Bs PBR 2019 01 007

ARTICLE IN PRESS
The impact of sleep

deprivation on declarative
memory
James N. Cousinsa,*, Guillen Fernándezb
a
Centre for Cognitive Neuroscience, Neuroscience and Behavioral Disorders Programme,
Duke-NUS Medical School, Singapore
b
Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre,
Nijmegen, The Netherlands
*Corresponding author: Tel.: +65-6516-3934; Fax: + 65-6221-8625,
e-mail address: james.cousins@duke-nus.edu.sg
Abstract
Sleep plays a crucial role in memory stabilization and integration, yet many people obtain
insufficient sleep. This review assesses what is known about the level of sleep deprivation that
leads to impairments during encoding, consolidation and retrieval of declarative memories,
and what can be determined about the underlying neurophysiological processes. Neuroimag-
ing studies that deprived sleep after learning have provided some of the most compelling
evidence for sleep’s role in the long-term reorganization of memories in the brain (systems
consolidation). However, the behavioral consequences of losing sleep after learning—shown
by increased forgetting—appear to recover over time and are unaffected by more common
forms of partial sleep restriction across several nights. The capacity to encode new memories
is the most vulnerable to sleep loss, since long-term deficits have been observed after total and
partial sleep deprivation, while retrieval mechanisms are relatively unaffected. The negative
impact of sleep loss on memory has been explored extensively after a night of total sleep dep-
rivation, but further research is needed on the consequences of partial sleep loss over many
days so that impairments may be generalized to more common forms of sleep loss.
Keywords
Long-term memory, Sleep, Sleep deprivation, Encoding, Consolidation, Retrieval, Declara-
tive memory
1 Introduction
The role played by sleep in memory was first observed nearly a century ago (Jenkins
and Dallenbach, 1924), but has undergone a renaissance in the last 3 decades in tan-
dem with advances in neuroimaging. Research has primarily focused on the covert
Progress in Brain Research, ISSN 0079-6123, https://doi.org/10.1016/bs.pbr.2019.01.007
© 2019 Elsevier B.V. All rights reserved.
1
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2 Progress in brain research: Sleep deprivation cognition
processing of memories after learning, where sleep is considered to be the ideal en-
vironment for network level changes to memory representations that stabilize them
for long-term storage (Diekelmann and Born, 2010; Tononi and Cirelli, 2014). More
recently, the importance of sleep to prepare the brain for new learning has also
attracted attention from experimental research, indicating that sleep may be critical
at all stages of long-term memory.
These findings exist upon a backdrop of widespread sleep curtailment, driven by
factors that range from smartphone use (Cain and Gradisar, 2010) to academic pres-
sures (Gillen-O’Neel et al., 2013) and stress (Feld and Shusterman, 2015; Massar
et al., 2017). This is particularly true of adolescents, who curtail sleep to less than
7 h per night during the week (Crowley et al., 2007; Lo et al., 2015), far below
The National Sleep Foundation recommendation of 8–10 h for this age group
(Hirshkowitz et al., 2015). Moreover, epidemiological studies consistently find a
relationship between academic performance and sleep loss (Curcio et al., 2006).
Insufficient sleep is not only a problem for adolescents, but also is common in
healthy adult populations, individuals with sleep disorders, and occurs as a conse-
quence of normal aging (Krause et al., 2017).
In light of this, the motivation for experimental research addressing the effects of
sleep deprivation on memory is twofold. The first is to understand the neurophysiology
underlying the effect of sleep loss on different stages of memory, including the
reorganization of representations in the brain, which particular networks are most
vulnerable, and the contributions of different stages of sleep to these processes.
Importantly, these effects may be due to an absence of beneficial memory processes that
are associated with sleep (e.g., consolidation), but may also be a result of the deleterious
effects associated with extended wakefulness. The second, and arguably most neglected,
is to assess the practical relevance of such findings in order to guide public policy on
health and education, including what forms of sleep deprivation lead to memory impair-
ments and the extent to which lab-based findings can be generalized to real learning.
This review seeks to provide a comprehensive overview of human sleep depri-
vation studies that have investigated the initial learning, long-term storage and
retrieval of memories at delays ranging from a few minutes to many months.
A full account of sleep’s role in memory cannot be determined from deprivation
studies alone, but the contributions they have made to current understanding will
be assessed in view of the strengths and limitations of this approach. We will begin
by outlining key concepts in memory and sleep deprivation methodology, before
addressing the effects of sleep loss on each stage of long-term memory.
2 Memory stages and sleep

