task results in improvement with prac-
tice; however, off-line improvement was shown when the delay between sessions was filled with sleep rather than wake. Interest-
ingly, correlations were found between improvement on the task and the amount of SWS obtained in the first quarter of the night
and REM sleep in the last quarter, both necessary components for improvement. These correlations led the authors to propose
a two-step model of memory consolidation, with early SWS serving to begin consolidation processes that are completed during
the last quarter of REM sleep.
Many procedural tasks involve the isolated use of one hand (typically the nondominant hand), and the skill learning is, by exten-
sion, localized to a particular corresponding region in the brain. Interestingly, sleep-dependent benefits have been shown to be
related to physiological phenomena occurring locally at these particular sites of learning. For example, in the 2004 study by Huber
et al., participants learned a motor task that required them to reach for targets using a handheld cursor while the trajectory of the
cursor was manipulated by rotating it. Therefore, participants had to learn how to compensate for the rotation to reach the target,
a skill that involves the right parietal cortex. Sleep was subsequently recorded using high-density EEG, and this revealed that SWA
was greater over six electrodes recording from the corresponding right parietal regions involved in performing the task. Remarkably,
postsleep performance positively correlated with SWA, but only from these six electrodes. Another study, by Nishida and Walker
(2007), used the finger-tapping task described earlier, which relies on the use of the motor cortex contralateral to the hand perform-
ing the task. After training on the task, participants either napped or remained awake. Only those who napped showed improve-
ment on the task, and this improvement was correlated with Stage 2 sleep. Specifically, when using topographical spindle
analyses to compare spindle activity over the nonlearning hemisphere to the learning hemisphere, they found a positive correlation
between the difference in spindle activity after learning and postnap improvement, indicating a local benefit of sleep to learning.
It is beyond the capacity of this chapter to present a comprehensive review of the ways in which sleep benefits both procedural
and declarative memories, and as such we chose to focus more on the declarative memory system. We refer the interested reader to
Diekelmann and Born (2010), Walker and Stickgold (2006), and Rasch and Born (2013), which provide more extensive reviews on
the procedural memory literature. We now focus on how sleep and sleep deprivation influences the formation and consolidation of
declarative memories.
2.31.5.2 Sleep Facilitates Declarative Memory

There is a vast wealth of evidence that demonstrates the relationship between sleep and declarative memory consolidation,
primarily examining episodic and emotional memory. Further in the chapter, we will discuss the ways in which sleep benefits
semantic memory as well, aiding integration of information and extraction of semantic gist (section Sleep Aids Memory Transfor-
mation: Generalization, Integration, and Reorganization). But first, we will provide evidence from several typically used research
protocols, such as a full night of sleep versus a day of wakefulness, split-night designs examining early and late sleep, and napping.
In section Recent Work on Sleep Deprivation, we will also discuss the damaging effects of sleep deprivation on declarative memory.
2.31.5.2.1 Overnight Sleep

One common task that results in hippocampal dependent declarative memories is the paired-associates task. In this task, two items
are presented and participants are asked to create an association and remember the components as a pair (typically visually presented
word or pictures pairs). Maurer et al. (2015) used a 12-h protocol and had subjects participate in both sleep and daytime wake condi-
tions in counterbalanced order to serve as their own controls. For each condition, participants encoded a novel set of face–name pairs
(in the evening for the sleep condition and in the morning for the wake condition) and during a recognition test 12 h later, they were
shown each encoded face twice, once with the correct associated name and once with a novel name. Participants were asked to report
if they thought the pairing was correct. Comparing sleep to wake conditions within subjects, they report that participants correctly
recognized more face–name pairings after 12 h including sleep compared to 12 h awake. Payne et al. (2012a) also used a paired-
associates task, with participants encoding both semantically related and unrelated word pairs at either 9 a.m. or 9 p.m. and testing
via cued recall occurring either 30 min, 12 h, or 24 h later. Compared to the short delay (with no significant time-of-day differences
between short delay 9 a.m. and 9 p.m. groups), participants in the 12-h condition who slept had less memory deterioration for
semantically unrelated word pairs compared to the 12-h wake participants. Furthermore, participants who were tested 24 h posten-
coding and slept soon after learning had less memory deterioration than participants who slept after a day of wakefulness, demon-
strating the benefit of sleep shortly after learning when the amount of sleep and wake are equated. These results are similar to the ones
obtained by Talamini et al. (2008), who trained participants on face–location associations and tested 10 min later, followed by a
12-h delay including either sleep or wake, or a 24-h delay, with one group sleeping soon after learning and the other experiencing
a day of wakefulness first before sleeping. Similar to Payne et al. (2012a), they report no time-of-day effects on memory, an increase in
forgetting for wake participants relative to sleep participants in the 12-h condition, and more forgetting in the 24-h condition for
participants who remained awake first relative to those who slept soon after learning.
Extended delays such as the 24-h delay not only help to rule out protection from interference as the explanation behind results,
as the sleep-first and wake-first conditions have equivalent amounts of sleep and waking activity, but can also demonstrate the
restorative properties of sleep for memory. For example, Backhaus et al. (2007) conducted a study with both 12-h and
24-h delay, assessing memory for word pairs in children. Learning either occurred in the morning or the evening, followed by
wake or sleep, respectively. The first test, administered 12 h after learning, demonstrated that performance was superior when it
followed sleep compared to wake. Interestingly, when performance was again assessed 24 h after learning, there were no changes
in performance from that measured at 12 h in the sleep-first group. Sleep soon after learning seemingly stabilized the memory trace,
which protected the memory from the effects of subsequent interference and decay incurred during subsequent wakefulness. Perfor-
mance of the wake-first group revealed an interesting effect. At the 12-h test, memory was worse in those who were awake for the day
prior to sleep, but then showed improvement at the 24-h test following the subsequent overnight sleep interval. Other studies have
found similar rejuvenating effects of sleep following a degrading period of wakefulness (Fenn et al., 2003), indicating that in some
cases, sleep can actively restore and recover what decayed during wake.
While many studies use the protocol comparing overnight sleep to daytime wakefulness, other studies have employed designs
created to examine the contributions of different sleep compositions within an overnight period of sleep. One commonly used
method is the split-night design (see Fig. 3). As mentioned earlier, given the cyclical nature of sleep and the varying distributions
of SWS and REM sleep cross the night, researchers can capitalize on the SWS-rich early sleep and REM-rich late sleep to differentiate
the contributions of each kind of sleep to different task performance (Yaroush et al., 1971; Barrett and Ekstrand, 1972; Gais et al.,
2000). In a pivotal study by Plihal and Born (1997), participants encoded declarative word pairs as well as a procedural task in a coun-
terbalanced early/late sleep within-subjects design. On one experimental night, words were encoded in the evening before a 3-h sleep
interval in the early part of the night (11 p.m.–2 a.m.), rich in SWS, and then subjects were awakened and tested. In the other condi-
tion, separated by at least a week, subjects were awakened after 3 h of early sleep to encode a different set of word pairs and procedural
task before the REM sleep-rich second half of the night (3–6 a.m.). Additionally, wake control participants stayed awake between
encoding and testing for the early (11 p.m.–2 a.m.) and late (3 a.m.–6 a.m.) conditions. Plihal and Born (1997) reported that
when participants slept in the early (SWS-rich) part of the night, they had better cued recall memory for the word pairs than
when they slept in the latter half of the night, as well as better memory compared to both wake conditions. REM-rich sleep was found
to benefit the procedural task rather than the declarative associate task relative to the early (SWS-rich) and wake conditions. Plihal and
Born (1999) repeated this study with an object placement task, which utilized spatial memory, also hippocampal dependent, and
reported that early SWS-rich sleep led to better performance than late sleep and wake conditions. Drosopoulos et al. (2005) found
similar results of early sleep benefitting declarative memory, again implicating SWS. Because these studies indicate a role for specific
stages of sleep, namely SWS for declarative memory consolidation, rather than a period of sleep in general, they strongly suggest that
sleep actively promotes learning instead of simply protecting newly learned information from interference. As we will discuss more
later, this early/late sleep split-night paradigm, while not an ideal design to address potential circadian confounds, has been subse-
quently used to implicate active sleep processes in other types of declarative memory consolidation, including emotional memory,
and modulation of physiological reactivity as well (Wagner et al., 2001; Groch et al., 2013).
2.31.5.2.2 Daytime Napping Benefits Memory

