Download Memory Processing in Relation to Sleep

Memory Processing in Relation
to Sleep
Philippe Peigneux and Carlyle Smith
Abstract
Although each of us empirically recognizes the utmost importance of sleep for the quality of our everyday life, its functions
have long remained shrouded in mystery. Beyond its putative
physiologic functions, there is now growing evidence that
sleep plays a prominent role in brain plasticity and in memoryconsolidation processes. According to this proposal, memory
traces formed during a learning episode are not immediately
stored in their definitive form. Rather, they are initially kept
in a labile, fragile state, during which they can be easily disrupted. Over time and especially during sleep, they subsequently undergo a series of transformations during which
they will be consolidated and fully integrated into long-term
memory. In this chapter, we present experimental data that
provide support for the hypothesis that sleep exerts a promoting effect on plastic processes of memory consolidation. Some
studies have assessed the effects of posttraining sleep deprivation on memory consolidation and on the reorganization of
the neural substrates of long-term memories. Others have
investigated the effects of learning on posttraining sleep and
In 1867, Hervey de Saint Denys, fascinated by his dreams
since the age of 14, published Les Rêves et les Moyens de les
Diriger.1 In his book, he reported a series of ingenious
experiments showing that experienced events are incorporated into our dreams, in which they can be combined to
create original associations between “memory images” of
the past. Hence, he strongly opposed the idea that sleep
may be a sudden drop in a state of cognitive “non-being”
in which our resting brain is disconnected. On the contrary, he claimed that “a sleep without dreams cannot exist,
just as a wake state without mentation does not exist.”
Besides dreaming activity, however, addressed in Section
7 of this book, we know that the sleeping brain houses a
wide set of cognitive processes, including the ongoing
treatment of elaborated external stimuli, the revival of
experiences, and last, but not least, the consolidation of
new information in memory. Interestingly, recognition
that persistence of mental activity in the sleeper may be an
integral part of the physiologic processes that subtend
memory consolidation arose only in the last quarter of the
20th century. The hypothesis had to wait till now to receive
widespread acknowledgement, as illustrated by the fact
that for the first time a chapter devoted to sleep in relation
to memory has been introduced in this fifth edition of
Principles and Practices in Sleep Medicine.
This chapter introduces the issues surrounding the role
that sleep may play in memory consolidation, focusing on
human data. Reviews about relationships between sleep
and memory in animals are addressed can be found elsewhere.2-4 We will here outline key findings and milestones
in probing the sleep-for-memory hypothesis, as well as
ongoing debates and thoughtful questions that remain.
Chapter
29
reexpression of behavior-specific neural patterns during posttraining sleep, and still others have probed the effects of
within-sleep stimulation on sleep patterns and overnight memories. Besides-demonstrating a role of sleep in memory consolidation processes, these studies have also indicated that
sleep stages are functionally different, in that they may subserve distinct memory processes. Available evidence reveals
complex interactions between sleep and memory systems, in
agreement with the fact that memory is a complex construct
of specialized memory subdomains, and that sleep is composed of distinct stages characterized by specific physiologic
mechanisms. Despite advances that have refined our understanding of the relationships between sleep and cognitive processes, the underlying mechanisms still remain to be fully
elucidated. Further steps are now required to understand how
sleep disorders and pathologies accompanied by sleep disturbances affect cognitive functions, and especially learning and
memory consolidation in humans, eventually leading to remedial interventions.
Before approaching the subject, however, we will briefly
introduce the concepts of memory consolidation and
memory systems in humans. Previous chapters have shown
that sleep is a multidimensional state of vigilance, composed of rapid eye movement (REM) and non-REM
(NREM) episodes that present distinctive features and rely
on specific neuroanatomic substrates.4 From both cognitive and neurophysiologic perspectives, memory is not a
unitary phenomenon. Rather, memory should be seen as a
generic concept for information storage, encompassing
a series of specific subdomains.5 Consequently, the interaction between multidimensional states of sleep and distinctive memory systems makes it logical that not all sleep
manipulations will have the same impact on performance,
depending on the various parameters embedded in the
memory task.2,6,7 We will examine the growing number of
behavioral studies that have enlightened our understanding of the role played by sleep episodes in memory
consolidation. The rapid evolution of neurophysiologic
techniques and analytical approaches allows scrutiny of the
complex relations between cognitive processes and their
underlying neural substrates. Part of this chapter will focus
on the neurophysiologic mechanisms acting in sleep to
support, or at least favor, memory consolidation processes.
Molecular biology of memory consolidation is beyond the
scope of this chapter and is reviewed elsewhere.4 The relationship between consolidation of learning and sleep is a
crucial issue because memory is at the root of most of our
daily behaviors, such as simple skill acquisition (e.g., typewriting), sophisticated operational procedures (e.g., using
computer-based systems), and keeping track of personal
events and relationships.
335
Kryger_6453_Ch 29_main.indd 335
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336 PART I / Section 4 • Physiology in Sleep
MEMORY SYSTEMS AND MEMORY
CONSOLIDATION
We are able to learn, store, and remember various types
of information in different ways and for variable periods
of time, from conscious acquisition strategies to incidental
detection of environmental events. Cerebral damage can
selectively alter some of these processes while leaving
others undisturbed. These simple observations have led to
the proposal that memory is not a unitary phenomenon
but rather a complex construct of more or less specialized
memory subdomains.5 First, a seminal distinction that
dates back to William James is made between short- and
long-term memory stores. The former is dedicated to the
temporary storage of volatile information for up to seconds,
whereas the latter, the main focus in this chapter, houses
potentially lasting information that is deemed consolidated
and less susceptible to disruption. Long-term memories in
humans may further belong to multiple systems, primarily
delineated between declarative and nondeclarative memories (Fig. 29-1).
Distinguishing features of declarative memory are that
information is easily accessible to verbal description and
that encoding or retrieval is usually carried out explicitly—
that is, the subject is aware that the stored information
exists and is being accessed. Declarative memory is further
composed of semantic and episodic memory components.
Semantic memory is the receptacle for our general knowledge about the world, regardless of the spatiotemporal
context of knowledge acquisition (e.g., we know that Paris
is the capital of France, and that fuel is combustible, but
we are probably unable to recollect how and when we
learned these facts). Episodic memory, on the other hand,
refers to the system that stores events and information
along with their contextual location in time and space (e.g.,
I can vividly remember having visited the British Museum
with my cousin on a rainy day in the fall of 1993).
Declarative memory
Emotion
Episodic
memory
Semantic
memory
Personally
experienced events,
spatial and temporal
memory features
Facts and concepts
about the world,
general knowledge
Nondeclarative
memory
L
Skills and
habits
Priming
Conditioning
“How to” knowledge,
perceptual, motor
and cognitive abilities
Processing
facilitation after
prior exposure
Elementary
associative
memory
Figure 29-1 Schematic organization of long-term memory
systems.
Kryger_6453_Ch 29_main.indd 336
Distinctive features of nondeclarative memories are that
they are not easily accessible to verbal description and can
be acquired and reexpressed implicitly. Thus, our behavioral performance can be affected by the new memory even
if we are not consciously aware that new information has
been encoded or is being retrieved. Memory abilities
aggregated under the nondeclarative label also gather different forms: skills, habits, priming, and conditioning.
Although grouped under the nondeclarative label, these
various processes are subtended by distinct neuroanatomic
substrates in both humans and animals, further suggesting
their relative independence.5
Besides the transverse division between long-term
memory subsystems proposed by these influential models,
there is a dynamic longitudinal process. Newly acquired
information is not immediately stored at the time of
learning in its final form, if such a stable state exists.