Declarative memory refers to learned information that is available for conscious re-
trieval and is stored in the brain from timescales ranging from minutes to a life time.
They are often further subdivided into memories for events (episodic) and factual
knowledge that is stored in the absence of any specific study context in terms of when
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2 Memory stages and sleep 3
and where this knowledge was acquired (semantic) (Cohen and Squire, 1980). Non-
declarative memory refers to learning that is not consciously accessible, such as pro-
cedural skills, which have been reviewed extensively elsewhere (e.g., Robertson
et al., 2004).
The functions of long-term memory are divided into three sub-processes—
encoding, consolidation and retrieval—each of which is potentially impaired by in-
sufficient sleep. Upon perception of a stimulus, encoding is thought to take place
primarily through changes in the strength of connections between neurons, resulting
in formation of a trace within distributed networks in the brain. The synaptic homeo-
stasis hypothesis (Tononi and Cirelli, 2014) is a prominent model to account for why
sleep is critical to prepare the brain for encoding. Synaptic connections are potenti-
ated during wakefulness, and slow-wave activity is proposed to globally downscale
synaptic weights to avoid saturation in memory networks, thus facilitating new
learning.
Newly formed declarative memories are initially susceptible to forgetting due to
interference and decay. Successful retention relies on processes where the represen-
tation is transformed at the cellular level (synaptic consolidation), and over longer
periods become stabilized in the neocortex and less dependent on the hippocampus
(systems consolidation), a process that may extend for several years (Frankland and
Bontempi, 2005). Two stage models propose that in order to avoid interference be-
tween incoming information and stored memories, these hippocampal and neocorti-
cal systems operate in distinct but complementary ways to support memory
consolidation (Kumaran et al., 2016; Marr, 1970; McClelland et al., 1995). The hip-
pocampus rapidly acquires the specifics of individual experience, binding together
diverse inputs from several brain areas. The neocortex more gradually develops
structured knowledge from experience, although this can occur more rapidly when
learned information is consistent with existing knowledge (Tse et al., 2007). The
reactivation of these representations during offline periods, particularly sleep, is pro-
posed to drive this process (Diekelmann and Born, 2010). During retrieval, stored
memories are accessed using a variety of internal or external cues, and also recon-
structed based on prior knowledge (Bartlett, 1932).
Several approaches have been used to study the negative impact of sleep depri-
vation on each of these memory functions (Fig. 1). The most common is to compare
performance after a night of total sleep deprivation to a night of nocturnal sleep,
sometimes allowing additional nights of recovery sleep in order to remove general
effects of fatigue. This method has provided important insights regarding systems
consolidation and the identification of underlying network dysfunction during
encoding, but seldom occurs outside the laboratory, making it unclear whether such
effects can be generalized to more common forms of sleep loss.
Partial sleep deprivation studies solve this issue of generalizability, typically
allowing 3–4 h of nocturnal sleep for one or several consecutive nights. The
night-half paradigm (Yaroush et al., 1971) is one such approach, which takes advan-
tage of the fact that sleep in the first half of the night is dominated by slow-wave sleep
(SWS), while the second half is predominantly rapid-eye movement sleep (REM).
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FIG. 1
Experimental designs for examining the effects of sleep deprivation on different stages of
memory processing. Total sleep deprivation is the most commonly used paradigm for
laboratory experiments. For encoding, 1 night of nocturnal sleep is missed prior to learning,
meaning that participants have been awake typically for 24–36 h prior to encoding. This is
followed by recovery sleep to ensure that participants are no longer sleep deprived when
retrieval takes place. For consolidation, encoding takes place when participants are well
rested, prior to the night of sleep deprivation, which is again followed by recovery sleep. For
retrieval, encoding is followed by 1–2 nights of nocturnal sleep, allowing encoded materials to
be consolidated to some extent, then the night of sleep deprivation takes place prior to
retrieval. Chronic sleep restriction represents a more common form of sleep loss that includes
several consecutive nights of insufficient sleep, although fewer experimental studies have
been carried out on this type of sleep schedule. Experimental designs are identical to the total
sleep deprivation paradigm except that they include several nights of partial sleep deprivation
in place of the single night of total sleep loss. Partial sleep deprivation designs are also utilized
with fewer nights than shown, particularly for the half-night paradigm which compares
conditions that sleep in the early or late half of the night (not shown here).
Depriving sleep in one half of the night or the other indicates the relative contribu-
tions of each stage to memory. The other form of partial deprivation uses awakenings
or subtle acoustic stimulation to provide targeted disruption of specific aspects of
sleep. We will now provide a focused examination of studies using these methods
to determine the effects of sleep deprivation on each stage of long-term memory:
encoding, consolidation and retrieval.
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2.1 Encoding
Encoding refers to the process of acquiring information from the environment and
placing it into memory, which relies on a complex interaction of factors. Attending
to a stimulus is of course critical in order for information to proceed to more perma-
nent long-term stores of memory (Atkinson and Shiffrin, 1971). This requires the
ability to focus and sustain attention on a stimulus while ignoring distractors, as well
as cognitive control processes that allocate resources toward the goal of creating an
enduring memory trace. These underlying cognitive processes consistently deteriorate
after sleep loss, with impairments scaling in a dose-dependent manner with the amount
of time spent awake (Lim and Dinges, 2010), which will impact on an individual’s
capacity to encode. Also the type of processing the stimulus undergoes will determine
the strength of encoding, where shallow processing (e.g., sensory) leads to a weaker
memory trace than deeper processing (e.g., semantic) (Craik and Lockhart, 1972).
In order for a stimulus to be successfully encoded into declarative memory, it is
thought to induce structural changes in the brain to enable activity that will produce
the mental experience of remembering during subsequent retrieval. There is a general
consensus that sleep is critical to prepare the brain for encoding, but it is tremendously
difficult to separate the contributions of these underlying factors to behavioral and
neurophysiological impairments that have been observed after sleep deprivation.
The amount of sleep that leads to encoding deficits is also unknown, particularly in
relation to chronic sleep loss.
An extreme form of sleep deprivation provided the first indication that online
memory processes may be disrupted by sleep loss, where 3–4 consecutive nights
of deprivation were found to distort participants’ perception of time (Morris et al.,
1960). This “temporal memory” was revisited 40-years later by Harrison and
Horne (2000), who asked participants to encode two separate sets of faces after
1 night of total sleep deprivation. When tested 5 min later, recognition of faces
was unaffected relative to a control group who slept, but the associated context of
which set the faces belonged to was impaired. Caffeine was administered in two
separate groups to reduce general effects of fatigue, but the deficit remained.
The negative impact of total sleep deprivation is not restricted to temporal
memory—or more broadly “contextual memory”—but to the encoding of a range
of verbal and visual materials. For example, one study observed a significant 16% def-
icit in the capacity to incidentally encode pictures (Yoo et al., 2007). Others have found
similar deficits for verbal word lists (Chuah et al., 2009; Drummond et al., 2000, 2005),
face pairs (Alberca-Reina et al., 2014), film clips (Tempesta et al., 2016) and pictures
(Kaida et al., 2015; Poh and Chee, 2017; Saletin et al., 2016).
These impairments may also interact with other factors that are known to influ-
ence encoding, such as emotion. A recent study explored memory for positive, neg-
ative or neutral film clips watched after total sleep deprivation (Tempesta et al.,
2016). Importantly, memory tests took place after 2 nights of recovery sleep, allow-
ing any effects to be attributed to encoding rather than retrieval. They found a 15%
reduction in contextual memory for the order of events in all film clips when
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encoding took place after deprivation. Recognition was reduced by 26% overall, a
difference that was significant for positive and neutral film clips, but negative clips
were unaffected. The encoding of emotional memories relies on activity primarily in
the amygdala, hippocampus and prefrontal cortex (Dolcos et al., 2005; Erk et al.,
2003). The authors speculate that negative memories rely on the amygdala, which
may still encode effectively after sleep loss, while hippocampal-dependent contex-
tual memories are more vulnerable to sleep loss.
Why does sleep deprivation impair new learning? This question has been
addressed by a handful of studies using forms of partial sleep deprivation, which
allow the separation of sleep stages and their relative contributions to memory deficits
to an extent. When sleep is restricted to only 4 h, it tends to be dominated by SWS due
to the homeostatic drive to release sleep pressure accumulated across wakefulness
(Borbely, 1982), while REM sleep that dominates later sleep periods is lost. Relative
to an 8 h sleep opportunity, restriction to only a 4 h opportunity was found to have no
effect on the encoding of face pairs (Alberca-Reina et al., 2014). Similarly, encoding of
a 2D-object location task remained unimpaired after 2 nights of only 4.25 h sleep
opportunity (Cedernaes et al., 2015). These findings suggest that 4 h of SWS-rich sleep
is sufficient to restore encoding capacity, and support the notion that slow-wave activ-
ity is most critical (Tononi and Cirelli, 2014). Congruent with this, even subtle disrup-
tion of SWS via acoustic stimulation can impair encoding the following day (Van Der
Werf et al., 2009), while acoustic disruption of REM sleep was found to have no
negative effect on encoding, even for pictures with emotional tone (Kaida et al., 2015).
Few studies have examined memory function under more sustained levels of
sleep loss, which is surprising because it closely mirrors common patterns of cur-
tailed sleep during the week followed by “recovery” sleep on weekends (Crowley
et al., 2007; Lo et al., 2015). The consequences of this type of schedule were recently
tested in adolescents. Picture encoding was significantly reduced by 9% when ado-
lescents were restricted to a 5 h sleep opportunity for 5 nights (Cousins et al., 2017),
while the capacity to learn detailed factual knowledge was reduced by 26% after only
4 nights of 5 h sleep opportunity (Cousins et al., unpublished; Fig. 2). SWS tends to
remain relatively preserved under this level of chronic deprivation, while stage 2 and
REM sleep durations have been shown to be significantly reduced (Ong et al., 2016;
Voderholzer et al., 2011), therefore the proposed dependence of encoding capacity
on SWS does not hold up under conditions of chronic sleep loss.
The retrieval of false information may also indicate deficient prior encoding.
The misinformation paradigm asks participants to view a series of photographs,
then a later misinformation phase attempts to incorporate false information to mem-
ories for those scenes via narratives that include misleading statements among accu-
rate ones. Incorporation of this false information increased after total sleep
deprivation, but only when the initial viewing of images and misinformation from
leading questions occurred after deprivation (Frenda et al., 2014). This effect was
also observed in young adults after total sleep deprivation and in adolescents under-
going severe chronic deprivation to only 5-h sleep opportunity for 7 nights (Lo et al.,
2016a). These findings not only indicate degraded encoding after sleep loss, making
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FIG. 2
Retention of factual knowledge was impaired after 4 days of chronic sleep restriction.
(A) The experiment was part of an 11-day study that included 2 baseline nights (B1, B2),
a 5-night sleep restriction period (SR1-SR5) and 3 recovery nights (R1–R3). Encoding
(E) took place on sleep restriction day 4 (SR4) and was followed by retrieval 30 min later (R),
when the 5 h group had undergone 4 nights of 5 h sleep opportunity. The control group
were permitted 9 h sleep opportunity on every night of the protocol. Encoding included six
30–40-min blocks containing detailed facts about 12 species of arthropod, separated by
breaks. Participants were tested using 120 two-alternative forced choice questions of
varying difficulty. Questions were followed by a confidence rating (certain,
somewhat certain, guess). Certain memory (correct-incorrect) was significantly worse in the
SR group relative to controls (Cousins et al., unpublished).
memories more susceptible to false retrieval, but also they illustrate the potential
consequences of these effects in, for example, wrongful conviction due to inaccurate
eye witness testimony.
The Deese-Roediger McDermott (DRM) paradigm is another well-established
method to examine false memory (Roediger and McDermott, 1995). Participants
learn lists of words (e.g., bed, pillow, night) that are missing a semantically related
associate (e.g., sleep), and incorrect retrieval of this un-studied associate is taken as a
measure of false recall. These false memories have been suggested to result from the
formation of a gist memory trace for the learned lists. In contrast with the misinforma-
tion paradigm, chronic (4 nights of 4 h sleep opportunity) and total sleep deprivation
prior to encoding word lists were shown to decrease subsequent false recognition, as
well as recognition of previously encoded words (Chatburn et al., 2017). The authors
speculate that sleep deprivation may impair both the encoding of individual words and
the formation of gist memory traces for the overall word lists.
What are the neural changes that might account for these encoding impairments?
Declarative learning comprises distributed activity in neocortical sensory and asso-
ciation networks that are bound together by the medial temporal lobe, specifically the
hippocampus (McClelland et al., 1995). After total sleep deprivation, Yoo et al.
(2007) observed decreased posterior hippocampal activity during picture encoding,
alongside reduced functional coupling with neocortical regions and increased con-
nectivity with arousal networks of the brainstem and thalamus.
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This hippocampal dysfunction after sleep loss is also observed in animal

studies. Hippocampal long-term potentiation—one of the primary mechanisms of
neuroplasticity—is decreased and decays more rapidly after sleep deprivation
(Campbell et al., 2002; Kreutzmann et al., 2015). Global synaptic potentiation also
decreases during sleep (de Vivo et al., 2017) and this may be a mechanism to facil-
itate new learning (Tononi and Cirelli, 2014).
Slow-wave activity during sleep and subsequent encoding-related activity
in the hippocampus have been linked in several human neuroimaging studies.
The disruption of slow waves by subtle acoustic stimulation in elderly participants
led to reduced capacity to encode pictures and a concomitant reduction in
hippocampal activity (Van Der Werf et al., 2009). Acoustic stimulation that is
coordinated with the slow oscillation has the opposite effect of boosting slow
waves, and this is associated with improved encoding (Ngo et al., 2013) and
increased hippocampal activity (Ong et al., 2018). Additionally, individuals with
higher gray matter in certain hippocampal sub-fields (CA3/dentate gyrus) were
more vulnerable to encoding impairments after total sleep deprivation, but also
showed higher slow-wave activity during recovery sleep and larger subsequent
improvements in performance (Saletin et al., 2013).
Other neuroimaging studies in humans have corroborated this decrease in hippo-
campal activation during encoding (Poh and Chee, 2017), but wide ranging networks
that subserve a range of cognitive functions have also been implicated. For example,
reduced activity was observed in several temporal and parietal regions during verbal
learning (Chuah et al., 2009), networks that had a high degree of overlap with those
observed while performing working memory tasks after total sleep deprivation (Chee
and Chuah, 2007). Conversely, others have identified increased activity in frontal and
parietal regions during verbal encoding (Drummond et al., 2000; Jonelis et al., 2012),
interpreted as compensatory activity to support task performance that may interact
with task difficulty (Drummond et al., 2005). It is difficult to determine whether such
increases in activity really do compensate for deficits, as they may simply represent
reduced efficiency of processing in those regions after sleep deprivation.
Going beyond increases and decreases in activity, a recent study used multi-voxel
pattern analysis to assess the quality of information represented in the brain during
the encoding of scenes (Poh and Chee, 2017). Greater similarity of representations
across repetitions of stimuli is associated with better memory in well-rested individ-
uals (Xue et al., 2010). Total sleep deprivation was found to reduce the stability of
neural representations across repetitions in the parahippocampal place area, while
the level of stability correlated with subsequent memory in well-rested participants,
but not those who were sleep deprived. The authors suggest this might reflect de-
graded quality of cortical sensory information, or fluctuations in top-down atten-
tional control that leads to instability across repetitions.
These imaging findings highlight the challenge of delineating domain specific
effects in the sleep deprived state, which produces wide ranging deficits. Incidental
picture encoding tasks control for attentional lapses to some degree, since encoding
trials where the wrong response is made to simple questions about the stimulus
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(e.g., does the picture contain a building or not?) are removed from analyses. Studies
using this paradigm also found no relationship between task response times—which
are an indicator of general levels of alertness—and encoding performance (Cousins
et al., 2017; Yoo et al., 2007). Such dissociations between cognitive measures have
been noted several times in prior work (Rupp et al., 2012; Van Dongen et al., 2003,
2004), suggesting that encoding specific mechanisms may be affected by sleep dep-
rivation in addition to deficits to attention. There is consistent evidence that
hippocampal-dependent memory functions are reduced after total sleep deprivation
(e.g., Yoo et al., 2007) and chronic sleep loss (Cousins et al., 2017, 2019), while net-
works governing other critical processes for encoding like attention are also impli-
cated. The observed encoding impairments are likely to be due to a combination of
these factors.
2.1.1 Conclusion
The complete removal of nocturnal sleep consistently impairs the subsequent encod-
ing of many declarative memories, and this is linked to deficient function of a range
of neural networks supporting memory and associated processes such as attention
and executive function. These deficits may be dependent on the loss of SWS, because
half a night of sleep dominated by SWS is sufficient to restore encoding capacity.
This supports the proposed role for SWS to refresh memory networks for subsequent
encoding (Tononi and Cirelli, 2014). However, this explanation breaks down under
more extended periods of chronic sleep restriction, where encoding is impaired but
SWS is preserved. It therefore remains an open question as to what other features of
sleep have a functional role for encoding in these circumstances. Stage 2 and REM
sleep are reduced under these conditions, therefore they may play a more important
role when encoding mechanisms are pushed to their limits across consecutive days
of sleep loss. Sleep spindles are also reduced, and there is some evidence that these
are important to prepare the brain for new learning (Mander et al., 2011). To our
knowledge, experimental research of memory under these more typical patterns
of restricted sleep over several days has only been examined in adolescents, therefore
further research is warranted to establish the levels of restriction that impair learning
in adults and the features of sleep that are most critical to encoding.
2.2 Consolidation
The initial encoding of a memory is followed by stabilizing processes at the level of
both synapses and systems in the brain. This covert reverberating activity occurs
across both wakefulness and sleep and is susceptible to impairment by subsequent
learning (M€ uller and Pilzecker, 1900), as well as pharmacological and electrophys-
iological interventions (McGaugh, 2000). While the waking brain is optimized to
encode and retrieve information in the external environment, the sleeping brain is
proposed to provide the optimal conditions for consolidation processes to strengthen
and integrate memories into long-term storage (Rasch and Born, 2014). Several
lines of converging evidence support this preferential role for sleep in strengthening,
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stabilizing and reorganizing memories in the brain. Recently developed techniques