The split-night procedure, while it begins to address the unique contributions of sleep stages while equating the amount of sleep
between groups, does have potential confounds inherent to the design. These include differences in sleep pressure and sleep inertia
between the conditions as well as circadian differences in learning and retrieval across conditions. These potential confounds can
(A) Learning Sleep Retrieval
Sleep Learning Sleep Retrieval
1800 1900 2230 0130 0230 0330 0400 0700 1100 1200 hours
(B)
Learning Retrieval
Sleep Learning Retrieval
1800 1900 2230 0130 0230 0330 1100 1200 hours
Figure 3 Experimental protocol from Gais, S., Plihal, W., Wagner, U., Born, J., 2000. Early sleep triggers memory for early visual discrimination
skills. Nat. Neurosci. 3 (12), 1335–1339. (A) Protocol for the early and late sleep condition and (B) for the early and late wake control condition.
White portions represent times when subjects were awake. Gray fields are intervals of sleep, and black fields represent the time of the texture discrim-
ination task.
also be present in designs of daytime wakefulness compared to overnight sleep previously described. Napping protocols, however,
have been increasingly employed to study declarative memory consolidation, offering several benefits over these other study
designs. Naps allow for time-of-day effects to be controlled in that participants who nap and participants who remain awake encode
the information and are tested at the same time of day. Additionally, naps appear to confer similar benefits to memory as compar-
atively longer overnight periods of sleep (although see Lo et al., 2014). Schmidt et al. (2006) examined sleep spindles and spectral
frequencies and discovered increases in spindle density and spindle frequency range spectral power after learning difficult,
compared to easy, paired-associate findings that correlated positively with postnap memory performance. Takashima et al.
(2006) discovered a significant positive relationship between image recognition during retrieval and the amount of SWS obtained
during the 90-min nap opportunity up to 30 days after encoding. These findings were accompanied by a negative correlation
between memory and hippocampal activation, which grew stronger over a 30-day period. The authors interpreted this finding to
mean that after obtaining SWS, there was superior system consolidation from the hippocampus to the neocortex, compared to those
having remained awake. Even dreams reported from NREM sleep during a daytime nap have been found to reflect memory process-
ing. Wamsley et al. (2010) found a positive correlation between dream imagery reported from NREM sleep and postnap perfor-
mance, using a virtual maze-learning task, suggesting that the memory for navigating through the maze is being replayed during
the nap and that this reactivation boosts subsequent memory performance.
Different durations of naps can be used to study sleep stages more finely and with less disruption as well, with very short naps
(5–20 min) typically only including Stage 1 and Stage 2; moderate (20–60 min) naps including Stages 1, 2, and SWS but not
REM; and longer naps (60 min þ) generally including a full cycle of sleep. Lahl, Wispel, Willigens, and Pietrowsky (2008) had partic-
ipants encode a word list and undergo a recall memory test an hour later. In between, participants either remained awake, napped for
approximately 6 min, or napped for around 30 min. Participants demonstrated a dose-dependent memory effect in which those who
napped for 6 min outperformed those who stayed awake, and those who napped for 30 min outperformed those who napped for
6 min. In a study reminiscent of Lahl et al.’s work, Alger et al. (2012) used a bimodal paired-associates task, which required partic-
ipants to bind together visually presented words and familiar sounds, testing them 90 min later. Similar to Lahl et al., participants were
divided into three groups that remained awake, obtained a 10-min nap, or napped for 60 min between encoding and testing. They
replicated the conclusions of Lahl et al., in part, with better memory shortly after the nap/wake retention period in the nap groups
compared to wake, but with better memory after the longer nap than the brief nap. However, the benefit of a 10-min nap was found
to be temporary and not indicative of true memory stabilization. This was determined when using a stimuli-related interference task
that was introduced directly following the initial memory test, where new words were paired with sounds that had previously been
paired with other words. Memory for the paired associates degraded in the 10-min nap group, resulting from retroactive inhibition,
while the memory of those who had slept for 60 min was relatively protected and preserved across time. Memory performance was
superior in the longer nap condition compared to the 10-min nap and wake groups when tested 1 week later. The primary difference
between the short and long naps was the presence of SWS. While the 6-min and 10-min naps in both nap studies (Lahl et al., 2008;
Alger et al., 2012) only contained Stages 1 and 2, the 60-min naps all contained SWS, which may have actively protected and began to
consolidate the memory traces. In fact, similar results from Schabus et al. (2005) found that only nappers who obtained SWS during
a 60-min nap opportunity showed improvement in the declarative task, compared to those who only had Stage 1 and 2 sleep.
In addition to comparing short to long naps, a nap protocol can be used to manipulate the sleep composition or limit sleep to
include only part of a sleep cycle without creating sleep pressure/inertia/deprivation confounds as in the early sleep/late sleep designs.
Tucker et al. (2006) took advantage of the ability to examine NREM sleep only during a nap without incurring REM deprivation
effects to explore the benefit of NREM sleep on declarative memory. They had participants encode verbal paired associates, with
an immediate memory test. Following encoding, participants either napped for about an hour or remained awake, and all partici-
pants were tested through cued recall 5 h after encoding. Nap participants were found to have superior overall memory and better
improvement from baseline. Furthermore, Tucker and Fishbein (2008) demonstrated that a nap only containing NREM sleep lead to
improvement on a declarative memory task, but only when the learned material was strongly encoded prior to the nap. This finding
suggests that the sleeping brain can preferentially process information that was more difficult to learn, perhaps requiring more neural
resources at encoding. These stronger connections formed at encoding likely had a higher probability of reactivating during the NREM
sleep episode (but see Drosopoulos et al., 2007).
Due to circadian influences, naps earlier in the day tend to have higher concentrations of REM and Stage 2 sleep, whereas naps
later in the day tend to have an increased homeostatic need for SWS. A few researchers have taken advantage of this natural alteration
of sleep stages in designing nap studies. Alger et al. (2010) asked subjects to encode neutral scenes and then divided subjects into
conditions that either remained awake or took a 90-min nap immediately, 2 h, or 4 h after learning, followed by a memory test
for the material 7 h after encoding. They hypothesized that memory would either decay the longer that participants were awake before
the nap or that all nap conditions would perform equally. Contrary to expected results, the group with the greatest delay (4 h)
between training and testing demonstrated superior memory, with a linear relationship between time awake before the nap and
performance at retest. Importantly, subjects in the late nap also obtained the greatest amount of SWS, nearly significantly more
than the immediate nap group, reflecting the homeostatic increase in the need for SWS. These findings suggest a critical role for
SWS in processing this information. In another manipulation of sleep composition, Kaestner et al. (2013) examined subjects who
participated in three different conditions involving drug manipulations to enhance or reduce certain aspects of sleep to explore
the impact on memory. The drugs included zolpidem, which enhances sleep spindle density and decreases and/or delays REM sleep,
sodium oxybate, which increases SWS but decreases sleep spindle density, and a placebo. The time of nap was between 9 a.m. and 11
a.m., a time of day when REM sleep is generally fairly prominent. Participants slept in the lab before the experimental
manipulation were awakened around 5 a.m., and then encoded emotional (positive high arousal, positive low arousal, negative high
arousal, and negative low arousal) and neutral picture stimuli at 6 a.m., and were administered a drug (or placebo). They were then
allowed an approximately 90-min nap, which was either high in spindle activity, SWS, or REM sleep based on the drug condition.
This was followed by a retrieval session at around 3 p.m. When comparing the conditions, the high spindle density zolpidem condi-
tion resulted in better recognition of negative and high arousal information, compared to placebo (with naturally more REM sleep).
This suggests that spindles during Stage 2 sleep may play a role in the consolidation of emotional memory, compared to SWS- and
REM-rich sleep (although we will discuss emotional memory in more detail later, see section Sleep and Emotional Memory).
While declarative memory benefits across a variety of sleep manipulations and memory manipulations has been previously well
studied, it is evident that there is not a consensus regarding what stage of sleep benefits what aspect of memory, particularly as many
of these studies are only able to imply a role for a particular stage of sleep through manipulating the composition of the sleep stages
during sleep (e.g., eliminating REM during a nap or using split-night design) or correlation. The focus in the field of sleep and
memory is beginning to shift to understanding how specific sleep features, such as sleep spindles, slow oscillations, and theta rhythm,
beyond the constrains of defined sleep stages, may influence different types of memory, both through observation and manipulating
features of sleep to further promote or inhibit memory. In addition, there are a growing number of studies manipulating the reac-
tivation of memory during sleep that add to our understanding of the sleep and consolidation process. We discuss this literature next.
2.31.5.3 Manipulations of Sleep Physiology and Memory During Sleep

The field of sleep and memory has gained additional momentum with the advent of new technological and pharmacological
advances to manipulate sleep features with the intention of examining the effect on subsequent memory. Along with this research,
several experiments have manipulated the reactivation of memory during sleep to examine the impact on sleep-based consolidation
based on the premise that reactivation leads to strengthening of the memory. Both of these lines of research add to the growing body
of literature assigning an active role for sleep in the consolidation of memory, particularly for declarative memory. Techniques such
as transcranial direct current stimulation (tDCS, also referred to as transcranial slow oscillation stimulation, tSOS) can induce or
impair frontal SOs, auditory stimuli can be introduced to synchronize (promote) or desynchronize (suppress) SWA, and pharma-
cological drugs can be used to promote or suppress physiological features of sleep, such as slow oscillations and sleep spindles.
Below, we consider just a few of these techniques and the findings stemming from their use.
2.31.5.3.1 Manipulation of Sleep Physiology