Rather, memories undergo a series of transformations
over hours, days, or even years, during which time they
are gradually incorporated into preexisting sets of mnemonic representations,8-10 or are subjected to forgetting.11
This is the concept of memory consolidation, which can
be defined as the time-dependent process that converts
labile memory traces into more permanent or enhanced
forms.12 These transformations are made possible by our
brain plasticity—that is, the capacity of the brain to modify
its structure and function over time, within certain boundaries.13 Eventually, time-dependent processes of consolidation and the ensuing robust memory trace will enduringly
adjust the behavioral responses to the recent environmental changes, thereby enlarging the organism’s behavioral repertoire.14
Scientific evidence suggests that sleep and the associated
processes of brain plasticity4 are major players in timedependent processes of memory consolidation, acting as
key constituents in the chain of transformations that help
integrate information for the long term. Furthermore,
these studies suggest that distinct sleep stages may have
distinct memory-related functions, which has been interpreted in two different but nonexclusive ways. According
to the dual-process hypotheses, REM and NREM sleep
act differently on memory traces depending on the memory
system or process to which they belong. For example, it
has been proposed that slow-wave sleep (SWS)—the
deepest stage of NREM sleep—facilitates consolidation of
declarative and spatial memories, whereas REM sleep
facilitates consolidation of nondeclarative memories.15,16
Another interpretation is that particular sequences of sleep
states reflect the succession of brain processing events supporting memory consolidation.17 An example is the proposal that REM sleep actively consolidates or integrates
complex associative information, whereas NREM sleep
passively prevents retroactive interference of recently
acquired complex associative information.18 In this view,
SWS and REM sleep play complementary roles and have
to act serially to consolidate the new memory trace, in a
double-step process.19,20 Both approaches assume that it is
sleep on the first posttraining night that is important for
memory consolidation. Nonetheless, it would be premature to claim that only sleep may achieve the necessary
conditions to consolidate novel memories in the nervous
system, as both sleeplike cognitive and neural processes of
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memory consolidation have also been observed during
wakefulness.21-23
METHODS FOR STUDYING THE
ROLE OF SLEEP FOR MEMORY
CONSOLIDATION
Three experimental approaches have been used to test the
hypothesis that sleep exerts a favorable or promoting effect
on memory consolidation. These approaches focus on (1)
the effects of posttraining sleep deprivation on memory
consolidation and on the reorganization of the neural substrates of long-term memories, (2) the effects of learning
on posttraining sleep and reexpression of behavior-specific
neural patterns during posttraining sleep, or (3) the effects
of within-sleep stimulation on sleep patterns and overnight
memories.
Posttraining Sleep Deprivation
The first and probably most ancient line of investigation
has probed the putatively detrimental effect of sleep deprivation on the night after learning, based on the assumption
that memory performance over the long term will be better
if participants are allowed to sleep after learning rather
than being deprived of sleep. In classic procedures, subjects
learn new material. Afterward, some participants are
allowed to sleep normally whereas others either do not
sleep at all (total sleep deprivation), are awakened at the
onset of occurrences of the sleep stage under study (selective sleep deprivation), are kept awake during the period
of the night in which the sleep stage is predominant (partial
sleep deprivation), or have a shortened sleep duration
(sleep restriction). Finally, prenight and postnight memory
measures are compared between sleeping and sleepdeprived subgroups, either the next day or several days
later. Jenkins and Dalenbach24 used this approach about 85
years ago and found that the forgetting curve for newly
learned verbal material described by the German psychologist Ebinghaus was significantly dampened by the presence of an intermediate period of sleep. Nonetheless, they
did not attribute this effect to a specific role of sleep per
se in memory processing but merely to the protective role
that sleep may have against “interference, inhibition, or
obliteration of the old by the new.”24 However, this
hypothesis of a purely passive role for sleep in memory
processes has been challenged by studies of selective sleep
deprivation that attribute a specific role to REM sleep in
memory storage and consolidation, in both human and
animal species.25 Also, it was demonstrated that memory
over an interval with relatively high amounts of stage 4
sleep (i.e., in the first half of the night) was superior to
memory over an interval with relatively high amounts of
REM sleep (i.e., in the second half of the night).26 This
seemingly apparent contradiction was resolved later, with
the demonstration that recall of paired-associate lists was
significantly better after sleep than wakefulness in the first
part of the night only, whereas consolidation of mirrortracing skills specifically benefited from sleep in the second
part of the night.15 Results showed that memories belonging to the declarative and nondeclarative systems do not
benefit from the same sleep components. Other experimental manipulations inferred a specific role for stage 2
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CHAPTER 29 • Memory Processing in Relation to Sleep 337
sleep in the second part of the night for the consolidation
of motor memories.27,28 Hence, sleep deprivation studies
have suggested that each stage of human sleep (REM sleep,
SWS, stage 2 sleep) might be involved in a distinctive way
in learning and memory consolidation processes.6,7
In the recent past, neuroimaging investigations have
complemented these findings using functional magnetic
resonance imaging (fMRI). As in behavioral paradigms,
subjects are trained to the task and then either deprived of
sleep or allowed to sleep on the following night. A few days
later, cerebral activity is recorded during memory retrieval
and the two posttraining sleep conditions are compared.
One or two additional nights of regular sleep are usually
allowed after the posttraining night before testing in the
scanner, to avoid different arousal states that may confound neural activity associated with memory retrieval
between sleeping and sleep-deprived subjects. These neuroimaging studies have yielded two important contributions. First, they have demonstrated that sleep deprivation
during the posttraining night eventually impedes the reorganization and optimization of the cerebral activity, subtending delayed retrieval of consolidated memories during
wakefulness.29-32 Second, they have shown that sleepdependent changes in memory-related brain activity patterns may be present even when similarity in behavioral
performance between posttraining sleep conditions suggests an absence of sleep-related effect on memory.30,32
The latter results further indicate that long-term memory
performance can be achieved using different cerebral strategies initiated as a function of the status of sleep during
the posttraining night.
Posttraining Sleep Modifications
The second line of investigation stemmed from the reasoning that if newly acquired information underwent an
ongoing process of consolidation during sleep, then this
should be reflected in neural and physiologic features of
posttraining sleep. Using electroencephalographic (EEG)
recording techniques, numerous animal studies have
reported changes in, or memory-related associations with,
a series of postlearning sleep parameters, including sleep
stage duration or proportion relative to total sleep time,
density of rapid eye movements, power increase in selected
EEG frequency ranges, changes in density and duration of
phasic events (e.g., spindles, ponto-geniculo-occipital
waves), and reexpression of learning-specific neural patterns (for reviews, see references 3, 4, 6, 33, 34).
Likewise, in humans, numerous EEG studies have evidenced that both the architecture of sleep and distinctive
features of sleep stages can be affected by prior learning
experience. For example, postlearning sleep modifications
have been shown when looking at absolute or proportional
(i.e., relative to total sleep time) increases in the duration
of REM sleep,6,20,35-37 stage 2 sleep38 and SWS20 episodes.