allow direct examination of these processes, for example via manipulation of elec-
trophysiology and specific memories with acoustic stimulation (Cousins et al., 2014;
Ngo et al., 2013; Rudoy et al., 2009), and measurement of patterns of memory reac-
tivation during sleep with EEG (Belal et al., 2018; Cairney et al., 2018; Sch€onauer
et al., 2017) and fMRI (Van Dongen et al., 2012). The weight of evidence suggests
declarative memory consolidation primarily relies on SWS, although subsequent pe-
riods of REM may play a complementary role in neuronal plasticity (Diekelmann
and Born, 2010; Giuditta, 2014).
The complete or partial removal of sleep by comparison is a coarser method to
investigate consolidation, but sleep deprivation studies compliment this literature in
two ways. The exaggerated sleep effects provided by total sleep deprivation make it a
powerful tool to observe the often subtle differences in brain activity when retrieving
memories after long delays of up to 6 months (e.g., Gais et al., 2007). From a more
applied perspective, sleep deprivation studies allow the assessment of whether com-
mon patterns of sleep loss have negative consequences for memory consolidation in
the long term.
The consolidation of most lab-based declarative memory tasks are affected by
total sleep deprivation, which invariably use linguistic stimuli (Gais et al., 2006,
2007; Idzikowski, 1984; Lin and Yang, 2014; Sch€onauer et al., 2015; Sterpenich
et al., 2017) or pictures of faces and objects (Griessenberger et al., 2012; except
see Mograss et al., 2009). Navigation tasks represent a more naturalistic form of
learning, and these are less consistently affected by sleep loss. Recognition of
previously navigated routes was reduced by 8% when tested immediately after total
sleep deprivation, while performance of those who slept improved by 21% (Ferrara
et al., 2006). A follow-up study allowing 1 night of recovery sleep observed approx-
imately 9% improvement in spatial memory in those who slept compared with no
change after sleep deprivation (Ferrara et al., 2008), while no impairments were
observed after 2 nights of recovery sleep (Orban et al., 2006; Rauchs et al.,
2008). This clearly indicates recovery of losses to consolidation over time.
Sleep-dependent memory consolidation also protects memories from retroactive
interference (Ellenbogen et al., 2009). Consistent with this, total sleep deprivation
led to greater interference when paired associates were retrieved under a different
emotional context to encoding, which was achieved by inducing different moods
in participants within each session (Deliens et al., 2013a). Conversely in a separate
study, the same authors examined the interference induced by learning new paired
associates prior to retrieval of pairs that were learned before sleep. They found ret-
roactive interference only when initial learning was followed by nocturnal sleep, but
not total sleep deprivation (Deliens et al., 2013b). The authors suggest that in this
instance, sleep-dependent consolidation may have promoted the updating of the
original pairs with new words encountered during interference learning (reconsoli-
dation). At the very least these studies suggest that the effects of sleep loss are
dependent on the specific type of interference employed in the task.
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Sleep is also proposed to preferentially consolidate emotional memories while