Marshall et al. (2004, 2006) used tDCS in an attempt to investigate the impact of exogenously inducing SWA on memory consol-
idation processes. In this technique, an alternating electrical current is applied to the scalp over frontal cortical sites using a frequency
that matches the endogenous SO (<1 Hz), resulting in increases of endogenous SOs. They had participants encode a word pair and
a mirror-tracing (procedural) task before sleep, during which participants either received SO-tDCS or underwent a sham condition
during the first period of SWS (Marshall et al., 2006). After SO-tDCS or sham stimulation, participants were awakened at the end of
their first REM sleep cycle and tested after a 10-min delay. Participants underwent both conditions a week apart in a counterbalanced
order. This was contrasted to a control condition receiving either SO-tDCS or a sham condition while awake, with control partic-
ipants also undergoing both conditions a week apart in a counterbalanced order. They report that SO-tDCS increased SWA and that
this increase resulted in improved memory, but only for declarative memory in sleeping participants. In a more recent study,
Marshall et al. (2011) had participants encode paired-associates and procedural memory tasks before sleep, which included
tDCS to induce theta oscillations or sham conditions during the first period SWS (study 1) or during REM (study 2). For both
studies, participants underwent both theta-tDCS and sham conditions in counterbalanced order at least 10 days apart. For study
1, they report that theta-tDCS reduced SWS and EEG power in SOs and increased stage 2 sleep, which coincided with inferior declar-
ative memory the next morning, but had no effect on procedural memory. This is similar to the previously discussed study in which
tDCS affected declarative but not procedural memory. For the REM study, they report that theta-tDCS increased gamma band
activity but had no memory effect. Taken together, these studies suggest a strong link between SWS and declarative memory,
with increased SWA resulting in better memory and reduced SWA resulting in poorer memory.
Using another technique to manipulate sleep physiology, Ngo et al. (2013) used auditory stimulation in the form of two
different auditory stimuli (50 ms and pink noise) during sleep, compared to sham stimulation, to increase SWA and examine
the impact on declarative memory. They asked participants to encode paired associates, followed by an immediate cued recall
test. Then, participants were exposed to the auditory stimulation induced after detection of slow oscillatory activity, or a sham
condition, followed by a cued recall test in the morning. Participants underwent both conditions in counterbalanced order at least
a week apart. The auditory stimuli were delivered concurrently with the up phases of the SOs and formed what they deemed
“SO trains,” suggesting that the brain responded to this stimulation by resonating the induced activity. In addition to this,
phase-locked fast spindle activity was increased with stimulation. They report the acoustic stimulation condition resulted in a higher
retention rate for the paired associates relative to the sham condition, and that this memory was correlated with SWS, suggesting
that stimulation of SOs entrained the slow-wave rhythms during SWS and that this facilitated memory. Using a different memory
paradigm, Ong et al. (2016) had participants undergo a baseline nap to determine the appropriate sound level for acoustic stim-
ulation. Following the baseline nap, participants encoded semantically related word pairs before a baseline memory test and under-
went both an acoustically stimulated nap and a sham nap in counterbalanced order and on different days, followed by a cued-recall
task 45 min after waking. They report that acoustic stimulation increased SWA and reduced forgetting relative to the sham
condition.
Interestingly, this type of acoustic manipulation has also been used to support a causal role of slow waves (virtually absent from
REM sleep) in the consolidation of procedural memories (Landsness et al., 2009). Participants were trained on a rotation-
adaptation task in which they had to learn to reach for targets on a visual display while the cursor trajectory, unbeknownst to
them, was rotated by the program. During the night postencoding, the authors used acoustic stimulation to successfully suppress
slow waves during NREM sleep without waking participants. In a within-subject design, participants received slow-wave suppres-
sion on one night and control acoustic stimulation on another night (i.e., stimulation during NREM sleep but when there were no
slow waves present in the EEG). Similar to the studies discussed earlier, the control stimulation condition led to an increase in
performance when memory was tested the following morning. In contrast, acoustic stimulation that suppressed slow waves
impaired memory. Number of slow waves, as well as SWA, was positively correlated with the performance.
Finally, pharmacological interventions can be used to alter sleep composition to investigate the effect on memory. Similar to the
study by Kaestner et al. (2013) discussed earlier (see section Daytime Napping Benefits Memory), Mednick et al. (2013) used three
drug conditions to alter the composition of sleep achieved in an early morning nap. They had participants encode word pairs after
awakening them early in the morning, with an immediate recall test of performance. Following encoding and baseline testing,
participants were administered zolpidem, which increases sleep spindle density while decreasing or delaying REM sleep, sodium
oxybate, which increases SWS but decreases spindles, or a placebo. They then allowed participants to nap for 90 min, followed later
in the day by a recall test. All participants underwent each study condition, at least 5 days apart in counterbalanced order. Zolpidem
increased spindle activity and improved memory, while sodium oxybate, which did not increase spindles, did not improve memory,
assigning an active role for sleep spindles in memory consolidation.
2.31.5.3.2 Reactivation of Memory During Sleep

Clearly, there is a link between the physiological manipulations of sleep and altered memory that further argues against the idea that
memory is only passively aided by sleep. In addition to manipulating sleep physiology to influence memory, recent studies have
attempted to manipulate memory reactivation during sleep. This targeted memory reactivation uses external stimuli during sleep,
such as odor or sound, to promote memory (for review, see Oudiette and Paller, 2013).
In a groundbreaking study by Rasch et al. (2007), participants encoded object–location pairs and a procedural finger-tapping
task in the presence of an olfactory stimuli (odor of a rose). During subsequent sleep, the same odor was introduced time locked
to SWS. In a control condition, just the vehicle was presented during sleep, without the rose odor. After sleep, memory was tested in
the absence of the odor. They reported that those who received the odor during sleep demonstrated better declarative memory as
a result of cued reactivation of the memory trace, compared to the control condition. A control experiment addressed the idea that
perhaps the rose odor alone during sleep promoted memory consolidation, regardless of whether it had been contextually paired
with the learned material during wake. In this case, the odor alone during sleep was found to have no effect on memory. In a third
and fourth control experiment, the authors tested whether the exposure of the rose odor, having first been contextually paired with
the learned material, would be affective as a reactivation cue during REM sleep or during subsequent wake. Of all these experiments,
the reexposure of the odor was only found to benefit memory when it was introduced during SWS. This suggests that these cues help
SWS to facilitate memory consolidation through reactivation and communication between the hippocampus and neocortex. Rihm
et al. (2014) performed a similar study in which participants encoded object–location pairs with an odor cue. During subsequent
nocturnal sleep, participants were exposed to the same odor, a different odor, or an odorless vehicle during SWS. They reported
improved memory for the pairs, but only when reexposed to the same odor. This effect was accompanied with increased frontal
delta frequency oscillations relative to the different odor (but no odor) and an increase in parietal sleep spindles relative to
both different odor and no odor, demonstrating the increase in consolidation processes resulting from this reactivation via odor
reexposure.
Auditory stimuli can also be used to pair with and reactivate learned information during sleep. Rudoy et al. (2009) utilized a similar
memory paradigm as Rasch and et al. (object–location pairs), but had participants encode object–location pairs in the presence of
a distinctive sound for each pair. Following initial baseline testing, participants either napped for at least 60 min or remained awake.
Napping participants were presented with the auditory cues for half of the stimuli during SWS sleep. In a control experiment, partic-
ipants underwent another cognitive task while hearing a similar mix of auditory cues while remaining awake. They report that within
the nap experiment, pairs that had been reactivated with an auditory cue during sleep had less memory decay compared to stimuli that
were not reactivated during sleep. Further, they demonstrate that memory trials with better accuracy evoked larger amplitude EEG
responses to the sound cues during sleep, demonstrating both a behavioral and physiological effect of auditory stimulation. Within
the control experiment, auditory reactivation during wake had no effect on memory. Creery et al. (2015) repeated this study using
45 min delay between encoding and initial testing to remove working memory confounds. They report that auditory cueing during
sleep reduced forgetting between pre- and postnap assessments, relative to uncued stimuli, but only for those who had performed well
during initial testing. Looking more deeply, the authors suggest that auditory cueing only benefitted relatively strongly learned object–
location pairs, but did not benefit the very weak or very strongly learned pairs. Acoustic stimulation has also been examined using
emotional stimuli. Cairney et al. (2014) had participants encode negative and neutral picture–location pairings in the presence of
semantically related sounds (e.g., a picture of bomb explosion paired with the sound of an explosion). After encoding, participants
underwent a prenap memory test that presented the pictures and associated sounds and asked participants to indicate the location
of the picture as well as their confidence. This was followed by a 90-min nap opportunity, during which half of the encoded sounds
were replayed during SWS (counterbalanced between participants). Following sleep, participants completed a final memory test. They
report similar memory accuracy effects in high confidence answers for cued and uncued stimuli for both negative and neutral cate-
gories. However, reaction times in high confidence responses for negative stimuli were faster relative to neutral stimuli when they
were cued during sleep compared uncued stimuli. Further, spindle count predicted the decreased reaction time for negative stimuli
relative to neutral stimuli for cued, but not for uncued stimuli.
Based on the presented evidence, it is clear that the sleeping brain can actively modulate memory. However, while some infor-
mation is stored and integrated into memory systems during sleep, not all memories benefit from sleep, nor are all memories
preserved. Most information that undergoes enough processing to be stored in long-term memory is expected to have value in
informing decisions or behavior. Indeed, some scientists have proposed that memory is optimally designed to imagine the future,
rather than remember the past (Schacter et al., 2007). If this is true, then the brain must use some criteria or indicators to determine
what information could be useful in the future as it is encoding and consolidating, and what information can be discarded. In the
next section, we discuss one such cue that serves to tag information as important to remember.
2.31.5.4 Sleep and Emotional Memory