Other studies have reported increased density of rapid eye
movements39,40 and stage 2 spindle activity in the sigma
frequency band,41-50 as well as increases in REM sleep theta
power.51 Many found statistical correlations between quantitative parameters of sleep and overnight performance
improvements20,37,41-44,48-50 or levels of performance at the
end of learning,45 suggesting a close link between changes
in sleep physiology and memory consolidation. In support
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338 PART I / Section 4 • Physiology in Sleep
of the double-step hypothesis described earlier, others
studies evidenced relationships between performance
changes and the organization of NREM/REM sleep
cycles.19,52 Hence, these investigations, mostly based on
noninvasive electrophysiologic techniques, have consistently demonstrated that physiology of sleep is influenced
by prior learning during the day. Additionally, waking
experience was shown to influence the content of hypnagogic hallucinations53 and of dreams collected on awakening from sleep stages54,55 on the postexposure night,
although delayed incorporations of up to weeks have also
been reported often.55
Noninvasive neuroimaging studies, especially using positron emission tomography (PET) measurements, with
their better spatial resolution and whole brain coverage,
have been used to look more precisely at the neural correlates of postlearning modifications during sleep. They
have shown that neural activity occurring during waking
task practice in learning-dedicated cerebral structures can
be reexpressed or continued during both REM56,57 and
NREM58 stages of sleep, as well as during posttraining
wakefulness.21 These data were in close agreement with
intracerebral recording studies in animals, which demonstrated neuronal reactivation during sleep.59,60 The animal
data suggested reactivation of coherent memory traces in
key cerebral structures during sleep that was deemed to
contribute to or reflect the result of the memory consolidation process. However, these seminal animal studies did
not experimentally establish the behavioral relevance of
reactivations in neuronal ensembles, as they never sought
to show a relationship with subsequent behavioral modifications. A significant contribution of human neuroimaging
data was to show that experience-dependent reactivations
of local—that is, hippocampal—activity during SWS are
correlated to overnight gains in memory performance after
spatial navigation.58 On the other hand, levels of implicit
procedural learning achieved before sleep correlated with
the amplitude of reactivation in cortical areas during REM
sleep,57 at which time connectivity patterns between learning-related areas were additionally reinforced.61 Taken
together, human reactivation studies have suggested the
neuronal replay of previous experience during sleep, and
that posttraining sleep activity in brain areas involved
during the learning episode represents a neural signature
of memory-related cognitive processes. Another (but not
exclusive) hypothesis is that learning in the awake state
induces local synaptic changes that themselves induce local
changes in slow-wave activity (SWA), the main marker of
sleep homeostasis, and that these changes are ultimately
beneficial to imprint novel memories.62 In support of this
view, high-density electrophysiologic recordings have
demonstrated local increases in SWA in learning-related
areas during posttraining NREM sleep, correlating with
overnight performance improvements.63
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Within-Sleep Stimulations
Finally, a third approach to demonstrate memory processing during sleep has been to provide specific stimulations
during sleep with the aim of investigating whether meaningful stimuli could be recognized or new associations
formed, or whether presleep learning can be modified by
nonawakening stimulations. Evidence for such phenomena
Kryger_6453_Ch 29_main.indd 338
would indicate that active plastic processes are taking place
during sleep.
In line with animal studies,33 preliminary data have indicated the possibility of heart rate conditioning in man
during NREM sleep,64 suggesting plasticity during sleep.
On the other hand, no learning effect was found for lists
of paired-associate words presented during either REM or
stage 2 sleep and tested immediately afterward.65 Although
these results suggest a limitation in learning capacity
during sleep, there is consistent evidence that sleeping
subjects remain able to detect and discriminate external
sensory events as indexed by event-related auditory potentials (ERPs).66,67 Likewise, nociceptive stimulations during
sleep persistently elicit evoked responses.68 ERP and fMRI
data also indicated higher sensitivity to external stimuli
during tonic than phasic periods of REM sleep.69,70 Higherlevel processing of externally presented events was also
found during sleep, as auditory ERPs are elicited after
hearing one’s own name both while sleeping and awake.71
Nonetheless, brain responsiveness during sleep is not independent of prior waking experience. Learning semantic
associations72 or discriminating auditory patterns67 during
wakefulness leads to changes in evoked response potentials
during sleep,72 even up to 2 days later.67 These results
support the idea that external events can be processed
during certain periods of sleep, and that stimulus significance affects this processing.
Further demonstrating an active role for sleep in memory
consolidation processes, several studies have established
that stimulations in the posttraining sleep period may
enhance performance as compared with a standard,
unmodified posttraining night.73-77 Presentation of nonawakening auditory stimulations during REM sleep after
Morse code learning73 or re-presentation during REM
sleep of sounds heard in background while learning a
complex logic task74 increased overnight memory. This
effect was present only when auditory stimulations were
displayed in coincidence with the bursts of rapid eye movements that reflect phasic ponto-geniculo-occipital (PGO)
activity in man. Likewise, presentation during SWS of
odors that were used as contextual cues during the learning
episode triggered hippocampal responses and improved
overnight retention of declarative memories.77 Transcranial direct-current stimulation that modulates excitability
in cortical areas improved declarative memory when
applied during SWS,76 especially when application of oscillating potentials at about 0.75 Hz induced slow oscillationlike potential fields that mimic the slow oscillations of deep
NREM sleep.75 Finally, artificially maintaining high levels
of cortisol feedback and cholinergic tone during SWS
impairs hippocampus-dependent declarative memory formation,78-80 suggesting that the natural shift in central
nervous system cholinergic tone from high levels during
acquisition-related wakefulness periods to minimal levels
during SWS optimizes declarative memory consolidation.81 On the other hand, preventing natural increases in
cortisol during REM sleep periods appears to enhance
amygdala-dependent emotional memory.80 These studies
have demonstrated beneficial (or detrimental) effects of
various stimulations and manipulations in the posttraining
sleep periods on overnight gains in performance, and
therefore have provided interesting evidences that sleep
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CHAPTER 29 • Memory Processing in Relation to Sleep 339
does not play a merely passive role in memory processing
by protecting novel memories from interference. Rather,
they support the hypothesis that sleep acts in a complex
manner in providing optimal conditions for the consolidation of novel memories in the nervous system.
mPFC sites when initial encoding was followed by a night
of sleep than by sleep deprivation, suggesting that sleep
leads to long-lasting changes in the representation of
memories at the neuroanatomic level.31 These results may
be consistent with the hypothesis that sleep exerts an effect
on the gradual semanticization of the learned material.
SLEEP AND DECLARATIVE MEMORY
As discussed, long-term declarative memory comprises
semantic and episodic memory components. Experimental
data indicate that the role of sleep in consolidating these
two memory components may be dissociated to a certain
extent, and that emotional variables play a modulatory role
in episodic memory consolidation. These aspects will be
covered in the following section.
Episodic Memory
The effect of sleep on episodic memory has been
extensively studied using a series of declarative memory
paradigms encompassing learning of verbal material
such
as
lists
of
words
or
paired-associate
words15,31,41,42,50,51,75,76,78,79,84-89 and sentences or prose passages,90 and explicit encoding of landscapes,83 objects’
locations,77 faces,91 visuospatial memory,16,48 and navigation in virtual30,32,58,92 or natural93 environments.
Among these, most studies using partial behavioral15,16,31,85
or pharmacologic79 sleep deprivation have consistently
found that SWS, or at least the first half of the night of
sleep (which is rich in SWS), is beneficial for the consolidation of novel declarative memories. Consolidation of
declarative learning was also linked to increased spindle
activity during posttraining stage 2 sleep,41,42,48-50 as well as
to the alteration of SWS94 and spindles95 in schizophrenia.
Spindles are strong candidates to subtend memory consolidation processes during sleep because they are thought to
support neural plasticity.96 As well, declarative learning
abilities have been linked with increased spindle activity
during stage 2 sleep44,97 and periodic arousal fluctuations
during non-REM sleep98 in healthy subjects. On the other
hand, declarative memory deficits are associated with
decreased sleep spindle activity in patients with Alzheimer’s disease,99 and NREM sleep duration and number of
cycles in patients with chronic nonrestorative sleep.100
However, others reported that overnight performance
gains on declarative verbal memory depend primarily on
preserved organization of sleep cycles—that is, sleep continuity—rather than on the integrity of a specific sleep
stage per se.19 These studies may stand in contrast with
much older ones that showed impairment in recall of sentences and short stories101 or lists of words102 after selective
REM sleep deprivation. Also, a more recent study found
that REM sleep deprivation specifically impaired recall of
spatial and temporal features of memories, as well as the
subject’s confidence in his own remembering,89 these
parameters being considered as genuine components of
episodic memory, as opposed to general recall, which may
partially rely on semantic, decontextualized memories.2
Accordingly, it has been reported that consolidation
during sleep enhances explicit recollection in recognition
memory103 and strengthens the original temporal sequence
structure for lists of triplet words.104
Semantic Memory
Few studies have looked at the role of sleep for consolidation of semantic information, although ERP studies have
demonstrated that semantic processing of externally presented stimuli is possible during REM and stage 2 sleep,
but not during SWS.66,71,72 Also, it has been shown that the
semantic priming (i.e., the facilitatory processing effect
resulting from prior presentation of semantically related
material) qualitatively differs upon awakening from stage
2 and REM sleep.82 Despite evidence for residual semantic
processing, attempts to create novel semantic associations
using direct auditory stimulation during sleep have been
unsuccessful.65 Other evidence for a role of sleep in processing newly acquired semantic memories are not fully
conclusive because the tasks that have been used comprise
other cognitive components that may obscure the interpretation.2 For example, improvement in a French immersion course over 6 weeks was correlated with REM sleep
increases,36 but learning a novel language is a task that
involves episodic memory processes as well as the creation
of novel semantic associations. Likewise, learning Morse
code, which was found to be associated with increases in
REM sleep parameters,37 may be viewed as a specific form
of cognitive procedural learning of novel associations.