reducing their affective tone, allowing the retrieval of experience without the asso-
ciated negative emotional impact (Walker and van Der Helm, 2009). The conse-
quence of sleep loss to processing of emotional content was examined in one
study where participants observed positive, negative and neutral pictures prior to
a night of sleep deprivation, with recognition tested after a further 2 nights of recov-
ery sleep (Sterpenich et al., 2007). Sleep deprivation was associated with degraded
recognition of positive and neutral images relative to a night of sleep, while negative
content remained relatively preserved. These differences were no longer present
when the same participants were tested 6-months later (Sterpenich et al., 2009).
Further studies have produced mixed results with regard to the effects of sleep loss
on emotional memory. One study found that while total sleep deprivation impaired
picture recognition after 1 week, there was no interaction with emotion (Atienza and
Cantero, 2008). Similarly, episodic memory for film clips was reduced if viewing
was followed by a night of sleep deprivation, regardless of emotion contained in
the clips (Tempesta et al., 2017), while others failed to show a negative impact of
sleep deprivation on recognition of emotional or neutral film clips (Kuriyama
et al., 2010). Another study used a novel approach by measuring the number of spon-
taneous intrusions of a traumatic film clip over several days when the initial viewing
was followed by sleep or total sleep deprivation (Porcheret et al., 2015). They found
significantly fewer intrusions immediately after sleep deprivation, but no group dif-
ferences after subsequent recovery sleep. A parsimonious account for these incon-
sistent findings is that any differential effects of emotion on memory after sleep
deprivation are recovered over time.
Remarkably, those studies that have tested the persistence of total sleep depriva-
tion effects on declarative memory consolidation beyond a few days consistently fail
to observe lasting deficits: after 3 days (Orban et al., 2006; Porcheret et al., 2015;
Rauchs et al., 2008, 2011), 7 days (Sch€ onauer et al., 2015; Smith, 1995, except
see Atienza and Cantero, 2008), 10 days (Kuriyama et al., 2010) and 6-months
(Gais et al., 2007; Sterpenich et al., 2009). Notably, many of these studies observed
changes in the underlying brain networks supporting retrieval, suggesting altered
systems consolidation despite a lack of overt behavioral effects, which will be
discussed below. This was systematically explored in a pair of simple but elegant
experiments that found immediate impairments for nonsense syllables and paired as-
sociates on the morning after deprivation, but these were no longer apparent after 3–6
recovery nights of sleep (Sch€ onauer et al., 2015). Deficits for consolidation of a
non-hippocampal procedural memory task (mirror tracing) however could not be
recovered. The authors speculate that the hippocampus might serve as a buffer for
declarative information until the next sleep opportunity when consolidation can
occur. An alternative possibility concerns the simple linguistic stimuli typically used,
which are difficult to retain at longer delays and therefore high levels of forgetting
might obscure subtle sleep effects. This was tested in a study using a more naturistic
task, where participants learned detailed factual material across a 5 h period that was
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tested 7 days later (Cousins et al., unpublished). Consistent with prior research, there
was no memory impairment after 1 week if learning was followed by total sleep
deprivation.
Examples of memories being altered qualitatively during sleep are proposed to be
a consequence of reorganization and integration of information with existing knowl-
edge (Lewis and Durrant, 2011; Stickgold and Walker, 2013), although the effects of
sleep loss on this process have produced mixed results. A study using the Deese-
Roediger McDermott false memory paradigm found that 33% fewer words were
falsely recognized after total sleep deprivation when compared to nocturnal sleep
(Darsaud et al., 2011), which may reflect the extraction of the underlying gist of word
lists during sleep (Lewis and Durrant, 2011; Stickgold and Walker, 2013). Notably
however, two other studies failed to find similar differences between sleep and sleep
deprivation for recognition (Diekelmann et al., 2008) or free recall (Diekelmann
et al., 2010).
Memory for problems in the remote associates task (RAT) are also thought to
undergo reorganization during sleep (Cai et al., 2009). Each trial displays three
apparently unrelated words (e.g., cottage, swiss, cake) and participants must provide
a fourth word that is common to each of them (e.g., cheese). A study using a variant
of this task found that solution rates for incubated problems did not differ between
nocturnal sleep and sleep deprived participants, while sleep deprivation was even
associated with a modest but significant 1.6 s increase in the average speed of solu-
tions (Landmann et al., 2016). Similarly, others have failed to find impairments for
this task after total or chronic deprivation to only 5 h sleep opportunity for 2 nights
(Cousins et al., unpublished). Establishing the circumstances where sleep qualita-
tively alters memories is vitally important to understand how learned information
is reorganized during sleep and what adaptive function that might convey. The pro-
posal that sleep reorganizes memories to facilitate problem solving and extract the
gist of learned information, leading to false memories, is not well supported by
studies of sleep deprivation.
Sleep deprivation has also been shown to negatively affect prospective memory,
which is the ability to remember that an intention must be carried out in the future
(prospective component) and also remember what exactly that intention is (retro-
spective component). This is tested by providing participants with an intention
(e.g., press a certain key) to carry out at a predefined time or in response to a cue
(e.g., a predefined word appears) that is only presented later while performing a
different task. Depriving 1 night of sleep led to approximately half as many intended
actions being carried out in relation to cues when compared to those who slept nor-
mally (Diekelmann et al., 2013b). This was shown to benefit both prospective
remembering that an intention should be carried out and retrospective remembering
of what exactly the intention was (Diekelmann et al., 2013a). Retrieval in both
studies took place after a night of recovery sleep when participants were no longer
sleep deprived, therefore failure to recall the intention most likely reflected a
failure to consolidate the association between cue and intention during the sleep
deprivation night.
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With regard to partial sleep loss, earlier studies disrupted REM sleep by awak-
enings and compared that to non-specific disruption of non-REM stages, with some
finding REM-related impairments to memory (Empson and Clarke, 1970; Tilley and
Empson, 1978) and others finding none (Chernik, 1972). This technique provided
some early evidence that REM sleep may be important for consolidation of emo-
tional memories, where disruption of REM sleep led to impaired recall of threatening
material (Grieser et al., 1972).
More recently, targeted disruption of SWS and REM has produced mixed results.
Selective disruption of SWS was shown to impair consolidation of visuospatial
memories, although consolidation of verbal information was reduced after disruption
of SWS or REM (Casey et al., 2016). Others failed to show any impact of depriving
SWS or REM on declarative or procedural consolidation (Genzel et al., 2009;
Morgenthaler et al., 2014). Moreover, this method of determining contributions of
different sleep stages to consolidation has been criticized because of the stress asso-
ciated with repeated arousals (Born and Gais, 2000). In light of these non-specific, or
non-existent effects, sleep disruption may not be an effective method to separate the
influence of different sleep stages on memory consolidation.
The half-night paradigm was first utilized to examine REM and SWS contribu-
tions to consolidation, revealing less forgetting of paired associates after the first 4 h
of SWS-rich sleep, relative to later REM-rich sleep or daytime wakefulness (Barret
and Ekstrand, 1972; Yaroush et al., 1971). Subsequent half-night studies have shown
similar SWS-dependence (Drosopoulos et al., 2005; Gais and Born, 2004; Hockey
et al., 1972; Plihal and Born, 1997; except see Rauchs et al., 2004) with roughly
4 h of SWS-rich sleep providing consolidation benefits that were equivalent to a full
night of sleep in some cases (Cedernaes et al., 2015, 2016; Kopasz et al., 2010;
Tucker and Fishbein, 2009). Similarly for prospective memory, depriving early
SWS-rich sleep led to an impairment that was equivalent to losing a full night of
sleep, while depriving only late-night REM-rich sleep had no negative effects
(Diekelmann et al., 2013b).
This method of partial sleep deprivation has provided fairly consistent evidence
for a preferential role of REM sleep in processing emotional memories. A later pe-
riod of REM-rich sleep promoted better memory of emotional texts than SWS-rich
early sleep or wakefulness (Wagner et al., 2001). Interestingly, participants who slept
retained better memory of emotional texts when tested 4-years later (Wagner et al.,
2006), which contrasts with the previously discussed studies that failed to find such
long-term effects for non-emotional content (e.g., Gais et al., 2007). Memory for
emotional pictures was also enhanced relative to neutral pictures after REM-rich
sleep (Groch et al., 2013, 2015), while retention of contextual information (the color
of a picture frame) benefited from early SWS-rich sleep (Groch et al., 2015). These
findings support the view that REM sleep favors the consolidation of emotional con-
tent, while SWS is critical for consolidation of declarative materials regardless of emo-
tional valence. However, the conclusions that can be drawn from half-night studies
about the role of sleep stages in memory are limited, because the reduction of sleep
into SWS-rich and REM-rich periods is a huge oversimplification of the complex
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differences between early- and late-night sleep. For example, other features of sleep
vary across the ultradian cycle, such as stage 2 and sleep spindles, while the interac-
tions between sleep stages are also disrupted to varying degrees by this method of par-
tial sleep deprivation.
Several consecutive nights of insufficient sleep also appear to have little effect on
memory consolidation. Adolescents who learned paired associates prior to undergo-
ing 4 nights of chronic sleep deprivation (5, 6, 7, 8 or 9 h sleep opportunity) were
found to be unimpaired when tested after two recovery nights and also after 4 weeks,
alongside relative preservation of SWS and reductions in REM sleep (Voderholzer
et al., 2011). A more extreme manipulation, again in adolescents, showed no effect
of 7 nights of only 5 h sleep opportunity on consolidation of a prose passage (Lo et al.,
2016b), or prospective memory (Leong et al., 2018), also with relatively preserved
SWS (Ong et al., 2016). Thus, partial and chronic sleep deprivation appear to have
no long-term negative impact on memory consolidation, while the effect of 1 night
of total sleep deprivation is temporary and can be recovered after 2–3 nights of sub-
sequent sleep.
Despite this lack of lasting effects on behavioral metrics of memory consolida-
tion, human neuroimaging studies consistently suggest that underlying systems con-
solidation is affected by total sleep deprivation. Prominent models of this process
conceptualize a gradual shift in the dependence of new memories from the hippo-
campus to the neocortex (Kumaran et al., 2016; Marr, 1970; McClelland et al.,
1995). This has been observed to occur over time (Takashima et al., 2006) and sleep
is proposed to drive this process (Diekelmann and Born, 2010).
Congruent with this, retrieval of paired associates after 6 months was associated
with significantly greater activity in medial prefrontal cortex (mPFC) in participants
who slept after learning compared to those who underwent total sleep deprivation
(Gais et al., 2007). Similarly for the consolidation of emotional pictures, those
who slept the night after learning had greater mPFC activity during retrieval after
6 months, alongside enhanced connectivity between mPFC and regions including
the precuneus and amygdala (Sterpenich et al., 2009). The mPFC has thus been re-
cently implicated in integrating novel information with existing knowledge, and this
becomes progressively more important for retrieval of memories with consolidation
(Fernández and Morris, 2018). These studies support a role for sleep in this process.
Accordingly, one might expect a concomitant sleep-related decrease in hippo-
campal involvement during retrieval. Instead, those who slept in the above-
mentioned studies displayed increased hippocampal activity 2 days (Gais et al.,
2007) and 3 days after learning (Sterpenich et al., 2007), relative to those who were
sleep deprived. Others have found similar hippocampal increases after 3 days for
recall of word lists (Darsaud et al., 2011) and nonwords (Sterpenich et al., 2017).
These findings do not necessarily contradict the role of sleep in a long-term shift
from hippocampal to neocortical representations, but do suggest the role of the
hippocampus at these relatively short delays should be revised. Sleep-dependent
enhancements to behavioral measures of memory were evident in some of these
studies at shorter delays (Gais et al., 2007; Sterpenich et al., 2007, 2017), therefore
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increased hippocampal activation may simply relate to stronger memories in partic-