Emotion generally helps prioritize memory, possibly due to the biologically relevant nature of emotional content that can be adaptive
to survival (e.g., fearing a snake can minimize behaviors that would lead to a poisonous snake bite). In general, emotionally salient
stimuli have been shown to be better remembered relative to neutral stimuli (e.g., Bradley et al., 1992; Cahill and McGaugh, 1998; see
for review Kensinger, 2009). Emotion can be defined in terms of valence, or how positive or negative the stimuli is deemed, and
arousal, or how agitated or excited the stimuli makes you feel (Kensinger, 2004). Most studies of emotional memory in the laboratory
utilize artificial stimuli, such as words and images, due to the practical and ethical difficulties of generating naturalistic emotional
experiences (e.g., simulating a robbery). To this end, image databases such as the International Affective Picture System (IAPS;
Lang et al., 1997, 2008) and Nencki Affective Picture System (NAPS) (Marchewka et al., 2014) are used, which contain a catalog of
pictures that cover the spectrum of valence and arousal, from negative to positive, as well as low and high arousal images, and has
been used in numerous studies to date.
Emotional memories, which often contain more complexity than nonemotional memories, recruit the amygdala and regions of
prefrontal cortex that modulate amygdalar activity in addition to the important memory structures of the MTL. Neural connectivity
evidence and fMRI studies suggest that the amygdala imparts emotional memory benefits through direct and indirect modulation of
the hippocampus (Cahill et al., 1996; Dolcos et al., 2005; Labar and Phelps, 1998; for review see Petrovich et al., 2001; McGaugh,
2004; Phelps, 2006). Sleep, especially REM sleep, has been associated with better preservation and, even in some cases, enhance-
ment of emotional memory relative to similar delays including wake (e.g., Hu, et al., 2006; Payne et al., 2008, 2012b; for review see
van Der Helm and Walker, 2009; Payne and Kensinger, 2010). For example, Hu et al. (2006) had participants encode emotional and
neutral IAPS stimuli followed by a memory test, which asked for “remember/know” judgments after a 12-h delay including over-
night sleep or daytime wakefulness. Participants underwent both conditions in a counterbalanced order at least a week apart. They
report that participants who slept had better memory accuracy for arousing stimuli in the “know” category.
While sleep, overall, has been found to benefit emotional over neutral memory, some studies demonstrate emotional memory
effects that correlate with measures of specific sleep stages. REM sleep, and features of REM sleep including oscillation on the theta
frequency range in particular, has been associated with emotional memory consolidation. As emotional memory effects are sup-
ported by neural connectivity of the amygdala and the hippocampus, REM sleep appears to strengthen this connectivity, possibly
supporting emotional memory consolidation (Genzel et al., 2015; Nishida et al., 2009; Payne et al., 2012b; Wagner et al., 2001).
While initial studies examined this hypothesis using REM sleep deprivation, in which participants were woken when PSG indi-
cated REM sleep, it was unclear whether memory effects where due to less REM sleep or the effects of stress and sleep deprivation
(Horne and McGrath, 1984). The split-night early/late sleep design discussed earlier was also used by Wagner et al. (2001) to
examine the effects of sleep features on memory for emotional and neutral texts. After initial encoding and testing of texts,
they report that participants who slept later in the REM-rich part of the night had higher retention of emotional relative to neutral
encoded texts compared to the earlier SWS-rich sleep condition. The late sleep group also had significantly higher retention for
emotional texts when compared to a late wake group (i.e., late sleep deprivation). When memory was reassessed 4 years later
(Wagner et al., 2006), all participants who slept, regardless of early versus late placement, had better memory compared to
wake for emotional texts, while memory for neutral texts was similar between wake and sleep groups. The authors suggested
that for the early SWS-rich sleep condition, the sleep they obtained when going back to sleep after the initial assessment was
REM-rich, and this aided in encoding for long-term memory, mirroring the sleep patterns for the late sleep condition. Groch
et al. (2013) also utilized a split-night design to examine negative and neutral IAPS pictures, rather than texts. They report better
memory for negative pictures relative to neutral pictures in the late, REM-rich sleep condition, while the early, SWS-rich condition
had similar retention for negative and neutral stimuli. Further, emotional memory correlated with percentage of time spent in
REM sleep. They also explored event-related potentials (ERPs) during encoding and retrieval, with a special interest in the frontal
late positive potential around 300–500 ms after stimulus presentation, which is associated with recognition accuracy (Rugg et al.,
1998). ERP responses over frontal areas to correctly recognized previously encoded negative pictures referenced to new negative
pictures that were correctly rejected were significantly increased in the late, REM-rich sleep condition, while this was not the case in
the early sleep condition. The increased late positive potential could mirror REM sleep theta activity and coordination between the
amygdala and other memory brain structures (Popa et al., 2010).
While sleep effects on emotional memory have been most commonly associated with REM sleep, there is also evidence that
suggests NREM sleep supports emotional memory formation. In a 2011 study by Groch et al., participants encoded neutral and
emotional texts and IAPS images and rated them on measures of valence and arousal before sleeping in the SWS-rich early part
of the night. During sleep, participants were administered clonidine, an NE suppressant, or a placebo, and each participant under-
went both drug administration conditions. Clonidine administration had relatively little effect on sleep architecture, but under
clonidine participants were less able to remember temporal aspects of the emotional story, rendering memory performance for
the emotional text similar to the neutral text. In the placebo condition, however, memory for the emotional story was better
than memory for the neutral text. Additionally, ratings for both emotional and neutral images changed from encoding to retest;
for the placebo condition, emotional stimuli were rated less negative, and both neutral and negative stimuli were rated as less
arousing, while in the drug condition both emotional and neutral stimuli were rated as less negative, but there was no significant
effect on ratings of arousal. This suggests that NE during SWS-rich sleep may play a role in distinguishing between emotional and
neutral consolidation.
2.31.5.4.1 Selective Consolidation of Complex Emotional Memories

While sleep has been shown to improve emotional memory, it has also been shown to selectively promote memory for emotional
elements over neutral elements within complex stimuli (Cunningham et al., 2014a; Payne et al., 2012b; Payne et al., 2008). One task
used to study this subtle phenomenon is the emotional memory trade-off task (Kensinger et al., 2007), which consists of participants
incidentally encoding negative or neutral objects (e.g., a chipmunk or a snake) interposed on a plausible background (e.g., a forest,
see Fig. 4). At retrieval, participants are presented objects and backgrounds separately and intermixed with new objects and back-
grounds that serve as foils. The typically reported effect is that emotional objects are correctly recognized more often than neutral
objects, but backgrounds paired with negative objects at encoding are recognized with less accuracy than backgrounds paired with
neutral objects at encoding, creating a memory trade-off. Although this effect occurs after a short delay (Kensinger et al., 2007; Payne
et al., 2008), the magnitude of the trade-off effect (the difference between memory for the emotional object and the background) is
magnified after a night of sleep relative to a day of wakefulness (Payne et al., 2008). Memory for emotional objects has been positively
correlated with total time spent in nocturnal REM sleep, as well as percentage of a night’s sleep spent in REM (Payne et al., 2012b).
When looking at a 24-h design, participants who viewed emotional memory trade-off stimuli with sleep occurring soon after encod-
ing demonstrated an increase in the emotional trade-off relative to the wake-first group (Payne et al., 2012b). These findings provide
evidence that sleep-based consolidation benefits are optimized when sleep follows learning in short order, rather than after a longer
delay, and further cannot be entirely explained by interference effects, as both sleep-first and sleep-second groups spent similar
amounts of time (16 h) awake between encoding and retrieval exposed to interference (Wixted, 2004; Mednick et al., 2011).
The sleep-based emotional memory trade-off effects have been further examined using fMRI to determine neural activity underlying
the effect. Payne and Kensinger (2011) compared neural activity for successfully recognized emotional stimuli across sleep and wake
groups and found that the wake group used a diffuse network including lateral prefrontal, parietal, and medial temporal brain regions
to retrieve the emotional objects, while those who slept evinced a more refined, consolidated network consisting of the amygdala,
Figure 4 Examples of the emotional memory trade-off scenes presented to subjects. Images were created by placing either a negative or neutral
central element (e.g., the cars or car accidents) on plausible neutral backgrounds. Memory for the individual scene components are later tested sepa-
rately. From Payne, J.D., Stickgold, R., Swanberg, K., Kensinger, E.A., 2008. Sleep preferentially enhances memory for emotional components of
scenes. Psychol. Sci. 19, 781–788.
vmPFC, and cingulate gyrus. Also, the sleep group, relative to the wake group, had stronger connectivity between the critical memory
networks of the hippocampus, vmPFC, and amygdala for emotional stimuli.
While it is clear that the sleeping brain preferentially processes emotional content, the question of how it mechanistically triggers
such processing remains unknown. The concept of “emotional tagging” (Richter-Levin and Akirav, 2003) suggests that the encoding
of arousing material activates neural mechanisms, likely involving the amygdala and other key memory regions, resulting in long-
term plasticity in those synapses marked by the tag (Morris, 2006). Payne et al. have recently suggested that, working in concert with
the arousal generated by the emotional stimuli themselves, elevations in arousal-related neuromodulators, including NE and
cortisol, might help set tags at a synaptic level at the time of encoding. Then, provided sleep occurs shortly after encoding. Processes
that are unique to sleep operate to selectively stabilize and consolidate those tagged representations. The idea is that the uniquely
high-frequency oscillations that are associated with sleep (e.g., sleep spindles, theta rhythm, hippocampal sharp wave–ripple
complexes, etc.) help stabilize this information for preferential processing in a manner that leads to long-lasting plastic changes
in the brain (see Bennion et al., 2015; Cunningham et al., 2014a).
For instance, Cunningham et al. (2014a) monitored participant’s heart rate deceleration (HRD) and skin conductance response
(SCR) during encoding and testing of emotional memory trade-off images. They report correlations between greater HRD and SCR
reactivity to negative scenes at encoding and enhanced memory for the negative objects at recognition, but only after a period of sleep.
This finding suggests that physiological responses that occur in response to the viewing of negative stimuli may help set selective tags
for this information at the time of encoding, possibly through neurochemicals such as NE and/or cortisol and that these tags are then
solidified during subsequent sleep. Using different physiological metrics, Bennion et al. (2013) monitored resting cortisol levels and
attention via eye tracking during encoding of emotional memory trade-off images and found that correct recognition of emotional
stimuli at testing correlated with higher resting cortisol levels at encoding, but again, only after a period of sleep. Additionally, Benn-
ion et al. (2013) used fMRI scanning during recognition and reported that, after sleep, correctly recognized emotional items demon-
strated refined neural networks in the amygdala and vmPFC that were influenced by cortisol’s effect on attention at encoding. Taken
together, these findings suggest that the cortisol and other stress and arousal-related neuromodulators present during encoding may
help selectively tag important elements of stimuli, typically the emotional foci of the scenes that were attended to, and that subse-
quent sleep-based consolidation processes stabilize these tagged elements, which in turn results in better memory during recognition.
In section Sleep Aids Memory Transformation: Generalization, Integration, and Reorganization we will discuss other ways in which
particular information is prioritized over other information during sleep.
So far, we have discussed the benefits of a period of sleep compared to a period of normal wakefulness on memory performance.
We will next examine how the lack of sleep impairs the normal processes of memory consolidation that takes place in a healthy, well-
rested state. Continued waking activity reduces the potential for future learning to take place and reduces available neural resources,
and many students, such as our student asleep on her textbook, have likely found it difficult to learn or consolidate information
during extended periods of wakefulness.
2.31.6 Sleep Deprivation Impairs Memory
Good sleep is something that a large number of individuals do not achieve on a daily basis. According to the National Sleep Foun-
dation, close to 50% of people (aged 25–55 years) from five different countries do not sleep the recommended number of hours they
need on workdays. Lack of sleep is common in modern society and can lead to errors in safety-critical workplaces, such as in health
care (e.g., Dorrian et al., 2008). The brains of sleep-deprived young adults have been shown to function like those of 60-year-old
individuals in a variety of cognitive tests (Harrison et al., 2000). Inadequate sleep is characterized by decreased alertness and cognitive
ability, which lead to performance impairments in speech, reasoning, decision-making, judgment, and of relevance to this chapter,
memory (Thomas et al., 2000). While the previous sections have discussed how either an overnight period of sleep or daytime nap
benefits declarative memory, it is also essential to review how lack of sleep hinders memory. Both animal and human studies have
shown the impairment of newly learned information by partial or total sleep deprivation, leading to a subsequent decline in memory
performance compared to control groups (Peigneux et al., 2001; Gais et al., 2006; Ferrara et al., 2006). We discuss current work exam-
ining the impact of sleep deprivation on memory.
2.31.6.1 Recent Work on Sleep Deprivation