Also, it is believed that transfer of novel information from
hippocampus-dependent episodic memory stores to neocortical, semantic, decontextualized memory representations is a gradual process that may take years to complete.8
Therefore, protocols in which initial encoding, posttraining sleep periods and retrieval are temporally close are
probably not best suited to segregate the semantic component of memory from other constituents.
A few neuroimaging studies have investigated the cerebral correlates of declarative memory retrieval after
extended periods of time (up to 6 months) using pairedassociate list of words31 or pictures of landscapes.83
Although these experiments were not specifically designed
to probe whether the memorized material was semanticized at the time of retesting, neuroimaging results clearly
indicated a transfer from activity in hippocampal locations,
observed early after learning, toward activity in medial
prefrontal cortical (mPFC) sites recorded 6 months later
during memory retrieval.31,83 Furthermore, total sleep
deprivation on the postlearning night hindered this gradual
process of consolidation. Six months after learning verbal
material, memory retrieval more strongly activated the
Kryger_6453_Ch 29_main.indd 339
Emotion in Episodic Memory
The role of emotional variables in sleep-dependent processes has been a focus of recent interest.80,90,105-108 Emotion
can be seen as an important contextual cue in retention
of episodic memories, although it is not necessarily processed explicitly. Nonetheless, emotional material was
found to be better recalled after REM than after NREM
sleep90 and to be altered after sleep deprivation,105 although
more for the emotional content than the context of the
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340 PART I / Section 4 • Physiology in Sleep
information.108 However, others have found emotional
memories to be better preserved, or at least less disrupted,
than neutral memories after total sleep deprivation.80,106
These latter results suggest that consolidation of emotional memories also occurs efficiently during awake
periods, an effect that may be explained by the important
ecologic value of rapidly acquiring emotional stimulus–
response associations. Similarly, it was found that sleep
deprivation does not alter behavioral performance in an
ecologically valid virtual navigation task.30,32 Importantly,
a lack of behavioral effect does not guarantee that sleep
was without any consequence on memory consolidation
processes, as, in the case of both navigation and emotional
memories, underlying patterns of brain activity at retrieval
were effectively altered by sleep deprivation on the posttraining night.30,32,106
SLEEP AND NONDECLARATIVE
MEMORIES
As mentioned, memory abilities aggregated under the
nondeclarative label may be relatively independent from
both cognitive and neuroanatomic standpoints.5 Skills
and habits that refer to the gradual acquisition of novel
perceptual, motor, and cognitive abilities through repeated
practice (e.g., discriminating figures, playing piano, riding
a bicycle, detecting environmental regularities) have been
the most widely investigated in relation to sleep. In
this respect, numerous studies have found that posttraining sleep boosts acquisition levels on nonverbal
motor,35,46,109-115 perceptual,20,54,116-124 and perceptual–
motor15,27,29,43,45,56,57,61,63,125-129 procedural learning tasks.
Additionally, a few studies have found that sleep particularly enhances procedural memory performance in
brain-damaged individuals,130,131 but not in patients suffering from degenerative Parkinson’s disease,132 suggesting
the importance of sleep in motor rehabilitation programs.
Next, we further describe the role of sleep in (1) perceptual, (2) motor, and (3) perceptual–motor learning,
and (4) priming.
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Sleep and Perceptual Learning
One of the most consistent findings in the literature is the
prominent role of sleep in the development of visual discrimination abilities. Most studies have used the texture
discrimination task initially proposed by Karni and Sagi,133
where learning is retinotopic (i.e., specific to the trained
visual quadrant).20,116,120-124 It was initially found that selective REM sleep deprivation, but not SWS deprivation,
abolished overnight performance improvement during
visual perceptual learning, whereas no or only feeble
improvements occurred over episodes of wakefulness.133
However, another study using the same task found that
improvement in visual discrimination skills was mostly disrupted by early sleep deprivation (i.e., rich in SWS), and
even more so by total sleep deprivation.116 This apparent
contradiction was partially resolved with the finding that
overnight improvement was a direct function of both the
amount of SWS in the first quarter of the night and the
amount of REM sleep in the late quarter of the night,20
suggesting that SWS prompts memory formation, which
is possibly, but not necessarily, consolidated during REM
Kryger_6453_Ch 29_main.indd 340
sleep. There is further evidence of the complementary
roles of sleep stages in the offline (i.e., occurring outside
of actual practice) processes of consolidation for visual
perceptual learning. Indeed, others have found that
repeated practice on a task within the same day does not
lead to any improvement and can even result in performance deterioration for the trained visual quadrant, unless
there is an intervening sleep episode.123 But most importantly, they demonstrated that the duration of the sleep
episode and its constituent phases is crucial in this process,
as 30-minute daytime naps merely discontinued performance deterioration over repeated sessions,123 60-minute
naps reverted performance to its original level,123 and
90-minute naps yielded improvement in discrimination
performance.122 The main differences were more time
spent in NREM sleep in the 60-minute nap than in the
30-minute nap, and the occurrence of REM sleep in the
90-minute nap. Other studies confirm the importance of
posttraining sleep in the consolidation of coarse visual
discrimination119 as well as the effect of visual adaptation
paradigms on subsequent sleep parameters,54 thus demonstrating the importance of both REM and NREM sleep
stages for consolidation of procedural abilities in the visual
system.
However, sleep-dependent improvements cannot yet be
fully generalized across modalities, as contradictory results
have been reported in the auditory domain. Whereas some
authors have reported a beneficial influence of sleep on
acquisition of auditory discrimination skills118,134 and perceptual generalization of phonologic categories,117 others
have found that the same amount of time spent in the
awake state is sufficient to allow the development of auditory identification abilities.135,136 With respect to more
sophisticated auditory discrimination abilities, however, it
has been shown that integration of newly learned spoken
word forms, which must be discriminated from similarsounding entries during auditory word recognition,
requires an incubation-like period containing sleep.137
Sleep and Motor Learning
Using a simple sequential thumb-to-fingers opposition
task, Karni and coworkers investigated the time-dependent
evolution of motor learning.10 They showed that skilled
performance on this task is acquired across an initial,
within-session, fast learning phase, followed by a slow
phase of consolidation and optimization that can extend
for several weeks of repeated practice. Using the same task
or a keyboard-presses variant, others subsequently found
that posttraining sleep significantly enhanced performance
in the absence of further practice, as compared with the
same amount of time elapsed awake.46,109,111,112 However,
contrary to the observations made using perceptual visual
discrimination tasks described in the prior section, it
cannot be claimed here that posttraining time spent awake
prevents the formation of long-term motor memories, as
performance merely stabilizes at the level achieved at the
end of learning and does not deteriorate but rather modestly improves over repeated practice sessions. Still, a transitory boost in performance that is observed 5 to 30 minutes
after the end of learning138 disappears if tested without an
intermediate sleep period more than 4 hours later.46,138
Interestingly, performance improvement over the 5- to
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30-minute boost predicts performance levels after a night
of sleep.138 This precocious posttraining period appears
important for the initial stabilization of motor memories,21
as learning an interfering sequence of movements during
30 minutes to 2 hours after training disrupts delayed,
sleep-dependent consolidation of the original material,109,114 unless a nap is allowed.114 This role of sleep for
motor memory consolidation extends beyond a genuine
motor component, as training-related changes in sleep
architecture are observed after practice of a sequence of
finger movements but not after random key-presses,110 as
well as after acquiring new and complex motor patterns
such as trampolining35,115 but not after the familiar and
well-learned motor activities of soccer or dancing.115 These
latter results are in line with the demonstration that sleep
provides maximal benefit for motor-skill procedures that
proved to be most difficult during learning.113 Motor learning–related changes in posttraining sleep parameters were
mostly observed during stage 2 sleep,46,110,111 although
others have reported links with REM sleep115,139 or sleepcycle organization.35 Further studies are needed to delineate precisely the role and benefit of sleep on motor
learning.