ipants who slept (Nyberg et al., 1996). Others have proposed that pattern
separation—the unique hippocampal ability to separate independent representations
of very similar memories—represents another plausible mechanisms that could be
enhanced across sleep (Doxey et al., 2017; Hanert et al., 2017; Poh and Cousins,
2018), which would account for the observed enhancements to both memory and
hippocampal function.
These network level changes are also highly dependent on the type of declarative
memory undergoing consolidation, as demonstrated in a pair of studies exploring
route learning in 3D environments. Initially hippocampal-dependent representations
became more dependent on the striatum in participants who slept relative to those
undergoing total sleep deprivation (Orban et al., 2006; Rauchs et al., 2008), although
no behavioral enhancements were observed when retention was measured 3 days
after learning. This is consistent with other findings from navigation studies, where
the hippocampus is initially required to form a cognitive map of the environment,
but as routes become well known there is a shift to a route following strategy that
relies on the striatum (Hartley et al., 2003).
2.2.1 Conclusion
Consolidation appears to be less vulnerable to sleep loss than encoding, since partial
deprivation has no long-term negative impact on memory consolidation, while im-
pairments associated with 1 night of total sleep deprivation can be recovered over
time. This recovery is most likely due to memories being buffered until the opportune
moment when sleep can occur (Sch€ onauer et al., 2015). Experiments that directly
assess recovery sleep are needed to test this empirically and establish the limits of
what can be recovered, in terms of the amount of information learned across
extended wakefulness, the extent of sleep deprivation and the amount of recovery
sleep.
The half-night paradigm has provided consistent evidence that REM sleep pref-
erentially consolidates declarative memories with emotional valence, while SWS is
important to consolidate memories irrespective of emotional content. This may also
account for why several nights of partial sleep deprivation do not impair consolida-
tion, since SWS is relatively unaffected by this type of sleep schedule.
There are a number of challenges to assessing sleeps contribution to the process
of systems consolidation. The observed deficits after sleep deprivation are generally
interpreted as a removal of the beneficial consolidation benefits associated with
sleep, but it is possible that the sleep deprived state itself could also impair initial
consolidation mechanisms occurring during wakefulness. Moreover, systems con-
solidation is a process lasting from days to years, but it is only feasible to deprive
sleep for a small number of nights. The studies discussed certainly provide evidence
of a role for sleep in this process, but the time course of hippocampal contributions is
currently unclear, and the discrepancy between behavioral and neuroimaging
findings at longer delays deserves further attention.
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2.3 Retrieval
Declarative memories are stored in specific neural networks, therefore it is assumed
that reactivation of a particular network leads to reexperiencing of that fact or event.
Retrieval can occur spontaneously, but for most psychological tasks it is triggered by
either an instruction to recall studied items (free recall), cued with an associated
memory (cued recall) or cued by presentation of the to-be-remembered stimulus
itself (recognition). These different forms of retrieval require varying contributions
from attention and executive function. For example, free recall is most effortful,
requiring top-down allocation of resources in order to focus and sustain attention
on the generation of cues that may trigger the memory, and also reconstruct the mem-
ory in relation to prior knowledge. A failure to retrieve may mean that the memory is
no longer available in long-term storage, or the memory trace is not accessible by
means of the cues being utilized (Tulving, 1968). It is generally accepted that suc-
cessful retrieval relies to a high degree on the similarity between encoding and
retrieval (Kent and Lamberts, 2008; Kolers, 1975; Morris et al., 1977; Tulving
and Thomson, 1973). “State dependency” is an example of this that is most pertinent
to sleep deprivation, where a persons’ mental state at retrieval should ideally match
that at encoding in order for information to be successfully retrieved (Eich, 1980).
Retrieval is a confounding factor that is sometimes controlled in sleep studies of
encoding and consolidation, but the impact of sleep loss on retrieval itself has rarely
been directly tested. One method by which retrieval has been examined after sleep
deprivation is by allowing several days of normal sleep after initial learning—with
the assumption that consolidation mechanisms have mostly taken place during this
period—followed by total sleep deprivation the night prior to the retrieval session.
The first study to use this approach allowed only 1 night of normal sleep after learn-
ing, followed by deprivation before retrieval the next morning, and found no impair-
ments on several measures of retrieval (Idzikowski, 1984). Retrieval of paired
associates were similarly unaffected when 2 nights of sleep were permitted prior
to deprivation (Sch€ onauer et al., 2015). This study also probed access to pre-existing
long-term memory by asking participants to freely recall names beginning with a
certain letter, again finding no significant deficits. Similarly, deprivation of REM
sleep by awakenings had no effect on the ability to recall factual information from
the past decade (popular culture and events), nor emotional or neutral autobiograph-
ical memories from childhood (Greenberg et al., 1983).
There is some evidence that emotion during retrieval may interact with sleep dep-
rivation. Cedernaes et al. (2015) compared memory for object locations learned prior to
a full night of sleep (8 h opportunity) or short sleep (4h opportunity). Consolidation was
unaffected by short sleep, since memory did not differ between the two conditions
when tested the following morning. However, participants then underwent a stress pro-
tocol that included several challenging tasks prior to a further object location test. This
led to a significant 15% reduction during retrieval in the short sleepers, suggesting that
a full night of sleep is necessary to facilitate retrieval during periods of subjective stress.
Prospective memory—the ability to retrieve and execute an intention at some point
in the future—has also been examined when participants are sleep deprived during
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retrieval of those intentions. Retrieval of intentions may occur spontaneously if the cue
and intention have been effectively associated with one another in long-term memory,
which would be established during encoding and consolidation, or via resource-
dependent monitoring of the environment for the relevant cue during retrieval itself.
One study compared retrieval in response to the meaning of a word cue when an on-
going task supported processing of that cue (semantic judgments of whether objects are
living or non-living) or did not (judging whether objects begin with a certain letter),
providing an indication of whether sleep loss affects retrieval when resource demands
are low or high (Grundgeiger et al., 2014). A night of sleep deprivation impaired recall
of intentions during performance of both low and high resource demanding prospec-
tive memory tasks. The authors suggest this indicates a more global impact of sleep
deprivation on cognition, rather than specific impairment to cognitively demanding
retrieval strategies that are linked to prefrontal function, since there was no increased
impairment for the more demanding task. Similarly, total sleep deprivation led to
roughly half as many participants remembering to perform an intention at a specific
time, despite the fact that the frequency with which participants checked the time
was not effected (Esposito et al., 2015; Occhionero et al., 2017). Importantly, encoding
and retrieval of intentions in each of these prospective memory studies occurred while
participants were sleep deprived, making it difficult to separate whether it is the
retrieval of intentions that is impaired or the initial formation of those intentions.
Last, false recognition with the Deese-Roediger McDermott paradigm was found
to be increased by 12% when retrieval took place after total sleep deprivation
(Diekelmann et al., 2008). The effect was abolished after administration of caffeine,
although it remains unclear whether this related to increased arousal or something
specific to the retrieval process. A follow-up study found that when tested with free
recall instead of recognition, total sleep deprivation was associated with more false
memories relative to a normal day of wakefulness. However, effects were only found
in a sub-sample of poor performers, and no significant differences were observed
when deprivation was compared to a group who slept (Diekelmann et al., 2010).
2.3.1 Conclusion
While retrieval processes have clearly not received the same attention as other stages
of long-term memory in sleep deprivation research, the few studies that have tested it
suggest it is relatively resistant to sleep loss. This stands in stark contrast to the sen-
sitivity of attention mechanisms (Lim and Dinges, 2010), which may indicate that
minimal levels of attention are required for successful retrieval to occur. The com-
plex cognitive processes involved in retrieval (e.g., attention and executive function)
could be explored further by placing retrieval under more pressure, for example via
performance of other attentionally demanding tasks alongside, and manipulating
whether ongoing tasks support the retrieval process or not. Indeed, the interaction
between retrieval and stress after sleep loss (Cedernaes et al., 2015) suggests that
retrieval processes are impaired in the presence of other cognitive pressures.
The observed increase in false memories after sleep deprivation indicates a subtle
deficit in the selection of items from those accessed during retrieval, where seman-
tically similar information is mistakenly attributed to past experience. This selection
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process is strongly linked to function in frontal regions (Thompson-Schill et al.,

1997) that are known to be affected by sleep deprivation (Krause et al., 2017). Neu-
roimaging studies that purely examine retrieval after sleep deprivation are required
to examine these relationships and provide some indication as to why retrieval is
relatively impervious to sleep deprivation while encoding is not.
3 Limitations and future directions

Sleep deprivation research has provided important insights to the memory function
of sleep, but there is clearly a gulf between understanding of mechanistic explana-
tions of deficits, and the practical relevance of such findings to common patterns of
insufficient sleep. For example, most studies have examined the effect of 1 night of
total sleep deprivation on learning and memory, but this rarely occurs outside of a
laboratory. Encoding is the most vulnerable to sleep loss, although performance
can be sustained in young adults even after 2 nights of only 4 h sleep opportunity
(Cedernaes et al., 2015). The few studies addressing more sustained deprivation have
found deficits for encoding after 5 (Cousins et al., 2017) and 4 nights of only 5 h sleep
opportunity (Cousins et al., unpublished), while similar levels of sleep loss have no
impact on consolidation (Lo et al., 2015; Voderholzer et al., 2011). Importantly,
these studies have all been conducted with adolescents, therefore it remains unclear
if findings can be generalized to adults.
In terms of learning tasks, current understanding stems from episodic memory for
words and pictures, while a large portion of declarative learning in education in-
volves memorization of detailed interrelated facts and associated skills. This type
of naturalistic learning remains unexplored, making it hard to communicate to policy
makers exactly how the impairments associated with insufficient sleep translate to
real learning. Several recent studies have explored this in relation to daytime naps
by using educationally realistic learning materials (Cousins et al., 2018) and learning
in schools (Cabral et al., 2018; Lemos et al., 2014). In future, similar applied tech-
niques should be utilized in tandem with chronic sleep restriction manipulations that
closely match typical patterns of sleep loss.
It is a somewhat surprising recent observation that behavioral impairments to
consolidation after total sleep deprivation are typically recovered after a few days,
yet neuroimaging findings suggest a lasting impact on underlying systems consoli-
dation. This may indicate that the way in which memory has been tested—via cued
recall and recognition—is not sensitive to the changes to consolidation that are
induced by sleep deprivation. Systems consolidation is thought to reflect a process
where new information becomes gradually more integrated with existing knowledge,
therefore methods that probe this integration more directly may uncover longer term
deficits associated with sleep deprivation. One method would be to test the resistance
of learned material to interference from learning-related information, which may be
more vulnerable if it has not been effectively integrated into neocortical stores.
Another approach would be to examine how the learning of new words or concepts
influences prior knowledge. For example, the lexical competition induced by
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3 Limitations and future directions 19
learning new words that are phonological neighbors of words already stored in long-
term memory (Tamminen et al., 2010).
A central limitation of sleep deprivation research is that the source of impairments
may result from the removal of the beneficial effects of sleep, and from complex
effects related to the sleep deprived state itself. These are difficult to disentangle
because sleep research is limited to comparing relative performance between groups that
are sleep deprived, have recently slept, or have been awake throughout a day without
being sleep deprived per se, but there is no neutral condition to establish ground truth.
Another challenge is to determine the relative contributions of underlying cog-
nitive processes that indirectly enable encoding, such as attention and executive
function. Many facets of attention are consistently impaired after sleep deprivation
(Lim and Dinges, 2010), and may impact on an individual’s ability to attend to stim-
uli during encoding. Simple memory tasks such as the incidental encoding of pictures
can separate attention from other encoding mechanisms to some degree, and these
still show impaired encoding for information that was attended to. While this may
be the case for encoding of simplistic stimuli such as words and pictures, it is likely
that the demand on attentional resources and executive function are higher for more
naturalistic learning tasks. Future studies could explore this further by examining
how long-term memory is influenced by different levels of processing at encoding.
Neuroimaging studies also show overlap between the networks that are affected
by sleep loss for tasks that probe different cognitive operations, including attention,
working memory and encoding. Future studies using multivariate analysis techniques
should inform as to the quality of memory representations in different areas of the brain
when encoding after sleep deprivation, and may clarify whether increases in average
activity that have been observed after sleep loss (Drummond et al., 2000, 2005) contain
additional information that can compensate for impairments. Multivariate approaches
have also shown fine grain changes in brain regions supporting declarative memory
over time (e.g., Ritchey et al., 2015), which could be used in tandem with sleep dep-
rivation to establish the role played by sleep in systems consolidation.
There are also some methodological considerations that limit our ability to deter-
mine underlying physiological mechanisms using sleep deprivation paradigms. For
example, many studies only test memory immediately after encoding, when partic-
ipants are still sleep deprived, therefore we cannot discount the influence of sleep
deprivation on retrieval or general fatigue, rather than encoding. The few studies that
control this by allowing recovery sleep before testing have observed similar perfor-
mance decrements to those that did not (Alberca-Reina et al., 2014; Cousins et al.,
2017; Tempesta et al., 2016; Yoo et al., 2007), providing some degree of confidence
that memory deficits in those studies also relate to encoding. This also indicates min-
imal influence of state dependency—that ones’ mental state should ideally match
between encoding and retrieval—although future studies should address this directly
by comparing memory with and without recovery sleep. Interactions between encod-
ing and retrieval could also be explored by comparing sleep deprivation prior to
encoding, retrieval, and a combination of the two.
Several other influential factors operating at encoding remain to be examined.
The existence of prior knowledge or “schema” enhances the encoding and
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consolidation of declarative memories (Fernández and Morris, 2018; Tse et al.,