The turn of the century was accompanied by an increase in interest in the relationship between sleep and memory. The previous
sections of this chapter have discussed how a full night of sleep, as well as daytime naps, typically benefits various types of memory.
The following sections will discuss the more recent studies that have employed nighttime wakefulness (i.e., sleep deprivation) to
assess the sleep and memory relationship.
Sleep deprivation studies of declarative memory vary largely in the type of stimuli used including spatial tasks (e.g., Ferrara
et al., 2006; Orban et al., 2006), paired associates (e.g., Gais et al., 2006), emotionally negative and neutral content (e.g., Sterpenich
et al., 2007; Atienza and Cantero, 2008; Sterpenich et al., 2009), gist-based false memories (Diekelmann et al., 2008; Darsaud et al.,
2011; Frenda et al., 2014), and prospective memory tasks (e.g., Diekelmann et al., 2013; Grundgeiger et al., 2013; Esposito et al.,
2015).
In a study looking at how sleep deprivation affects spatial memory, participants were asked to navigate a novel neighborhood by
following an experimenter (Ferrara et al., 2006). Memory was tested shortly after in the laboratory by asking participants whether
a three-picture sequence represented the correct order of route landmarks that had been experienced as the participants walked by
them. Participants were then retested after a normal night of sleep, a night of sleep deprivation, or a similar 8-h period of daytime
wakefulness. The regular sleep group was the only group who showed a significant improvement at memory retest. Memory in the
daytime wake group was virtually identical across the retention interval, whereas in the sleep deprivation group performance signif-
icantly declined. Although time-of-day factors may have affected these findings, the fact that performance was maintained in the
daytime wake group and increased in the sleep group supports the view that consolidation-based enhancements are dependent
on sleep.
In the paired-associate domain, Gais et al. (2006) had participants encode pairs of English and German words. Memory for the
pairs was tested immediately after encoding and again 48 h later after participants had either been sleep deprived during the first
night postencoding or were allowed to sleep regularly. Of note, participants were allowed to sleep during the day after the night of
sleep deprivation, which means that the sleep deprivation group and the regular sleep group slept and remained awake across 48 h
in similar amounts (the sleep deprivation group slept an average of 13.2 h, whereas the sleep group slept an average of 14.9 h before
retest; see Fig. 5). Compared to the regular sleep condition, participants in the sleep deprivation condition had worse memory for
the word pairs, suggesting that sleep deprivation on the first night after learning leads to deterioration in declarative memory relative
to a normal night’s sleep, even if participants are allowed similar amounts of sleep prior to testing. These findings support the idea of
a sensitive time window in which postlearning sleep must occur to aid consolidation processes. This is also supported by rodent
studies, in which this critical time period coincides with sensitive periods of molecular signaling, protein synthesis, and mRNA
synthesis required for memory consolidation (Bourtchouladze et al., 1998; Igaz et al., 2002; Trifilieff et al., 2006).
While sleep seems to benefit emotional memory (see section Sleep and Emotional Memory), it appears that sleep deprivation
impairs memory consolidation for neutral and positive memory more than negative memory (Sterpenich et al., 2007). In one study,
participants encoded pictures of different emotional valence: positive, negative, and neutral. Participants were either allowed to
sleep normally or were sleep deprived during the first postencoding night, but then allowed to sleep the following two nights.
Memory was tested 72 h after encoding inside an fMRI scanner (imaging findings discussed in section Functional Imaging and Sleep
Deprivation). Compared to the regular sleep group, memory for positive and neutral material was impaired in the sleep deprivation
group. Interestingly, however, recollection for negative pictures was not found to be different between the groups. Similar findings
were reported by Atienza and Cantero (2008). In this study, memory for emotional pictures was less attenuated than memory for
neutral pictures after 40 h of sleep deprivation compared to regular sleep.
Diekelmann et al. (2013) had participants encode a task that included an event-based prospective memory component (i.e.,
participants are instructed to press a specific key when they see a particular stimulus as part of another ongoing task) and then
they were allowed to sleep or were sleep deprived. Memory was tested 2 days later, following a night of recovery sleep for the sleep
deprivation group, to rule out nonspecific effects of fatigue after acute sleep deprivation. Those who were sleep deprived postencod-
ing (targeting consolidation) were less likely to comply with the instruction given 2 days before, i.e., prospective memory was
impaired. Some may argue that participants in the sleep deprivation group were exposed to more interference during the retention
interval, which could have disrupted the intentional memory. In this case, sleep had a simple, passive role in the formation of
prospective memory. This explanation seems unlikely, as the authors showed, using the split-night procedure in another
experiment that those who slept during the first half of the night (SWS-rich sleep) had better prospective memory than those
who slept during the second half of the night (REM-rich sleep). These two experiments suggest an active role of sleep, particularly
SWS, in the consolidation of prospective memories.
2.31.6.1.1 Functional Imaging and Sleep Deprivation