Sleep and Perceptual–Motor Learning
The motor learning tasks just described have definite features. They are self-initiated, and acquisition is initially
carried out in an explicit, almost declarative manner, as
the motor sequence of movements to be generated is
already known and can even be verbalized. In this respect,
motor procedural learning reflects the optimization of
predefined motor forms possibly created with the con­
tribution of episodic memory processes. In contrast,
perceptual–motor procedural learning entails a motor
performance triggered by external stimulations, but the
organization of the material to be learned is not necessarily obvious to the subject, although it affects its performance. This type of task potentially allows us to
distinguish the role of sleep for consolidation of unconsciously as opposed to consciously formed memories. We
will cover this aspect after reviewing perceptual–motor
studies.
It was initially found that performance improvement on
the pursuit rotor task was blocked by total sleep deprivation and by sleep deprivation of the second part of the
night, but not by selective REM sleep deprivation.27 Task
improvement was also associated with increased sleep
spindle activity,45,51 suggesting that consolidation of motor
adaptive memories is mostly dependent on stage 2 sleep.
Functional MRI additionally showed that posttraining
total sleep deprivation hampered both performance
improvement and the reorganization of brain activity on a
visuomotor pursuit task with hidden regularities in the
target’s trajectory.29 However, mirror-tracing skills were
reported to improve more during the late part of the
night,15 and to be associated with REM sleep increases in
well-performing individuals,51 suggesting that this latter
task is rather REM sleep dependent. Still, performance
improvement on mirror tracing was also found to occur
after naps dominated by stage 2 sleep125 and to correlate
with stage 2 sleep spindle activity.43 This apparent discrepancy between sleep stages and task associations in the
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CHAPTER 29 • Memory Processing in Relation to Sleep 341
perceptual–motor learning domain might be explained by
differences in initial skill levels of participants. Indeed, an
association was reported between performance improvement on the pursuit rotor task and stage 2 spindle activity
in highly skilled subjects, whereas a similar relationship
was established with REM density in less skilled subjects,128
in line with the proposal that motor skills tasks involving
REM and stage 2 sleep might depend on two separate, but
overlapping, neural systems.28
This interpretation may be consistent with neuroimaging data that have established a relationship between posttraining REM sleep activity and the consolidation of
higher-order perceptual–motor cognitive skills. Indeed,
subcortical and neocortical areas already activated during
practice on a probabilistic sequence-learning task140 (i.e., a
paradigm of implicit sequence learning) were reactivated
during posttraining REM sleep in subjects previously
trained to the task.56,57,61 It was further demonstrated that
these reactivations were not merely activity dependent but
occurred specifically because a rules-based sequence was
implicitly learned during prior practice,57 supporting the
hypothesis that REM sleep is deeply involved in the reprocessing and optimization of the high-order information
contained in the material to be learned, as opposed to its
motor component alone. Moreover, it was found in a
40-hour constant routine protocol in which subjects were
allowed 75 minutes of sleep every 150 minutes that
sequence learning improved after naps, and most especially
after naps that followed the circadian peak of REM sleep
and in which REM sleep was present.141
Nonetheless, further studies using sequence-learning
tasks have raised several issues, and some of these remain
to be solved. It has been claimed that sleep is beneficial for
sequence learning only when acquisition of the sequential
regularities practiced during the task was explicit, with
time alone being sufficient for the consolidation of implicitly acquired sequences.23,142 These results appear to
contradict the findings of REM-sleep dependency for
high-order probabilistic sequence learning, in which learning was undoubtedly implicit.57,140,141 However, one overlooked difference between these studies and those claiming
a sleep dependency exclusively for explicit sequential material is that the latter have used deterministic, repeated
sequences, whereas the probabilistic sequences used in the
former studies are much more ambiguous. It is therefore
possible that sleep (and especially REM sleep) mostly supports the consolidation of implicitly acquired complex
relationships. This interpretation may be in line with the
proposal that different aspects of a procedural memory are
processed separately during consolidation, such as the
movement sequence in itself (e.g., a repeated, deterministic
sequence) improves over daytime wakefulness periods
independently of sleep, whereas its goal (e.g., the complex,
abstract rules for item succession in a probabilistic
sequence) improves after a night of sleep.129 How and
whether offline processes of memory consolidation do
actually benefit from posttraining sleep may also be a function of the circadian moment of the day when the material
is acquired,127 as well as the nature of the complex interactions between declarative and procedural memory
systems.22 The complexity of these interactions is further
illustrated by the demonstration that learning-related
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342 PART I / Section 4 • Physiology in Sleep
cerebral responses in cerebral structures linked to procedural (i.e., striatum) and declarative (i.e., hippocampus)
memory systems are both linearly related to an overnight
gain in performance in an implicit oculomotor sequencelearning task.143
Sleep and Priming
Perceptual priming refers to the facilitation or bias in the
processing of a stimulus as a function of a recent encounter
with that stimulus.144 The few studies that have investigated a role for sleep in consolidating the memory representations subtending priming16,145,146 or priming-like147,148
effects have yielded discrepant results. Although studies
have found that intervening deprivation of sleep, and especially REM sleep, alters priming effects in word-stem
completion16 as well as in face processing,145 and enhances
reactivity for emotional pictures,147 another study (using
better controlled tachistoscopic identification of drawings)
failed to disclose sleep-dependent effects.146 A variant of
priming is the “mere exposure effect,” obtained when incidental exposure to initially novel stimuli (e.g., nonsense
words, line drawings, ideograms, faces, novel three-dimensional objects) increases the likelihood that they will be
favored over nonpresented items later on during a preference judgment.144 Using this task to investigate the effects
of time, postexposure sleep, and cerebral lateralization, it
was found that although detrimental in both hemispheres,
total sleep deprivation did not affect performances to the
same extent, suggesting interhemispheric differences in
sleep-dependent processes of memory consolidation.148
Indeed, sleep deprivation abolished all memory effects
only in the right hemisphere.148 Interhemispheric differences in wake- and sleep-dependent memory consolidation
processes should therefore be investigated in more detail
in the future.
SLEEP-DEPENDENT MECHANISMS OF
BRAIN PLASTICITY AND MEMORY
CONSOLIDATION
In this section, we provide a rapid overview of specific
mechanisms viewed as particularly important to support
sleep-stage–related processes of brain plasticity and
memory consolidation: PGO waves, hippocampal rhythms,
and sleep spindles.