2007), and the latter may benefit from sleep (Hennies et al., 2016). The extent to
which schema- and non-schema-related information are vulnerable to sleep loss
has yet to be determined. Fast mapping is an incidental form of learning that links
new information to prior knowledge, which is proposed to rapidly integrate informa-
tion into the neocortex and be less dependent on hippocampal processing that under-
scores most forms of declarative learning (Atir-Sharon et al., 2015). Investigation of
this learning strategy after sleep deprivation may provide insights to the vulnerability
of hippocampal and neocortical routes to learning.
Retrieval appears to be relatively resistant to sleep loss, although study of this
function is severely undeveloped. For example, the differences between types of re-
trieval (free recall, cued recall and recognition) have yet to be systematically
examined. The observed increase in false memory at retrieval (Diekelmann et al.,
2008) hints at a subtle impairment with the reconstruction of memories in relation
to prior knowledge, which could be probed further with retrieval of more complex
stimuli such as prose passages (e.g., Bartlett, 1932). There are also several
retrieval-related phenomena that may be affected by sleep loss, such as the updating
of memories with new information and the finding that retrieval produces more endur-
ing long-term memories than restudy (testing effect). It has been proposed that retrieval
acts as a further encoding opportunity (Bjork, 1975), therefore it would also be inter-
esting to determine how retrieval after sleep deprivation impacts on memory when
tested again after recovery sleep.
In conclusion, sleep deprivation research has provided the first indications that
3–4 days of chronic sleep loss have a negative impact on memory, particularly
encoding. Future studies should address this with designs that are more relevant
to common patterns of insufficient sleep and learning. Sleep deprivation paradigms
may be less optimal than more focused approaches to study sleep’s role in consol-
idation, such as targeted memory reactivation (Rudoy et al., 2009), but they still
represent a useful paradigm to assess sleep’s contribution to systems consolidation
at longer delays. This long-term reorganization of memories forms a central tenet of
influential models for sleep’s role in systems consolidation (Diekelmann and Born,
2010), but the time course of hippocampal-dependence remains to be determined,
and further work is needed to understand what it means to observe changes in net-
works supporting memory without overt behavioral effects.
References
Alberca-Reina, E., Cantero, J.L., Atienza, M., 2014. Semantic congruence reverses effects of
sleep restriction on associative encoding. Neurobiol. Learn. Mem. 110, 27–34.
Atienza, M., Cantero, J., 2008. Modulatory effects of emotion and sleep on recollection and
familiarity. J. Sleep Res. 17 (3), 285–294.
Atir-Sharon, T., et al., 2015. Decoding the formation of new semantics: MVPA investigation
of rapid neocortical plasticity during associative encoding through fast mapping. Neural
Plast. 2015, 804385.
ARTICLE IN PRESS
References 21
Atkinson, R.C., Shiffrin, R.M., 1971. The control process of short-term memory. Sci. Am.
225 (2), 1–43.
Barret, T.R., Ekstrand, B.R., 1972. Effect of sleep on memory. III. Controlling for time of day
effect. J. Exp. Psychol. 96, 321–327.
Bartlett, F.C., 1932. Remembering: An Experimental and Social Study. Cambridge
University, Cambridge.
Belal, S., Cousins, J., El-Deredy, W., Parkes, L., Schneider, J., Tsujimura, H.,
Zoumpoulaki, A., Perapoch, M., Santamaria, L., Lewis, P., 2018. Identification of memory
reactivation during sleep by EEG classification. Neuroimage 176, 203–214.
Bjork, R.A., 1975. Retrieval as a memory modifier: an interpretation of negative recency and
related phenomena. In: Solso, R. (Ed.), Information Processing and Cogntion: The Loyola
Symposium. Erlbaum, Hillsdale, NJ, pp. 123–144.
Borbely, A.A., 1982. A two process model of sleep regulation. Hum. Neurobiol. 1 (3), 195–204.
Born, J., Gais, S., 2000. REM sleep deprivation: the wrong paradigm leading to wrong
conclusions. Behav. Brain Sci. 23 (6), 912–913.
Cabral, T., et al., 2018. Post-class naps boost declarative learning in a naturalistic school
setting. N.P.J. Sci. Learn. 3 (1), 14.
Cai, D.J., et al., 2009. REM, not incubation, improves creativity by priming associative
networks. Proc. Natl. Acad. Sci. U. S. A. 106, 10130–10134.
Cain, N., Gradisar, M., 2010. Electronic media use and sleep in school-aged children and
adolescents: a review. Sleep Med. 11 (8), 735–742.
Cairney, S.A., El Marj, N., Staresina, B.P., 2018. Memory consolidation is linked to spindle-
mediated information processing during sleep. Curr. Biol. 28 (6), 1–7.
Campbell, I.G., Guinan, M.J., Horowitz, J.M., 2002. Sleep deprivation impairs long-term
potentiation in rat hippocampal slices. J. Neurophysiol. 88, 1073–1076.
Casey, S.J., et al., 2016. Slow wave and REM sleep deprivation effects on explicit and implicit
memory during sleep. Neuropsychology 30 (8), 931–945.
Cedernaes, J., Rångtell, F.H., Axelsson, E.K., Yeganeh, A., Vogel, H., Broman, J.E.,
Dickson, S.L., Schi€oth, H.B., Benedict, C., 2015. Short sleep makes declarative memories
vulnerable to stress in humans. Sleep 38 (12), 16–18.
Cedernaes, J., Sand, F., Liethof, L., Lampola, L., Hassanzadeh, S., Axelsson, E.K.,
Yeganeh, A., Ros, O., Broman, J.E., Schi€ oth, H.B., Benedict, C., 2016. Learning and
sleep-dependent consolidation of spatial and procedural memories are unaltered in young
men under a fixed short sleep schedule. Neurobiol. Learn. Mem. 131, 87–94.
Chatburn, A., Kohler, M.J., Payne, J.D., Drummond, S.P., 2017. The effects of sleep restric-
tion and sleep deprivation in producing false memories. Neurobiol. Learn. Mem.
137, 107–113.
Chee, M.W.L., Chuah, Y.M.L., 2007. Functional neuroimaging and behavioral correlates of
capacity decline in visual short-term memory after sleep deprivation. Proc. Natl. Acad.
Sci. U. S. A. 104 (22), 9487–9492.
Chernik, D.A., 1972. Effect of REM sleep deprivation on learning and recall by humans.
Percept. Motor Skill. 34 (1), 283–294.
Chuah, L.Y.M., Chong, D.L., Chen, A.K., Rekshan III, W.R., Tan, J.C., Zheng, H.,
Chee, M.W., 2009. Donepezil improves episodic memory in young individuals vulnerable
to the effects of sleep deprivation. Sleep 32 (8), 999–1010.
Cohen, N.J., Squire, L.R., 1980. Preserved learning and retention of pattern-analyzing
skill in amnesia: dissociation of knowing how and knowing that. Science 210 (4466),
207–210.
ARTICLE IN PRESS
Cousins, J.N., El-Deredy, W., Parkes, L.M., Hennies, N., Lewis, P.A., 2014. Cued memory
reactivation during slow-wave sleep promotes explicit knowledge of a motor sequence.
J. Neurosci. 34 (48), 15870–15876.
Cousins, J.N., Sasmita, K., Chee, M.W.L., 2017. Memory encoding is impaired after multiple
nights of partial sleep restriction. J. Sleep Res. 27 (1), 138–145.
Cousins, J.N., Wong, K.F., Raghunath, B.L., Look, C., Chee, M.W.L., 2018. The long-term
memory benefits of a daytime nap compared to cramming. Sleep 42, zsy207.
Cousins, J.N., van Rijn, E., Ong, J.L., Chee, M.W.L., 2019. A split-sleep schedule rescues
short-term topographical memory after multiple nights of sleep restriction. Sleep 42, zsz018.
Craik, F.I.M., Lockhart, R.S., 1972. Levels of processing: a framework for memory research.
J. Verb. Learn Verb. B 11 (6), 671–684.
Crowley, S.J., Acebo, C., Carskadon, M.A., 2007. Sleep, circadian rhythms, and delayed phase
in adolescence. Sleep Med. 8 (6), 602–612.
Curcio, G., Ferrara, M., De Gennaro, L., 2006. Sleep loss, learning capacity and academic per-
formance. Sleep Med. Rev. 10 (5), 323–337.
Darsaud, A., Dehon, H., Lahl, O., Sterpenich, V., Boly, M., Dang-Vu, T., Desseilles, M., 2011.
Does sleep promote false memories? J. Cogn. Neurosci. 23 (1), 26–40.
de Vivo, L., et al., 2017. Ultrastructural evidence for synaptic scaling across the wake/sleep
cycle. Science 355 (6324), 507–510.
Deliens, G., Gilson, M., et al., 2013a. Sleep unbinds memories from their emotional context.
Cortex 49 (8), 2221–2228.
Deliens, G., Schmitz, R., et al., 2013b. Does recall after sleep-dependent memory consolida-
tion reinstate sensitivity to retroactive interference? PLoS One 8 (7), e68727.
Diekelmann, S., Born, J., 2010. The memory function of sleep. Nat. Rev. Neurosci. 11 (2),
114–126.
Diekelmann, S., Diekelmann, S., Landolt, H.P., Lahl, O., Born, J., Wagner, U., 2008. Sleep
loss produces false memories. PLoS One 3 (10), e3512.
Diekelmann, S., Born, J., Wagner, U., 2010. Sleep enhances false memories depending on
general memory performance. Behav. Brain Res. 208, 425–429.
Diekelmann, S., Wilhelm, I., Wagner, U., Born, J., 2013a. Sleep improves prospective remember-
ing by facilitating spontaneous-associative retrieval processes. PLoS One 8 (10), 1–10.
Diekelmann, S., Wilhelm, I., Wagner, U., Born, J., 2013b. Sleep to implement an intention.
Sleep 36 (1), 149–153.
Dolcos, F., LaBar, K.S., Cabeza, R., 2005. Remembering one year later: role of the amygdala
and the medial temporal lobe memory system in retrieving emotional memories. Proc.
Natl. Acad. Sci. U. S. A. 102 (7), 2626–2631.
Doxey, C.R., et al., 2017. The effects of sleep on the neural correlates of pattern separation.
Hippocampus 28 (2), 108–120.
Drosopoulos, S., Wagner, U., Born, J., 2005. Sleep enhances explicit recollection in recogni-
tion memory. Learn. Mem. 12 (1), 44–51.
Drummond, S.P., et al., 2000. Altered brain response to verbal learning following sleep dep-
rivation. Nature 403 (6770), 655–657.
Drummond, S.P.A., et al., 2005. Compensatory recruitment after sleep deprivation and the
relationship with performance. Psychiat. Res. Neuroim. 140 (3), 211–223.
Eich, J.E., 1980. The cue-dependent nature of state-dependent retrieval. Mem. Cognit. 8 (2),
157–173.
Ellenbogen, J.M., et al., 2009. The sleeping brain’s influence on verbal memory: boosting
resistance to interference. PLoS One 4 (1), 2–5.
ARTICLE IN PRESS
References 23
Empson, J.A.C., Clarke, P.R.F., 1970. Rapid eye movements and remembering. Nature
227 (5255), 287–288.
Erk, S., et al., 2003. Emotional context modulates subsequent memory effect. Neuroimage
18 (2), 439–447.
Esposito, M.J., Occhionero, M., Cicogna, P., 2015. Sleep deprivation and time-based prospec-
tive memory. Sleep 38 (11), 1823–1826.
Feld, L.D., Shusterman, A., 2015. Into the pressure cooker: student stress in college prepara-
tory high schools. J. Adolesc. 41, 31–42.
Fernández, G., Morris, R.G.M., 2018. Memory, novelty and prior knowledge. Trends
Neurosci. 41 (10), 654–659.
Ferrara, M., et al., 2006. The role of sleep in the consolidation of route learning in humans:
a behavioural study. Brain Res. Bull. 71, 4–9.
Ferrara, M., et al., 2008. Sleep to find your way: the role of sleep in the consolidation of mem-
ory for navigation in humans. Hippocampus 18, 844–851.
Frankland, P.W., Bontempi, B., 2005. The organisation of recent and remote memories. Nat.
Rev. Neurol. 6 (2), 119.
Frenda, S.J., et al., 2014. Sleep deprivation and false memories. Psychol. Sci. 25 (9),
1674–1681.
Gais, S., Born, J., 2004. Low acetylcholine during slow-wave sleep is critical for declarative
memory consolidation. Proc. Natl. Acad. Sci. U. S. A. 101 (7), 2140–2144.
Gais, S., Lucas, B., Born, J., 2006. Sleep after learning aids memory recall. Learn. Mem.
13 (3), 259–262.
Gais, S., et al., 2007. Sleep transforms the cerebral trace of declarative memories. Proc. Natl.
Acad. Sci. U. S. A. 104 (47), 18778–18783.
Genzel, L., et al., 2009. Slow wave sleep and REM sleep awakenings do not affect sleep
dependent memory consolidation. Sleep 32 (3), 302–310.
Gillen-O’Neel, C., Huynh, V.W., Fuligni, A.J., 2013. To study or to sleep? The academic costs
of extra studying at the expense of sleep. Child Dev. 84 (1), 133–142.
Giuditta, A., 2014. Sleep memory processing: the sequential hypothesis. Front. Sys. Neurosci.
8, 1–8.
Greenberg, R., et al., 1983. Memory, emotion, and REM sleep. J. Abnorm. Psychol. 92 (3),
378–381.
Grieser, C., Greenberg, R., Harrison, R.H., 1972. The adaptive function of sleep: the differ-
ential effects of sleep and dreaming on recall. J. Abnorm. Psychol. 80 (3), 280.
Griessenberger, H., et al., 2012. Consolidation of temporal order in episodic memories. Biol.
Psychol. 91 (1), 150–155.
Groch, S., Wilhelm, I., Diekelmann, S., Born, J., 2013. The role of REM sleep in the proces-
sing of emotional memories: evidence from behavior and event-related potentials. Neuro-
biol. Learn. Mem. 99, 1–9.
Groch, S., et al., 2015. Dissociating the contributions of slow-wave sleep and rapid eye
movement sleep to emotional item and source memory. Neurobiol. Learn. Mem.
122, 122–130.
Grundgeiger, T., Bayen, U.J., Horn, S.S., 2014. Effects of sleep deprivation on prospective
memory. Memory 22 (6), 679–686.
Hanert, A., Weber, F.D., Pedersen, A., Born, J., Bartsch, T., 2017. Sleep in humans stabilizes
pattern separation performance. J. Neurosci. 37 (50), 12238–12246.