Studies that include neuroimaging methodologies are particularly relevant to inform us of the large-scale neural deficits and
compensatory mechanisms that sleep deprivation can cause for memory formation processes. For example, Drummond et al.
(2000) deprived participants of sleep for 35 h and then tested their performance in a simple declarative task (i.e., learning a list
Figure 5 Experimental protocol from a 2006 study by Gais et al. This figure illustrates the timing of the sleep or sleep deprivation period on the
first night following learning (LR). The sleep deprivation group (SD) is allowed to obtain recovery sleep during the daytime, followed by another night
of sleep before retesting on day 3.
of nouns) inside the scanner. Sleep-deprived participants showed increased activation in the prefrontal cortex and parietal lobe,
whereas participants in the sleep group had less prefrontal activity and temporal lobe activity. Activation of the parietal lobe in
sleep-deprived participants was positively correlated with performance, suggesting that the brain, under the pressure of sleep depri-
vation compensated for a lack of temporal activation with higher activation in prefrontal and parietal areas (Drummond et al.,
2000). When word difficulty was manipulated, increased activation was found in prefrontal and parietal regions in response to
hard, but not easy words (Drummond et al., 2005).
Sleep deprivation also changes the brain networks utilized to retrieve emotional information. In the Sterpenich et al. (2007) study
discussed earlier, participants who were sleep deprived the first night postencoding had higher activation in the amygdala, while those
who obtained regular sleep recruited the hippocampus and medial prefrontal cortex more extensively. This suggests that even when
both groups performed similarly on memory tests, the sleep group underwent stronger memory consolidation and relied on a more
permanent memory network. Interestingly, when participants were retested 6 months later (Sterpenich et al., 2009), although there
were no behavioral sleep benefits, those who slept demonstrated a shift in emotional memory network activation to the amygdala,
frontal cortical areas including the ventromedial PFC, and the middle occipital cortex, while sleep-deprived subjects only recruited
ventral medial prefrontal cortex. This again suggests shallower encoding/consolidation for participants who were sleep deprived.
In another example of alternate brain networks at work in sleep-deprived subjects, Yoo et al. (2007) conducted a study in
which one group of participants obtained a normal night of sleep on the first night of the study while a second group was totally
sleep deprived, amassing a total of 35 h of sleep deprivation. Both groups viewed pictures while being scanned using fMRI on day
2 and were then subsequently tested using a remember/know recognition test on day 4, allowing the deprived group recovery
sleep before testing. Not only did the sleep-deprived participants perform more poorly, fMRI analyses revealed decreased bilat-
eral posterior hippocampal activation in the deprived group, while the control group had significantly stronger coupling between
bilateral hippocampus in the posterior cingulate with regions of the MTL and the inferior parietal lobule. Moreover, the sleep-
deprived group had significantly higher hippocampal connectivity with the brainstem and thalamus. The authors concluded that
this connectivity reflected functional episodic memory processing in the control group while the sleep-deprived group showed
activation correlating with basic alertness. Functional brain activity has also been investigated in the formation of gist-based false
memories after sleep deprivation (Darsaud et al., 2011). Gist-based false memories are commonly studied with the Deese–Roe-
diger–McDermott (DRM) task, in which participants encode lists of semantically related word lists (hospital, medicine, nurse,
etc.) and later, when asked to retrieve the words, they remember the study words (“nurse”), but also remember the theme, or
gist, of the list (in this case, “doctor,” a word not presented) with high probability and confidence (Roediger and McDermott,
1995; Gallo, 2010). Similar to the findings of Drummond et al. discussed earlier, participants who were sleep deprived the night
after encoding of DRM word lists relied on a broader, more distributed cortical network during recognition testing. These results
suggest that sleep deprivation shifts the brain to more effortful strategies to retrieve information to compensate for the effects of
sleep deprivation.
So far, we have predominantly highlighted evidence of how sleep, or sleep deprivation, affects previously encoded memory, i.e.,
during consolidation. However, as suggested by the synaptic homeostasis theory, sleep the night before may prime the brain to be
more likely to encode new information. To this point, we have thus far presented how crucial sleep is for memories after they have
been acquired. The next section will discuss the importance of obtaining enough sleep before encoding to begin with.
2.31.7 Sleep Prior to Encoding Primes for New Learning
As discussed in the previous sections, much of the literature regarding sleep and memory deals with the consolidation phase of
memory formation, but there is evidence to demonstrate that sleeping prior to encoding prepares the brain for the act of learning
new information. As we touched on in the last section, many of these studies examine how sleep deprivation, compared to normal
sleep, prior to performing a task impedes the ability to successfully encode information. With even one night of sleep deprivation,
the functioning of the prefrontal cortex, vital for effective memory encoding, is compromised, as measured by reductions in cerebral
metabolic rate (Brewer et al., 1998; Wagner et al., 1998), as well as higher activation when overcompensating for reduced activation
in the MTL (Drummond et al., 2000). However, it is difficult to tease apart whether encoding is impaired due to fatigue effects
compared to how healthy sleep may prepare the brain to take on new information through other mechanisms.
One way to address how sleep prior to encoding primes the brain for learning is by using a nap protocol, which eliminates the
potential confound of fatigue from sleep deprivation. In one such study, Mander et al. (2011) set out to test whether the capacity to
learn new episodic information remains the same across the day. To do so, they had two groups of participants encode and associate
two sets of face–name pairs, the first set encoded at noon and the second at 6 p.m. Between the learning sessions, one group was given
a 100-min nap opportunity while the other remained awake. Encoding ability was assessed immediately after learning each of the
face–name pair sets, with a recognition test of memory for the faces and the appropriate name pairs indicating how well participants
acquired the information. Results indicated that the ability to learn new episodic information declined between the noon and 6 p.m.
sessions in the no-nap condition, while those that napped demonstrated a numerical increase in encoding ability. Encoding ability
postnap as well as the difference in encoding ability between sessions was found to positively correlate with Stage 2 sleep and fast
sleep spindles. Furthermore, a source current–density analysis locked to the fast spindle onset revealed looping activity throughout
the left temporal lobe and the superior parietal and occipital cortices. The authors concluded that their findings were consistent with
the idea of hippocampal–neocortical communication, with systems consolidation allowing the memories to become more depen-
dent on the neocortex, thus freeing up the hippocampus for new learning during the second session.
Not only has sleep prior to encoding been found to benefit new learning, but more recent research has begun to examine if the
quality and composition of that sleep plays a role in preparing the brain for receiving new information. It may be that deep sleep
is what is necessary. In a 2009 study by Van Der Werf et al., it was hypothesized that deep sleep, or SWS, which has been theorized
to be the key stage of sleep for both systems consolidation and synaptic downscaling, may be what is important for effective subse-
quent encoding. To test this, they used mild acoustic sleep-perturbation, which resulted in reduced SWA and increased higher
frequency, shallower sleep. Using elderly individuals as their own controls in shallow and normal sleep conditions, they had partic-
ipants subsequently encode images of houses and landscapes while undergoing fMRI. The following day, memory for these images was
tested using a recognition test. Following shallow sleep, performance was significantly lower than after normal sleep, and there was
decreased activation in the anterior part of the right hippocampal formation during encoding of items that were later remembered.
This reduced activation was found to specifically impair declarative information processing, as no group differences were found
when assessing performance on a nonhippocampal dependent implicit learning task. These findings indicate that deep sleep prior
to learning declarative information results in local synaptic changes in the hippocampus, with the up- and down-states of SWA modu-
lating the hippocampal firing rate, allowing for optimal hippocampal activity in subsequent learning episodes.
In another experiment probing the idea that deep sleep is essential for successful subsequent encoding, Antonenko et al. (2013)
used tSOS (same as tDCS described earlier) to enhance the amount of SWA during a nap prior to learning, compared to allowing
normal sleep. Participants, serving as their own controls, obtained two naps in the lab, separated by approximately 4 weeks. In
one condition, participants napped around 3 p.m. during which tSOS was applied in NREM sleep to increase SWA. This was followed
by an encoding session in which three declarative tasks (picture learning, word pairs, word lists) and one procedural task (finger
tapping) were learned, with testing occurring after a short retention interval. The other condition was identical except for the use
of sham stimulation during the nap. After tSOS, performance for all declarative tasks was superior to that after a normal nap, while
procedural memory was unaffected by the stimulation. The authors were also able to examine the impact of stimulation on internally
generated spindle activity, which was found to be phase locked to the up-states of the induced SOs, mimicking what is normally seen
under physiologically normal conditions. Similar to Van Der Werf et al. (2009), the authors conclude that deep sleep prior to learning
is vital for effective encoding, most likely through both systems consolidation and active synaptic downscaling that serves to reset the
networks to baseline potentials, which in turn allows new information to be learned.
2.31.8 Sleep Aids Memory Transformation: Generalization, Integration, and Reorganization
Much of what we have discussed thus far reflects the advantage sleep confers to veridical information, examining memories insofar as
they match exactly what was encoded. However, as we touched on when discussing emotional memories, particularly for the specific
memory enhancement for the emotional components of complex memories, it becomes apparent that we do not simply remember
everything we experience in a straightforward fashion. The role of sleep in memory and learning processes goes beyond supporting
memory consolidation. It seems to support memory generalization, reorganization, and integration of new information into already-
existing knowledge networks (see Stickgold and Walker, 2013). Through history there have been many occurrences where “sleeping
on an issue” resulted in inventive solutions, such as the chemical structure of benzene or have the perfect organization of the periodic
table of elements (Stickgold and Walker, 2004). Sleep has been found to preferentially preserve that which is most important and
beneficial for us to remember, either because of its salient nature or because we can predict that we will need specific pieces of infor-
mation in the future. There is also evidence that sleep aides in the types of memory transformations that lead to integration of new
information into existing memory stores, extraction of the gist of an experience, inferential and creative connections between dispa-
rate ideas, and a gain of insight into hidden rules. Later, we discuss this research.
2.31.8.1 Preferential Consolidation of Prospective Information

Prospective memory, which involves knowledge that will be beneficial for future use, has been shown to be preferentially consol-
idated with a period of sleep, compared to less useful information. For example, Wilhelm et al. (2011) examined the impact of
retrieval expectancy, the knowledge that you will be tested on particular material at a later time, on sleep-based memory consoli-
dation. In their first study, participants encoded word pairs either in the morning or in the evening. Half of the participants were
explicitly informed that they would be tested on their memory for these associates after a 9-h retention period while the other half
were not. Participants in the uninformed condition who indicated that they had suspected they would be tested were excluded.
Within the informed and uninformed conditions, participants were divided into those who had a normal night sleep, those
who were awake during the day, and those who were awake overnight (i.e., sleep deprived). The second study involved only the
sleep condition and included a nonverbal, declarative object location task, and a procedural task of finger tapping. In the first study,
subjects who expected to be tested and slept normally performed better than all other conditions, including participants who slept
but did not expect to be tested. These particular sleep subjects showed significantly more SWS and SO activity during the night than
those who slept but did not expect the test, suggesting that deep sleep contributed to the selective retention of the word pairs. Study
2 found that sleep benefitted both memory for object locations as well as gains in finger-tapping skills when testing was expected
compared to when it was not. The authors also included a second test 30 min after the first test that was unexpected for both of the
original conditions. This test aimed to address concerns that the performance benefits in the group that expected to be tested were
not merely retrieval effects, but rather that expectancy boosted consolidation during sleep. This consolidation effect was confirmed
as the group that originally expected to be tested also performed better on this second, unexpected test. SWS, SO frequency activity,
and sleep spindles were all found to be increased in the sleep of those who had expected to be tested compared to those who did
not, and all of these measures correlated positively with declarative memory performance in those who expected the test.
In an extension of the idea of sleep-based preferential consolidation of prospective information, Cunningham et al. (2014b)
used the emotional memory trade-off task described in section Selective Consolidation of Complex Emotional Memories in
a prospective memory experiment. After learning the complex emotional and neutral scenes, half of the participants were told to
expect to be tested on the material after a retention period of 12 h, while the other half did not expect a test. Within each condition,
half slept overnight while the others experienced daytime wakefulness. Interestingly, those who expected the test and remained
awake across the retention period demonstrated a threefold increase in the magnitude of the trade-off between memory for negative
objects and their backgrounds compared to those who did not know they would be tested. However, no such difference was found
in the sleep condition. The authors concluded that emotionally negative salience was sufficient for the information to be preferen-
tially consolidated during sleep, regardless of whether the test was expected or not. This enhanced processing, however, does not
occur in the waking brain. Thus, expectation cues are necessary to generate additional processing, rescuing emotional memory
performance across wake.
Another example of preferential consolidation occurring for information that is expected to be used in the future comes from
Van Dongen et al. (2012). In this study, participants encoded two sets of picture location associations followed by baseline testing
to ensure equal encoding. Participants were then instructed that they would only be required to remember one set for a future test
following a 14-h delay. Over this retention period, half the participants slept overnight while the other half remained awake during
the day. Unexpectedly, memory for both sets was assessed during the test. Those who had slept demonstrated improved memory
retention for the associations they were told to remember over the set they thought they could forget. This retention of relevant
associations in the sleep condition was positively correlated with the total time spent asleep.
Finally, selective consolidation during sleep has been observed when examining item memory in a directed forgetting paradigm.
Saletin et al. (2011) had participants encode lists of words, giving an explicit direction of “R” to remember or “F” to forget after every
visually presented word. A baseline test showed “remember” words were better remembered than “forget” words, with performance
similar between participants. However, a nap opportunity of 100 min for half the participants during a subsequent retention period
led to significant selective enhancement of the “remember” items, compared to the wake group, but not for the “forget” items. This
effect was found to be correlated positively with fast sleep spindle, particularly over the left superior parietal cortex as well as
a repeating loop of current density that involved the memory-related regions of the superior parietal lobe, MTL, and right PFC. These
brain areas have previously been shown to be involved in successful remembering over forgetting based on instructions (Anderson
et al., 2004; Wylie et al., 2008; Nowicka et al., 2011). The authors concluded that sleep spindles, involving a network interconnect-
ing these areas, might be a mechanism by which selectivity of memory during sleep occurs.
2.31.8.2 Integration of New Information Into Existing Stores