L
PGO Waves
Ponto-geniculo-occipital waves are prominent phasic bioelectrical potentials, closely related to rapid eye movements, occurring in isolation or in bursts during the
transition from NREM to REM sleep or during REM
sleep itself. PGO waves are a fundamental process of REM
sleep in animals, playing a significant role in central
nervous system maturation.34 Intracerebral recordings in
epileptic patients,149 and noninvasive PET,150 fMRI,151 and
magnetoencephalography152 scanning in healthy volunteers, indicate that the rapid eye movements observed
during REM sleep are generated by mechanisms similar or
identical to PGO waves in animals. Most importantly,
animal data have suggested that PGO activity during REM
sleep is associated with learning and memory consolidation,34 suggesting that activation of this generator during
Kryger_6453_Ch 29_main.indd 342
REM sleep may represent one of the natural physiologic
processes of memory, possibly through the synchronization of fast oscillations that would convey experiencedependent information in thalamocortical and intracortical
circuits.153
Despite evidence from animal studies, a direct demonstration of the association between PGO activity and
memory consolidation during REM sleep in humans has
yet to be done. Nonetheless, the hypothesis is supported
by studies showing an increase in the density of rapid eye
movements during REM sleep after procedural learning40,154 and intensive learning periods,39 or a correlation
between retention levels after learning Morse code and the
frequency of rapid eye movements during posttraining
REM sleep.37 Also, presenting sounds in the background
while learning a complex logic task in the awake state
enhanced next-morning performance when the same
sounds were presented again during REM sleep. Most
interestingly, however, enhancement was found only when
sounds were coincident with the bursts of posttraining
rapid eye movements that reflect PGO activity,74 further
suggesting the association of REM sleep with memory
consolidation processes. Also, it has been proposed that
during human phasic REM sleep, propagation of PGO
activity in the parahippocampal or hippocampal area is
linked with verbal learning performance and mnemonic
retention values.155
Hippocampal Rhythms
The theta rhythm (i.e., regular sinusoidal oscillations in
the frequency range of 4 to 7 Hz recorded in the hippocampal EEG) is a prominent signature of REM sleep in
mammals, including humans.156 Theta represents the
online state of the hippocampus, believed to be critical for
temporal coding or decoding of active neuronal ensembles
and the modification of synaptic weights.156 Additionally,
population synchrony of pyramidal cells is maximal during
quiet wakefulness and SWS associated with sharp waves
(i.e., sharp waves of SWS are the consequence of synchronous discharge of bursting CA3 pyramidal neurons) and
fast ripples (140 to 200 Hz). Sharp waves and ripples
during SWS constitute good candidates to induce neuronal plasticity.157 Thus, the alternation between both REM
sleep/active-awake theta activity and SWS/quiet-wakefulness sharp waves and ripples could contribute to brain
plasticity. According to the two-stage model of memory
formation,157 neocortical information activates the entorhinal input, which will cause synaptic changes to occur in
the hippocampal CA3 system during learning associated
with active waking and REM sleep theta rhythmic activity
in the hippocampus. In the subsequent nontheta state (i.e.,
SWS, but possibly also quiet wakefulness), previously activated neurons are reactivated during sharp wave bursts,
and the memory representation transiently stored in the
CA3 region can be transferred to neocortical targets for
the long term.
Accordingly, human brain imaging studies have demonstrated after spatial navigation in a virtual town the
experience-dependent reactivation of hippocampal activity
during SWS, but not during REM sleep.58 Similarly, an
odor-cued activation in hippocampus-related memory
areas was observed during SWS,77 eventually leading to
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overnight performance improvement. These studies also
found long-term transfer of hippocampal memories
toward neocortical stores,31,83 an effect disturbed by sleep
deprivation on the posttraining night.31 In parallel, neuroimaging data have suggested the offline persistence of
memory-related cerebral activity during active wakefulness
and its dynamic evolution in the hippocampus.21 Although
this model is well supported by the these data and may
account for the offline processing of declarative material,
the fact that reactivations have been observed during both
posttraining REM sleep56,57 and wakefulness21 after procedural, nonhippocampal learning suggests that other
routes for consolidation exist, which should likewise be
investigated.
Sleep Spindles and Slow Waves
Traditionally, the sleep spindle has been defined as the
presence of rhythmic 12- to 14-Hz activity lasting a
minimum of 0.5 seconds and displaying an increasing, then
decreasing, amplitude envelope. This definition has
expanded to 12 to 16 Hz and includes both slow (11.5- to
14-Hz) and fast (14- to 16-Hz) spindles, which may reflect
two separate spindle generators with different brain topographies.158,159 Although spindles occur most frequently in
stage 2, they also appear to a lesser extent in delta sleep
(stages 3 and 4). A negative reciprocal relationship between
SWA and spindle occurrence seems to exist in NREM
sleep.158 Spindle mechanisms have been studied in the
cat.160,161 They are considered to result from intrinsic properties and from the connectivity patterns of the thalamic
neurons. Spindle generation seems an ideal mechanism
for neural plasticity.96 Therefore, spindles may play an
important role in the processes of memory consolidation
during sleep.
Accordingly, several studies have reported links between
the consolidation of verbal declarative memory and
increases in spindle density during the nocturnal and
diurnal sleep that follows learning.41,42,44,49 Verbal memory
association with spindle density increased in the left frontocentral scalp location at night, whereas memory for faces
did not elicit this effect.49 Similarly, postlearning increases
are observed during daytime napping in low-frequency
spectral power (11.25 to 13.75 Hz), particularly in the left
frontal scalp region. Additionally, these increases are positively correlated with learning performance in the difficult
word-association task, but not in the easy word-association
task or control condition.42 Similarly for procedural
memory, posttraining stage 2 sleep deprivation impaired
memory for a perceptual–motor task,27 and the amount of
stage 2 correlated with learning progress on the fingertapping task.109,111 Also, intensive training on perceptual–
motor learning tasks results in marked increases in number
and density of spindles during subsequent stage 2 sleep47
as well as an increase in average spindle duration.51 Posttraining increases in slow sigma power (12 to 14 Hz) have
been observed in frontal and occipital regions with no
changes in high-frequency sigma.51 Napping studies using
the same task provided similar results: subjects who regularly napped showed positive correlations between postnap
performance and stage 2 spindle density.162 In this case,
low-frequency spindles (12 to 14 Hz) were correlated with
performance at frontal sites, whereas high-frequency
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CHAPTER 29 • Memory Processing in Relation to Sleep 343
spindle activity (14 to 16 Hz) was correlated with performance at central and parietal sites. Moreover, subjects who
did not nap on a regular basis did not benefit from an
experimental nap in the study design.162 In another study
using a longer (60- to 90-minute) nap after motor performance for the finger-tapping task, it was found that those
subjects with the most significant increases in motor performance also had the largest increases in stage 2 sleep,
with a significant correlation between spindle density and
postnap performance that was confined to the learning
hemisphere.46 Finally, a marked increase in stage 2 spindle
densities was observed after acquisition of the finger-tapping task, but not after a control motor task, indicating
that the changes were not the result of general motor activity.110 That spindles have been related to consolidation for
both declarative and nondeclarative memories indicates
their prominent role in sleep-dependent memory
processes.
Still, it should be noticed that although stage 2 has been
the predominant stage of sleep involved, closer examination showed that REM sleep appeared to be more important for some participants after perceptual–motor
learning.128 To explain this, it has been proposed that there
are two independent neural systems for sleep-dependent
memory consolidation, one involved with stage 2 sleep, the
other with REM sleep. In this respect, subjects who report
the perceptual–motor task as being a novel experience
show an increase in density of rapid eye movements during
postacquisition REM sleep, but no changes in stage 2 sleep
parameters. On the other hand, those individuals who find
the task to be similar to others they have already experienced in their lives (as shown by reasonably good performance on the first few trials of the task) will show an
increase in spindle density during stage 2 sleep but no
changes in REM sleep. These latter subjects are considered to be refining an existing motor program rather than
learning a new one.28
In addition, spindle oscillations are grouped and regulated by slow waves163 that are thought to be important for
memory consolidation, as discussed earlier. Indeed, experience-dependent regional increases in delta activity
have been shown during NREM sleep,63 suggesting local
homeostatic mechanisms for memory consolidation.62 Furthermore, coherence was found to increase after learning
in the depolarizing phase of the slow oscillations below the
1-Hz frequency.163 On the other hand, transcranial direct
current stimulation that may contribute to modulation of
cortical excitability was found to improve the overnight
retention of declarative memories when applied during
NREM sleep at a slow rhythm whose frequency (less than
1 Hz) approximates these slow oscillations,75 further suggesting a facilitatory role of slow oscillatory EEG activity
in neuronal plasticity and the ongoing transformations and
consolidation of memory traces.
Conclusions
Although their results are at times elusive, studies supporting the proposal that sleep is an integral component
in the offline processes that subtend memory consolidation have now substantially flourished. Still, when compared with other domains of cognition, the field remains
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344 PART I / Section 4 • Physiology in Sleep
underdeveloped. There is an urgent need for replication
and validation of studies to confirm or disprove a series
of hypotheses regarding which memories can benefit from
sleep, and in which circumstances this can occur. Furthermore, the mechanisms that support these processes
remain to be fully elucidated and understood. Most important, we need to understand how sleep disorders and the
numerous pathologies accompanied by sleep disturbances
affect cognitive processes, especially learning and memory,
and to understand the extent to which sleep manipulation
helps or speeds up resolution of these pathologies. This
is an exciting area of research for sleep specialists, neuroscientists, and cognitive psychologists, who should join
forces to help patients suffering from sleep-related
afflictions.