Harrison, Y., Horne, J.A., 2000. Sleep loss and temporal memory. Q. J. Exp. Psychol. A.
53 (1), 271–279.
ARTICLE IN PRESS
Hartley, T., Maguire, E.A., Spiers, H.J., Burgess, N., 2003. The well-worn route and the path
less traveled: distinct neural bases of route following and wayfinding in humans. Neuron
37, 877–888.
Hennies, N., Ralph, M.A.L., Kempkes, M., Cousins, J.N., Lewis, P.A., 2016. Sleep spindle
density predicts the effect of prior knowledge on memory consolidation. J. Neurosci.
36 (13), 3799–3810.
Hirshkowitz, M., et al., 2015. National sleep foundation’s sleep time duration recommenda-
tions: methodology and results summary. SLEH 1 (1), 40–43.
Hockey, G.R., Davies, S., Gray, M.M., 1972. Forgetting as a function of sleep at different
times of day. Q. J. Exp. Psychol. 24 (4), 386–393.
Idzikowski, C., 1984. Sleep and memory. Br. J. Psychol. 75 (4), 439–449.
Jenkins, J.G., Dallenbach, K.M., 1924. Obliviscence during sleep and waking. Am. J. Psychol.
35 (4), 605–612.
Jonelis, M.B., et al., 2012. Age-related influences of prior sleep on brain activation during
verbal encoding. Front. Neurol. 3, 49.
Kaida, K., Niki, K., Born, J., 2015. Role of sleep for encoding of emotional memory. Neuro-
biol. Learn. Mem. 121, 72–74.
Kent, C., Lamberts, K., 2008. The encoding-retrieval relationship: retrieval as mental
simulation. Trends Cogn. Sci. 12 (3), 92–98.
Kolers, P.A., 1975. Addendum to “remembering operations” Mem. Cognit. 3 (1), 29–30.
Kopasz, M., Loessl, B., Valerius, G., 2010. Sleep deprivation: no persisting effect of partial
sleep curtailment on cognitive performance and declarative memory recall in adolescents.
J. Sleep Res. 19 (1), 71–79.
Krause, A.J., Simon, E.B., Mander, B.A., Greer, S.M., Saletin, J.M., Goldstein-Piekarski,
A.N., Walker, M.P., 2017. The sleep-deprived human brain. Nat. Rev. Neurosci.
18 (7), 404.
Kreutzmann, J.C., Havekes, R., Abel, T., Meerlo, P., 2015. Sleep deprivation and hippocampal
vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function.
Neuroscience 309, 173–190.
Kumaran, D., Hassabis, D., McClelland, J.L., 2016. What learning systems do intelligent
agents need? Complementary learning systems theory updated. Trends Cogn. Sci.
20 (7), 512–534.
Kuriyama, K., Soshi, T., Kim, Y., 2010. Sleep deprivation facilitates extinction of implicit fear
generalization and physiological response to fear. Biol. Psychiatry 68 (11), 991–998.
Landmann, N., et al., 2016. Sleep strengthens but does not reorganize memory traces in a
verbal creativity task. Sleep 39 (3), 705–713.
Lemos, N., Weissheimer, J., Ribeiro, S., 2014. Naps in school can enhance the duration of
declarative memories learned by adolescents. Front. Sys. Neurosci. 8, 103.
Leong, R.L.F., et al., 2018. Multiple nights of partial sleep deprivation do not affect prospec-
tive remembering at long delays. Sleep Med. 44, 19–23.
Lewis, P.A., Durrant, S.J., 2011. Overlapping memory replay during sleep builds cognitive
schemata. Trends Cogn. Sci. 15 (8), 343–351.
Lim, J., Dinges, D.F., 2010. A meta-analysis of the impact of short-term sleep deprivation on
cognitive variables. Psychol. Bull. 136 (3), 375–389.
Lin, C.C., Yang, C.M., 2014. Evidence of sleep-facilitating effect on formation of novel
semantic associations: an event-related potential (ERP) study. Neurobiol. Learn. Mem.
116, 69–78.
ARTICLE IN PRESS
References 25
Lo, J.C., et al., 2015. Cognitive performance, sleepiness, and mood in partially sleep deprived
adolescents: the need for sleep study. Sleep 39 (03), 687–698.
Lo, J.C., et al., 2016a. Sleep deprivation increases formation of false memory. J. Sleep Res.
25 (6), 673–682.
Lo, J.C., Bennion, K.A., Chee, M.W.L., 2016b. Sleep restriction can attenuate prioritization
benefits on declarative memory consolidation. J. Sleep Res. 25 (6), 664–672.
Mander, B.A., Santhanam, S., Saletin, J.M., Walker, M.P., 2011. Wake deterioration and sleep
restoration of human learning. Curr. Biol. 21 (5), R183–R184.
Marr, D., 1970. A theory for cerebral neocortex. Proc. R. Soc. London B Biol. 176 (1043),
161–234.
Massar, S.A.A., et al., 2017. Poor habitual sleep efficiency is associated with increased car-
diovascular and cortisol stress reactivity in men. Psychoneuroendocrinology 81, 151–156.
McClelland, J.L., McNaughton, B.L., O’Reilly, R.C., 1995. Why there are complementary
learning systems in the hippocampus and neocortex: insights from the successes and
failures of connectionist models of learning and memory. Psychol. Rev. 102 (3), 419.
McGaugh, J.L., 2000. Memory—a century of consolidation. Science 287 (5451), 248–251.
Mograss, M.A., et al., 2009. The effects of total sleep deprivation on recognition memory
processes: a study of event-related potential. Neurobiol. Learn. Mem. 91 (4), 343–352.
Morgenthaler, J., Wiesner, C.D., Hinze, K., Abels, L.C., Prehn-Kristensen, A., Goder, R.,
2014. Selective REM-sleep deprivation does not diminish emotional memory consolida-
tion in young healthy subjects. PLoS One 9 (2), e89849.
Morris, G.O., Williams, H.L., Lubin, A., 1960. Misperception and disorientation during sleep
deprivation. Arch. Gen. Psychiatry 2 (3), 247–254.
Morris, C.D., Bransford, J.D., Franks, J.J., 1977. Levels of processing versus transfer appro-
priate processing. J. Mem. Lang. 16 (5), 519.
M€uller, G.E., Pilzecker, A., 1900. Experimentelle Beitr€age Zur Lehre Vom Ged€achtniss.
vol. 1. JA Barth.
Ngo, H.V.V., et al., 2013. Auditory closed-loop stimulation of the sleep slow oscillation
enhances memory. Neuron 78, 545–553.
Nyberg, L., et al., 1996. Activation of medial temporal structures during episodic memory
retrieval. Nature 380 (6576), 715–717.
Occhionero, M., Cicogna, P., Esposito, M.J., 2017. The effect of sleep loss on dual time-based
prospective memory tasks. Am. J. Psychol. 130 (1), 93–103.
Ong, J.L., Lo, J.C., Gooley, J.J., Chee, M.W.L., 2016. EEG changes across multiple nights of
sleep restriction and recovery in adolescents : the need for sleep study. Sleep 39 (6),
1233–1240.
Ong, J.L., Patanaik, A., Chee, N.I., Lee, X.K., Poh, J.H., Chee, M.W., 2018. Auditory stim-
ulation of sleep slow oscillations modulates subsequent memory encoding through altered
hippocampal function. Sleep 41 (5), zsy031.
Orban, P., et al., 2006. Sleep after spatial learning promotes covert reorganization of brain
activity. Proc. Natl. Acad. Sci. U. S. A. 103, 7124–7129.
Plihal, W., Born, J., 1997. Effects of early and late nocturnal sleep on declarative and proce-
dural memory. J. Cogn. Neurosci. 9 (4), 534–547.
Poh, J.-H., Chee, M.W.L., 2017. Degradation of cortical representations during encoding
following sleep deprivation. Neuroimage 153, 131–138.
Poh, J.-H., Cousins, J.N., 2018. Is there a role for pattern separation during sleep? J. Neurosci.
38 (17), 4062–4064.
ARTICLE IN PRESS
Porcheret, K., et al., 2015. Psychological effect of an analogue traumatic event reduced by
sleep deprivation. Sleep 38 (7), 1017–1025.
Rasch, B., Born, J., 2014. About sleep’s role in memory. Psychol. Forsch. 27, 320–323.
Rauchs, G., et al., 2004. Consolidation of strictlyepisodic memories mainly requires rapid eye
movement sleep. Sleep 27 (3), 395–401.
Rauchs, G., et al., 2008. Sleep modulates the neural substrates of both spatial and contextual
memory consolidation. PLoS One 3 (8), e2949.
Rauchs, G., et al., 2011. Sleep contributes to the strengthening of some memories over others,
depending on hippocampal activity at learning. J. Neurosci. 31 (7), 2563–2568.
Ritchey, M., et al., 2015. Delay-dependent contributions of medial temporal lobe regions to
episodic memory retrieval. eLife 2015 (4), 1–19.
Robertson, E.M., Pascual-leone, A., Miall, R.C., 2004. Current concepts in procedural consol-
idation. Nat. Rev. Neurosci. 5, 1–7.
Roediger, H.L., McDermott, K.B., 1995. Creating false memories: remembering words not
presented in lists. J. Exp. Psychol. Learn. 21 (4), 803.
Rudoy, J.D., et al., 2009. Strengthening individual memories by reactivating them during
sleep. Science 326 (5956), 1079.
Rupp, T.L., Wesensten, N.J., Balkin, T.J., 2012. Trait-like vulnerability to total and partial
sleep loss. Sleep 35 (8), 1163–1172.
Saletin, J.M., Van Der Helm, E., Walker, M.P., 2013. Structural brain correlates of human
sleep oscillations. Neuroimage 83C, 658–668.
Saletin, X.J.M., et al., 2016. Human hippocampal structure: a novel biomarker predicting mne-
monic vulnerability to and recovery from sleep deprivation. J. Neurosci. 36 (8),
2355–2363.
Sch€onauer, M., Gr€atsch, M., Gais, S., 2015. Evidence for two distinct sleep-related long-term
memory consolidation processes. Cortex 63, 68–78.
Sch€onauer, M., et al., 2017. Decoding material-specific memory reprocessing during sleep in
humans. Nat. Commun. 8, 15404.
Smith, C., 1995. Sleep states and memory processes. Behav. Brain Res. 69 (1–2), 137–145.
Sterpenich, V., et al., 2007. Sleep-related hippocampo-cortical interplay during emotional
memory recollection. PLoS Biol. 5 (11), 2709–2722.
Sterpenich, V., et al., 2009. Sleep promotes the neural reorganization of remote emotional
memory. J. Neurosci. 29 (16), 5143–5152.
Sterpenich, V., Ceravolo, L., Schwartz, S., 2017. Sleep deprivation disrupts the contribution of
the hippocampus to the formation of novel lexical associations. Brain Lang. 167, 61–71.
Stickgold, R., Walker, M.P., 2013. Sleep-dependent memory triage: evolving generalization
through selective processing. Nat. Neurosci. 16 (2), 139–145.
Takashima, A., Petersson, K.M., Rutters, F., Tendolkar, I., Jensen, O., Zwarts, M.J., …
Fernandez, G., 2006. Declarative memory consolidation in humans: a prospective
functional magnetic resonance imaging study. Proc. Natl. Acad. Sci. U. S. A. 103 (3),
756–761.
Tamminen, J., Payne, J.D., Stickgold, R., Wamsley, E.J., Gaskell, M.G., 2010. Sleep spindle
activity is associated with the integration of new memories into existing knowledge.
J. Neurosci. 30 (43), 14356–14360.
Tempesta, D., et al., 2016. The effect of sleep deprivation on the encoding of contextual and
non-contextual aspects of emotional memory. Neurobiol. Learn. Mem. 131, 9–17.
Tempesta, D., et al., 2017. The effect of sleep deprivation on retrieval of emotional memory: a
behavioural study using film stimuli. Exp. Brain Res. 235 (10), 3059–3067.
ARTICLE IN PRESS
References 27
Thompson-Schill, S.L., D’Esposito, M., Aguirre, G.K., Farah, M.J., 1997. Role of left inferior
prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc. Natl. Acad. Sci.
U. S. A. 94 (26), 14792–14797.
Tilley, A.J., Empson, J.A.C., 1978. REM sleep and memory consolidation. Biol. Psychol.
6 (4), 293–300.
Tononi, G., Cirelli, C., 2014. Sleep and the price of plasticity: from synaptic and cellular
homeostasis to memory consolidation and integration. Neuron 81 (1), 12–34.
Tse, D., et al., 2007. Schemas and memory consolidation. Science 316 (2007), 76–82.
Tucker, M., Fishbein, W., 2009. The impact of sleep duration and subject intelligence on
declarative and motor memory performance: how much is enough? J. Sleep Res.
18 (3), 304–312.
Tulving, E., 1968. Theoretical issues in free recall. In: Dixon, T.R., Horton, D.L. (Eds.),
Verbal Behavior and General Behavior Theory. Prentice-Hall, Englewood Cliffs, NJ,
pp. 2–36.
Tulving, E., Thomson, D.M., 1973. Encoding specificity and retrieval processes in episodic
memory. Psychol. Rev. 80 (5), 352–373.
Van Der Werf, Y.D., et al., 2009. Sleep benefits subsequent hippocampal functioning. Nat.
Neurosci. 12, 122–123.
Van Dongen, H.P.A., et al., 2003. The cumulative cost of additional wakefulness: dose-
response effects on neurobehavioral functions and sleep physiology from chronic sleep
restriction and total sleep deprivation. Sleep 26, 117–126.
Van Dongen, H.P.A., Baynard, M.D., Maislin, G., Dinges, D.F., 2004. Systematic interindi-
vidual differences in neurobehavioral impairment from sleep loss: evidence of trait-like
differential vulnerability. Sleep 27 (3), 423–433.
Van Dongen, E.V., et al., 2012. Memory stabilization with targeted reactivation during human
slow-wave sleep. Proc. Natl. Acad. Sci. U. S. A. 109 (26), 10575–10580.
Voderholzer, U., et al., 2011. Sleep restriction over several days does not affect long-term
recall of declarative and procedural memories in adolescents. Sleep Med. 12 (2), 170–178.
Wagner, U., Gais, S., Born, J., 2001. Emotional memory formation is enhanced across sleep
intervals with high amounts of rapid eye movement sleep. Learn. Mem. 8 (2), 112–119.
Wagner, U., et al., 2006. Brief sleep after learning keeps emotional memories alive for years.
Biol. Psychiatry 60, 788–790.
Walker, M.P., van Der Helm, E., 2009. Overnight therapy? The role of sleep in emotional brain
processing. Psychol. Bull. 135 (5), 731.
Xue, G., et al., 2010. Greater neural pattern similarity across repetitions is associated with
better memory. Science 330 (6000), 97–101.
Yaroush, R., Sullivan, M.J., Ekstrand, B.R., 1971. Effect of sleep on memory: II. Differential
effect of the first and second half of the night. J. Exp. Psychol. 88 (3), 361.
Yoo, S.-S., et al., 2007. A deficit in the ability to form new human memories without sleep.
Nat. Neurosci. 10 (3), 385–392.