Some studies suggest that sleep is beneficial for the integration of new information into networks of preexisting knowledge (Dumay
and Gaskell, 2007; Tamminen et al., 2010; Tamminen et al., 2013). Recognition of the world “cathedral” will become slower when
a new similar-sounding word, such as, “cathedruke,” is integrated into the mental lexicon. When participants are tested in this lexical
competition effect, integration of the new words (i.e., the word “cathedral” is recognized slower) is only shown after a 12-h period
containing sleep, but not wake. This effect was shown to be associated with the memory for the new words, that is, better memory
lead to better integration after sleep.
In a similar study, although participants showed increased lexical competition (i.e., better integration) regardless of whether a
9-h period contained sleep or wakefulness, the authors found that a higher spindle count was associated with better integration,
suggesting that this physiological feature of NREM sleep is particularly important for integration of new information into preexist-
ing networks (Tamminen et al., 2010). In a more recent study, Tamminen et al. (2013) investigated the role of sleep spindles and
SWA (<4 Hz) in a similar task, except that new words had actual meaning. In this study, participants had to learn new concepts that
had either many or few semantic associates with old concepts. Concepts that have few semantic associates are learned faster and
more effectively due to less interference from competing (old) related concepts. In a within-subjects design, participants were
trained at least 1 week apart in new concepts with few semantic associates or with many associates (no wake controls were
included). After learning the concepts with few semantic associates, participants had higher sleep density and SWA, compared to
the condition of many semantic associates. These findings suggest that NREM features, specifically sleep spindle density and
SWA, may play a role in the preferential integration of new (meaningful) information that lacks semantic competition (i.e., new
concepts with few semantic associates).
2.31.8.3 Extraction of Gist

In addition to integration, sleep seems to support extraction of the “gist” of experience. As discussed in section Functional Imaging
and Sleep Deprivation, the DRM task results in creation of false memories, or memories for “critical lures” representative of the
theme, or gist, of the list, which are retrieved with high probability and confidence (Deese, 1959; Roediger and McDermott,
1995). Using the DRM task, Payne et al. (2009) found that participants were able to recall more gist words after a period of sleep,
but not wake; both after a 12-h and a 90-min delay (Payne et al., 2009). Similar results have been found by others after a 12-h delay,
but only in “low” performers on correct memory performance (Diekelmann et al., 2010). Importantly, the “low” performers in this
study had similar performance to the sample in the Payne study. McKeon et al. (2012) also found increased false recall after sleep
(compared to wake), regardless of whether the DRM word lists were emotionally negative or neutral. The role of sleep in this type of
gist extraction is far from clear. Studies have also found that sleep decreased gist memories when performance was tested through
recognition, as opposed to recall, memory. These results were found regardless of whether the stimuli was presented aurally (Exp. 1)
or visually (Exp. 2; Fenn et al., 2009).
Although SWS seems to have a primarily beneficial role for declarative memory (see sections General Theories Regarding
Memory Advantages From Sleep and Sleep During Consolidation Benefits Memory), some studies suggest that it might have a nega-
tive role for gist extraction, at least with the DRM task; negative correlations between SWS and false memory have been reported
(Payne et al., 2009; Lo et al., 2014). Unlike the other mainly episodic tasks used in this literature (e.g., word-pair associates),
the DRM paradigm heavily relies on semantic/gist processing due to the strong relatedness of the words in each list. Payne and
colleague (2009) suggested that SWS, while assisting episodic memory consolidation, might impede semantic processing, resulting
in a decreased association with gist memory performance.
2.31.8.4 Inferential Associations

Making inferential associations also may be supported by sleep. In a study by Ellenbogen et al. (2007), participants encoded pairs of
abstract shapes that, unbeknownst to the participant, followed a particular hierarchy: A > B, B > C, C > D, D > E, and E > F, so that
A > B > C > D > E > F, and therefore A > F (see Fig. 6). When memory was tested 20 min after inferential memory performance
(e.g., A > F) was at chance level. Only after 12 and 24 h did participants show increased inferential memory. Importantly, those
who obtained sleep in the 12-h delay, compared to those who did not (12-h wake group), were able to develop the most distant
associations (e.g., B > E). Subjective confidence of the task was not related to inferential performance, suggesting that this sleep
benefit may occur outside of conscious awareness. Other studies have provided similar evidence of the role of sleep in the formation
of associative relationships (Lau et al., 2010; Lau et al., 2011; Alger and Payne, 2016). In two of these studies (Lau et al., 2010; Alger
and Payne, 2016), participants had to encode a face (A) paired with an object (B), later to encode the same object paired to a different
face (AB–BC). Memory for both the individual pairs (A–B, B–C) and the inferential pairs (A–C) was better remembered by partic-
ipants who napped immediately after encoding, compared to those who did not.
These findings support the complementary learning systems model (McClelland et al., 1995), which proposes that new memories
are initially stored in the hippocampus, which acts as a “trainer” and redistributes these memories to the neocortex for long-term
storage. This “training” and redistribution is thought to occur during SWS, with the particular help of slow waves (<4 Hz) and sleep
spindles (see Diekelmann and Born, 2010). Lau et al. (2010) reported that time spent in SWS was associated with better relational
memory (A–C pair, although see Alger and Payne, 2016 with a REM sleep correlation). Importantly, this association was independent
of a positive correlation between direct associative memory and relational memory, which suggests that while sleep supports the
consolidation of explicitly learned material, it might have a different role in memory integration.
Figure 6 Example stimuli from Ellenbogen, J.M., Hu, P.T., Payne, J.D., Titone, D., Walker, M.P., 2007. Human relational memory requires time and
sleep. Proc. Natl. Acad. Sci. U.S.A. 104 (18), 7723–7728. Through multiple trials, participants learned individual “premise pairs.” For example, they
learned that the abstract shape with the orange hue > the blue, and that the blue > the green. After a delay, they were asked to make inferences
about pairings that had never been seen before, yet conformed to the hierarchy (orange > blue > green), such as orange > green. Sleeping prior to
tested triggered a significant boost in inferential ability.
2.31.8.5 Creativity
Creativity, which could be considered another form of flexible memory reorganization, is also benefited by sleep (Cai et al., 2009;
Ritter et al., 2012; Sio et al., 2013). In the remote associates task, participants are presented with three words (e.g., dream, break,
light) and are asked to find a word that associates all three (in this case, “day”: daydream, daybreak, daylight). Cai et al. (2009)
had participants complete the task in the morning, followed by a period of napping or wake, and finished with another version
of the task in the afternoon. Between the morning remote associates task and the retention interval, participants completed another
task with the purpose of priming half of the answers for the remote associates task. Napping resulted in performance improvement
for the remote associates task, but only for those items that were primed. Importantly, only participants who reached REM sleep
during their naps showed this improvement, compared to NREM-only nappers and wake controls. A similar behavioral effect
was also found without previous priming, but only for difficult items (Sio et al., 2013). In another study, participants who paired
a creative problem with an odor before going to sleep were better at solving the problem when the same odor was presented during
sleep, compared to those who were not exposed to the odor during sleep (Ritter et al., 2012). Unfortunately, in this study no wake
controls were included, so a sleep-specific effect cannot be fully considered.
As the study by Cai et al. (2009) suggest, it is believed that REM sleep is particularly important for creativity. The authors argue that
REM sleep is optimal for the spreading activation generated by a memory trace of a target item (in this case, the primed answers).
Elevated ACh levels in the hippocampus interrupt “talk” to the neocortex, while low levels of ACh in the neocortex facilitate spreading
activation within cortical regions (see also Payne and Nadel, 2004; Payne, 2011a), leading to a reorganization of associative networks,
which in term results in the reinterpretation of information in the hippocampus (e.g., reaching the solutions for the remote associates
task).
2.31.8.6 Gain of Insight