❖ Clinical Pearls
In the long term, patients with inadequate REM sleep
may be expected to experience more difficulty learning novel cognitive procedures than same-age individuals with healthy sleep. Patients exhibiting little
or impaired slow-wave sleep may be impaired in
declarative learning (e.g., memorizing large amounts
of factual material). Those with specific stage 2 sleep
disturbances can be expected to have trouble refining and performing reasonably simple motor skill
tasks. Patients with poor sleep quality or pathologies
affecting all sleep stages can be expected to have
deteriorated long-term performance with all types of
memory. Sleep is only a part of memory consolidation processes, however, so these deficits may manifest in a subtle manner and may, to a certain extent,
be compensated for by alternative consolidation
strategies. In-depth clinical investigation of memory
problems should always be done by a trained
neuropsychologist.
REFERENCES
L
1. Saint-Denys HD. Les rêves et les moyens de les diriger. Paris: Editions d’Aujourd’hui; 1977.
2. Rauchs G, Desgranges B, Foret J, Eustache F, et al. The relationships between memory systems and sleep stages. J Sleep Res
2005;14:123-140.
3. Smith C. Sleep states, memory processes and synaptic plasticity.
Behav Brain Res 1996;78:49-56.
4. Maquet P, Smith C, Stickgold R. Sleep and brain plasticity. Oxford:
Oxford University Press; 2003.
5. Squire LR. Memory systems of the brain: a brief history and current
perspective. Neurobiol Learn Mem 2004;82:171-177.
6. Peigneux P, Laureys S, Delbeuck X, Maquet P, et al. Sleeping brain,
learning brain. The role of sleep for memory systems. Neuroreport
2001;12:A111-A124.
7. Smith C. Sleep states and memory processes in humans: procedural
versus declarative memory systems. Sleep Med Rev 2001;5:
491-506.
8. McClelland JL, McNaughton BL, O’Reilly RC. 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 1995;102:419-457.
9. Bontempi B, Laurent-Demir C, Destrade C, Jaffard R, et al. Timedependent reorganization of brain circuitry underlying long-term
memory storage. Nature 1999;400:671-675.
Kryger_6453_Ch 29_main.indd 344
10. Karni A, Meyer G, ReyHipolito C, Adams MN, et al. The acquisition of skilled motor performance: fast and slow experiencedriven changes in primary motor cortex. PNAS USA 1998;95:
861-868.
11. Wixted JT. The psychology and neuroscience of forgetting. Annu
Rev Psychol 2004;55:235-269.
12. McGaugh JL. Time-dependent processes in memory storage.
Science 1966;153:1351-1358.
13. Kolb B, Whishaw IQ. Brain plasticity and behavior. Annu Rev
Psychol 1998;49:43-64.
14. Gaarder K. A conceptual model of sleep. Arch Gen Psychiatry
1966;14:253-260.
15. Plihal W, Born J. Effects of early and late nocturnal sleep on
declarative and procedural memory. J Cogn Neurosci 1997;9:
534-547.
16. Plihal W, Born J. Effects of early and late nocturnal sleep
on priming and spatial memory. Psychophysiology 1999;36:571582.
17. Giuditta A, Ambrosini MV, Montagnese P, Montagnese P, et al.
The sequential hypothesis of the function of sleep. Behav Brain Res
1995;69:157-166.
18. Scrima L. Isolated REM sleep facilitates recall of complex associative information. Psychophysiology 1982;19:252-259.
19. Ficca G, Lombardo P, Rossi L, Salzarulo P, et al. Morning recall
of verbal material depends on prior sleep organization. Behav Brain
Res 2000;112:159-163.
20. Stickgold R, Whidbee D, Schirmer B, Patel V, et al. Visual discrimination task improvement: a multi-step process occurring
during sleep. J Cogn Neurosci 2000;12:246-254.
21. Peigneux P, Orban P, Balteau E, Degueldre C, et al. Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 2006;4:e100.
22. Brown RM, Robertson EM. Off-line processing: reciprocal interactions between declarative and procedural memories. J Neurosci
2007;27:10468-10475.
23. Robertson EM, Pascual-Leone A, Press DZ. Awareness modifies
the skill-learning benefits of sleep. Curr Biol 2004;14:208-212.
24. Jenkins J, Dallenbach K. Obliviscence during sleep and waking. Am
J Psychol 1924;35:605-612.
25. Smith C. Sleep states and learning: a review of the animal literature.
Neurosci Biobehav Rev 1985;9:157-168.
26. Ekstrand BR. Effect of sleep on memory. J Exp Psychol 1967;
75:64-72.
27. Smith C, MacNeill C. Impaired motor memory for a pursuit rotor
task following Stage 2 sleep loss in college students. J Sleep Res
1994;3:206-213.
28. Smith C, Aubrey J, Peters K. Different roles for REM and stage 2
sleep in motor learning: a proposed model. Psychol Belg 2004;44:
79-102.
29. Maquet P, Schwartz S, Passingham R, Frith C. Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by
functional magnetic resonance imaging. J Neurosci 2003;23:
1432-1440.
30. Rauchs G, Orban P, Schmidt C, Albouy G, et al. Sleep modulates
the neural substrates of both spatial and contextual memory consolidation. PLoS ONE 2008;3:e2949.
31. Gais S, Albouy G, Boly M, Dang-Vu TT, et al. Sleep transforms
the cerebral trace of declarative memories. PNAS USA 2007;
104:18778-18783.
32. Orban P, Rauchs G, Balteau E, Degueldre C, et al. Sleep after
spatial learning promotes covert reorganization of brain activity.
PNAS USA 2006;103:7124-7129.
33. Hennevin E, Huetz C, Edeline JM. Neural representations during
sleep: from sensory processing to memory traces. Neurobiol Learn
Mem 2007;87:416-440.
34. Datta S, Patterson EH. Activation of phasic pontine wave (P-wave):
A mechanism of learning and memory processing. In: Maquet P,
Smith C, Stickgold R, editors. Sleep and brain plasticity. Oxford,
UK: Oxford University Press; 2003. p. 135-156.
35. Buchegger J, Meier-Koll A. Motor learning and ultradian sleep
cycle: an electroencephalographic study of trampoliners. Percept
Mot Skills 1988;67:635-645.
36. de Koninck J, Lorrain D, Christ G, Proulx G, et al. Intensive language learning and increases in rapid eye movement sleep: evidence
of a performance factor. Int J Psychophysiol 1989;8:43-47.
8/24/2010 7:23:51 PM
CHAPTER 29 • Memory Processing in Relation to Sleep 345
37. Mandai O, Guerrien A, Sockeel P, Dujardin K, et al. REM sleep
modifications following a Morse code learning session in humans.
Physiol Behav 1989;46:639-642.
38. Meier-Koll A, Bussman B, Schmidt C, Neuschwander D. Walking
through a maze alters the architecture of sleep. Percept Mot Skills
1999;88:1141-1159.
39. Smith C, Lapp L. Increases in number of REMS and REM density
in humans following an intensive learning period. Sleep 1991;
14:325-330.
40. Smith CT, Nixon MR, Nader RS. Posttraining increases in REM
sleep intensity implicate REM sleep in memory processing and
provide a biological marker of learning potential. Learn Mem
2004;11:714-719.
41. Gais S, Molle M, Helms K, Born J. Learning-dependent increases
in sleep spindle density. J Neurosci 2002;22:6830-6834.
42. Schmidt C, Peigneux P, Muto V, Schenkel M, et al. Encoding difficulty promotes postlearning changes in sleep spindle activity
during napping. J Neurosci 2006;26:8976-8982.
43. Tamaki M, Matsuoka T, Nittono H, Hori T. Fast sleep spindle
(13-15 hz) activity correlates with sleep-dependent improvement in
visuomotor performance. Sleep 2008;31:204-211.
44. Schabus M, Hoedlmoser K, Pecherstorfer T, Anderer P, et al.
Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res 2008;1191:127-135.
45. Peters KR, Ray L, Smith V, Smith C. Changes in the density of
stage 2 sleep spindles following motor learning in young and older
adults. J Sleep Res 2008;17:23-33.