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ARTICLE IN PRESS

The impact of sleep

2 Progress in brain research: Sleep deprivation cognition

2 Memory stages and sleep

2 Memory stages and sleep 3

4 Progress in brain research: Sleep deprivation cognition

2 Memory stages and sleep 5

6 Progress in brain research: Sleep deprivation cognition

2 Memory stages and sleep 7

8 Progress in brain research: Sleep deprivation cognition

This hippocampal dysfunction after sleep loss is also observed in animal

2 Memory stages and sleep 9

10 Progress in brain research: Sleep deprivation cognition

stabilizing and reorganizing memories in the brain. Recently developed techniques

2 Memory stages and sleep 11

Sleep is also proposed to preferentially consolidate emotional memories while

12 Progress in brain research: Sleep deprivation cognition

2 Memory stages and sleep 13

14 Progress in brain research: Sleep deprivation cognition

2 Memory stages and sleep 15

increased hippocampal activation may simply relate to stronger memories in partic-

16 Progress in brain research: Sleep deprivation cognition

2 Memory stages and sleep 17

18 Progress in brain research: Sleep deprivation cognition

process is strongly linked to function in frontal regions (Thompson-Schill et al.,

3 Limitations and future directions

3 Limitations and future directions 19

20 Progress in brain research: Sleep deprivation cognition

consolidation of declarative memories (Fernández and Morris, 2018; Tse et al.,

22 Progress in brain research: Sleep deprivation cognition

24 Progress in brain research: Sleep deprivation cognition

26 Progress in brain research: Sleep deprivation cognition

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