There is also evidence that sleep may play a role in gaining insight or extracting hidden rules. Wagner, Gais, Haider, Verleger, and Born
(2004) used a number reduction task, in which participants are instructed to reduce a series of eight numbers into seven, by employ-
ing a rule that reduces two numbers into one, to find the final number of the series as fast as possible (Thurstone and Thurstone, 1941;
see Fig. 7). There is a hidden rule, unknown to participants, that allows them to find the last number faster. Those who obtained a full
night of sleep, compared to daytime and nocturnal wakefulness, were twice as likely to find the hidden rule. Even a daytime nap can
be advantageous to insight and rule extraction. Lau et al. (2011) presented subjects with Chinese characters, which could be grouped
by characters containing the same radical, or component of the character with a shared semantic component among the group (char-
acters for “mother” or “sister” with the same radical meaning “female”). After a nap, subjects were better able to correctly infer the
meaning of a new character that shared a radical of one of the originally learned groups of characters. Furthermore, they were also able
to explicitly state the meaning of a radical when it was presented alone. Interestingly, the superior ability to extract this implicit rule
was better after sleep, compared to wake, regardless of whether the nap occurred immediately after the learning session or a couple
hours later. Other studies have found similar sleep benefits for rule-dependent memory tasks, such as those depending on musical
sequences (Durrant et al., 2011) or probabilistic learning (Fischer et al., 2006), even when sensory modalities are different between
encoding and testing (Durant et al., 2016). These collective findings provide evidence to the view that sleep is advantageous for
problem solving, likely due to memory reorganization occurring during sleep.
2.31.8.7 A Theory of Memory Transformation During Sleep

Much of the research discussed earlier use tasks that prompt the brain to flexibly incorporate and extract information that is the most
beneficial for the individual, with sleep playing a large part of these processes. Furthermore, many of these studies have found corre-
lations between specific stages or phenomena of sleep and performance reflecting the transformation of memory. Each of these types
of memory discussed in previous sections (e.g., inference, gist, insight) differs from one another in the way they are formed. Therefore,
Figure 7 A visual depiction of the number reduction task. Participants are required to solve puzzles composed of three digits (in this case 10 s, 40 s,
and 90 s). Starting from the left side, if the numbers are the same, they enter that same number (here, the first two numbers are 1, so the participant
enters 1). If the numbers are different, they enter the third number possible (1 and 4 requires an entry of 9). They then compare each new number to
the next number in the sequence until they reach the final number (in red). Unknown to the subjects, embedded in this task is a hidden shortcut that
can be used to speed performance; the last three numbers are always a mirror image of the prior three numbers, with the first number of the mirror
(in this case, 9) always being the same as the final answer.
Figure 8 The information overlap to abstract model (Lewis and Durant, 2011). This figure illustrates how the reactivation of two overlapping
memories could lead to schema formation. Replayed memories, represented by the circles (gray circles replayed during one reactivation time and blue
circles replayed both times) can overlap during simultaneous replay (gray circles at time 1 and 2) as well as in more than one replay (blue circles).
Through this combination of replay, which strengthens the areas of overlap, and downscaling, which reduces the more unique aspects of each
memory, a schema is formed. The information most often reactivated and with more overlap will be more strongly represented.
it makes sense that there may not be one overarching theory to explain what is accomplished during sleep. However, there are some
intriguing ideas (for review, see Landmann et al., 2014). One thought-provoking theory is the information overlap to abstract (iOtA;
Lewis and Durrant, 2011) model, which builds upon schema theory (Howard, 1987; Mandler, 2014) and includes a special role for
SWS (see Fig. 8). According to the iOtA model, overlap may occur in a simultaneous or sequential manner during memory reacti-
vation through several bouts of SWS in any given night. Neurons that represent shared elements are activated with simultaneous reac-
tivation, which results in Hebbian-like facilitation. The outcome of simultaneous replay is that areas associated with shared memories
will build a stronger connection that areas associated with single memories. During later synaptic downscaling, while overlapping
memory traces survive, weaker connections of nonoverlapping areas are diminished. In sequential reactivation, shared traces are
also more strongly activated, and activation from subsequent reactivations builds up on previous reactivations. SWS bouts
throughout the night downscale connections in between sequential reactivations, which result in a selective strengthening by overlap
that provides a controlled mechanism to extract similarities between traces and create schemas.
Integration of new information into existing schemata is also benefited by sleep, as detailed earlier. Reactivation of novel infor-
mation elicits activation of schemata traces associated to the novel information. Hebbian learning is the product of simultaneous
firing of schema traces and new information traces. Nonetheless, reactivation and Hebbian processing are not enough to integrate
new information. iOtA assumes that for integration to occur, the new information needs to overlap with schemata multiple times.
Multiple overlap leads to survival from SWS downscaling. Additionally, through multiple reactivations, only schema-associated
information is integrated into the schema, leaving less relevant information out. In this way, assimilation of new information
has little overlap with existing schemata necessitates more reactivations, particularly if encoding was weak.
Although this model cannot account for all the transformations we discussed earlier, it can be applied to many of the findings. For
gist extraction, and the DRM task in particular, since the gist of each list is highly related to the study words, sequential (re)activation of
the study words may lead to indirect strengthening of the gist words (e.g., Payne et al., 2009; Diekelmann et al., 2010). However, this
explanation counters the negative correlation between SWS, during which most iOtA processes are thought to occur, and recall of study
words in the Payne et al. (2009) study. For relational memory, overlapping reactivation of the premise pairs (A > B, B > C) should
result to the eventual production of the abstracted representation of the overall hierarchy (i.e., B > C þ C > D þ D > E ¼ B > E;
Ellenbogen et al., 2007). In the number reduction task, overlapping reactivation of the memory traces of successfully completed prob-
lems should result in the insightful realization of the hidden rule (Wagner et al., 2004). While this theory puts much of the emphasis
on SWS, it is reasonable to think that all of sleep is important for memory transformations to occur and be stabilized. Future work will
need to further investigate and modify this and other models of preferential memory consolidation and transformation during sleep,
perhaps including the possible involvement of other sleep stages and sleep phenomena in these processes.
2.31.9 Future Directions and Conclusions
In this chapter, we provide a comprehensive review of the evidence suggesting an active role for sleep in the acquisition, preservation,
enhancement, integration, and transformation of information. The effects of sleep on memory have generated an ever-expanding
body of literature, but here we have focused mainly on declarative and procedural memory and presented evidence that nocturnal
sleep and naps benefit memory. Further, we presented evidence that manipulation of sleep parameters through technological or phar-
macological means can promote memory, while sleep deprivation and suppression of physiological features can impair memory. The
field of sleep and memory is constantly evolving as new advancements in research methods and techniques are developed, allowing
us to probe the relationship at deeper and more refined levels. As research and technology evolve, it becomes evident that the impact
of sleep on memory is more complex than simple dichotomous associations between sleep stages and memory (e.g., REM sleep bene-
fits emotional memory) and that multiple sleep features combine to support varied forms of memory. This suggests that sleep may be
much more than simply the sum of its parts. Future research should focus on sleep as a whole, the importance of sleep cycles and
specific features within them, and the consequences of a disrupted progression of sleep. Beyond this, as the tools and methodologies
used to investigate the relationship between sleep and memory advance, special attention should be paid to the physiological
phenomena that occur throughout the stages of sleep, the interaction between sleep stages, and the neurochemical/neurohormonal
states during nocturnal compared to daytime sleep. Finally, much of the literature reviewed in this chapter comes from data collected
from healthy, young, relatively homogenous samples (e.g., undergraduate cohorts). There are other bodies of literature focused on
the relationship between sleep and memory formation and consolidation in clinical, aging, and child/adolescent populations.
However, these populations, among others, remain understudied. Therefore, developing a more complete picture of the progression
of the relationship between sleep and memory through the different life stages both in healthy and clinical individuals is a fruitful
area of future research.
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The Cognitive Psychology of Sleep and MEMORY

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2.

31 The Cognitive Psychology of Sleep and Memory

2.31.1 Introduction 571

2.31.2 An Introduction to the Stages of Sleep

2.31.2.1 Stage 1 Sleep

2.31.2.2 Stage 2 Sleep

2.31.2.3 Slow-Wave Sleep

2.31.2.4 Rapid Eye Movement Sleep

2.31.3 Classification and Phases of Memory

2.31.3.1 Phases of Memory

2.31.4 General Theories Regarding Memory Advantages From Sleep

2.31.5 Sleep During Consolidation Benefits Memory

2.31.5.2 Sleep Facilitates Declarative Memory

2.31.5.2.1 Overnight Sleep

2.31.5.2.2 Daytime Napping Benefits Memory

(A) Learning Sleep Retrieval

Sleep Learning Sleep Retrieval

Sleep Learning Retrieval

1800 1900 2230 0130 0230 0330 1100 1200 hours

2.31.5.3 Manipulations of Sleep Physiology and Memory During Sleep

2.31.5.3.1 Manipulation of Sleep Physiology

2.31.5.3.2 Reactivation of Memory During Sleep

2.31.5.4 Sleep and Emotional Memory

2.31.5.4.1 Selective Consolidation of Complex Emotional Memories

2.31.6 Sleep Deprivation Impairs Memory

2.31.6.1 Recent Work on Sleep Deprivation

2.31.6.1.1 Functional Imaging and Sleep Deprivation

2.31.7 Sleep Prior to Encoding Primes for New Learning

2.31.8 Sleep Aids Memory Transformation: Generalization, Integration, and Reorganization

2.31.8.1 Preferential Consolidation of Prospective Information

2.31.8.2 Integration of New Information Into Existing Stores

2.31.8.3 Extraction of Gist

2.31.8.4 Inferential Associations

2.31.8.6 Gain of Insight

2.31.8.7 A Theory of Memory Transformation During Sleep

2.31.9 Future Directions and Conclusions

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