46. Nishida M, Walker MP. Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2007;2:e341.
47. Fogel SM, Smith CT. Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res 2006;15:250-255.
48. Clemens Z, Fabo D, Halasz P. Twenty-four hours retention of
visuospatial memory correlates with the number of parietal sleep
spindles. Neurosci Lett 2006;403:52-56.
49. Clemens Z, Fabo D, Halasz P. Overnight verbal memory retention
correlates with the number of sleep spindles. Neuroscience
2005;132:529-535.
50. Schabus M, Gruber G, Parapatics S, Sauter C, et al. Sleep spindles
and their significance for declarative memory consolidation. Sleep
2004;27:1479-1485.
51. Fogel SM, Smith CT, Cote KA. Dissociable learning-dependent
changes in REM and non-REM sleep in declarative and procedural
memory systems. Behav Brain Res 2007;180:48-61.
52. Mazzoni G, Gori S, Formicola G, Gneri C, et al. Word recall correlates with sleep cycles in elderly subjects. J Sleep Res 1999;8:
185-188.
53. Stickgold R, Malia A, Maguire D, Roddenberry D, et al. Replaying
the game: hypnagogic images in normals and amnesics. Science
2000;290:350-353.
54. Corsi-Cabrera M, Becker J, Garcia L, Ibarra R, et al. Dream
content after using visual inverting prisms. Percept Mot Skills
1986;63:415-423.
55. Nielsen TA, Kuiken D, Alain G, Stenstrom P, et al. Immediate
and delayed incorporations of events into dreams: further replication and implications for dream function. J Sleep Res 2004;13:
327-336.
56. Maquet P, Laureys S, Peigneux P, Fuchs S, et al. Experiencedependent changes in cerebral activation during human REM sleep.
Nature Neurosci 2000;3:831-836.
57. Peigneux P, Laureys S, Fuchs S, Destrebecqz A, et al. Learned
material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage
2003;20:125-134.
58. Peigneux P, Laureys S, Fuchs S, Collette F, et al. Are spatial memories strengthened in the human hippocampus during slow wave
sleep? Neuron 2004;44:535-545.
59. Dave AS, Margoliash D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 2000;290:
812-816.
60. Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science 1994;265:676-679.
61. Laureys S, Peigneux P, Phillips C, Fuchs S, et al. Experiencedependent changes in cerebral functional connectivity during
human rapid eye movement sleep. Neuroscience 2001;105:521525.
Kryger_6453_Ch 29_main.indd 345
62. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep
Med Rev 2006;10:49-62.
63. Huber R, Ghilardi MF, Massimini M, Tononi G. Local sleep and
learning. Nature 2004;430:78-81.
64. Ikeda K, Morotomi T. Classical conditioning during human
NREM sleep and response transfer to wakefulness. Sleep 1996;
19:72-74.
65. Wood JM, Bootzin RR, Kihlstrom JF, Schacter DL. Implicit and
explicit memory for verbal information presented during sleep.
Psychol Science 1992;3:236-239.
66. Bastuji H, Perrin F, Garcia-Larrea L. Semantic analysis of auditory
input during sleep: studies with event-related potentials. Int J Psychophysiol 2002;46:243-255.
67. Atienza M, Cantero JL, Escera C. Auditory information processing
during human sleep as revealed by event-related brain potentials.
Clin Neurophysiol 2001;112:2031-2045.
68. Lavigne G, Brousseau M, Kato T, Mayer P, et al. Experimental
pain perception remains equally active over all sleep stages. Pain
2004;110:646-655.
69. Takahara M, Nittono H, Hori T. Comparison of the event-related
potentials between tonic and phasic periods of rapid eye movement
sleep. Psychiatry Clin Neurosci 2002;56:257-258.
70. Wehrle R, Kaufmann C, Wetter TC, Holsboer F, et al. Functional
microstates within human REM sleep: first evidence from fMRI of
a thalamocortical network specific for phasic REM periods. Eur J
Neurosci 2007;25:863-871.
71. Perrin F, Garcia-Larrea L, Mauguiere F, Bastuji H. A differential
brain response to the subject’s own name persists during sleep. Clin
Neurophysiol 1999;110:2153-2164.
72. Brualla J, Romero MF, Serrano M, Valdizan JR. Auditory eventrelated potentials to semantic priming during sleep. Electroencephalogr Clin Neurophysiol 1998;108:283-290.
73. Guerrien A, Dujardin K, Mandai O, Sockeel P, et al. Enhancement
of memory by auditory stimulation during postlearning REM sleep
in humans. Physiol Behav 1989;45:947-950.
74. Smith C, Weeden K. Post training REMs coincident auditory
stimulation enhances memory in humans. Psych J Univ Ottawa
1990;15:85-90.
75. Marshall L, Helgadottir H, Molle M, Born J. Boosting slow
oscillations during sleep potentiates memory. Nature 2006;444:
610-613.
76. Marshall L, Molle M, Hallschmid M, Born J, et al. Transcranial
direct current stimulation during sleep improves declarative
memory. J Neurosci 2004;24:9985-9992.
77. Rasch B, Buchel C, Gais S, Born J. Odor cues during slow-wave
sleep prompt declarative memory consolidation. Science 2007;315:
1426-1429.
78. Plihal W, Born J. Memory consolidation in human sleep depends
on inhibition of glucocorticoid release. Neuroreport 1999;10:
2741-2748.
79. Gais S, Born J. Low acetylcholine during slow-wave sleep is critical
for declarative memory consolidation. PNAS USA 2004;101:
2140-2144.
80. Wagner U, Degirmenci M, Drosopoulos S, Perras B, et al. Effects
of cortisol suppression on sleep-associated consolidation of neutral
and emotional memory. Biol Psychiatry 2005;58:885-893.
81. Rasch BH, Born J, Gais S. Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J Cogn Neurosci 2006;18:793-802.
82. Stickgold R, Scott L, Rittenhouse C, Hobson JA. Sleep-induced
changes in associative memory. J Cogn Neurosci 1999;11:182193.
83. Takashima A, Petersson KM, Rutters F, Tendolkar I, et al. Declarative memory consolidation in humans: a prospective functional
magnetic resonance imaging study. PNAS USA 2006;103:756761.
84. Ellenbogen JM, Hulbert JC, Stickgold R, Dinges DF, et al. Interfering with theories of sleep and memory: sleep, declarative memory,
and associative interference. Curr Biol 2006;16:1290-1294.
85. Tucker MA, Hirota Y, Wamsley EJ, Lau H, et al. A daytime nap
containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiol Learn Mem 2006;86:241-247.
86. Backhaus J, Born J, Hoeckesfeld R, Fokuhl S, et al. Midlife decline
in declarative memory consolidation is correlated with a decline in
slow wave sleep. Learn Mem 2007;14:336-341.
8/24/2010 7:23:51 PM
L
346 PART I / Section 4 • Physiology in Sleep
L
87. Backhaus J, Hoeckesfeld R, Born J, Hohagen F, et al. Immediate as
well as delayed post learning sleep but not wakefulness enhances
declarative memory consolidation in children. Neurobiol Learn
Mem 2008;89:76-80.
88. Tucker MA, Fishbein W. Enhancement of declarative memory
performance following a daytime nap is contingent on strength of
initial task acquisition. Sleep 2008;31:197-203.
89. Rauchs G, Bertran F, Guillery-Girard B, Desgranges B, et al. Consolidation of strictly episodic memories mainly requires rapid eye
movement sleep. Sleep 2004;27:395-401.
90. Wagner U, Gais S, Born J. Emotional memory formation is
enhanced across sleep intervals with high amounts of rapid eye
movement sleep. Learn Mem 2001;8:112-119.
91. Talamini LM, Nieuwenhuis IL, Takashima A, Jensen O. Sleep
directly following learning benefits consolidation of spatial associative memory. Learn Mem 2008;15:233-237.
92. Ferrara M, Iaria G, Tempesta D, Curcio G, et al. Sleep to find your
way: the role of sleep in the consolidation of memory for navigation
in humans. Hippocampus 2008;18:844-851.
93. Ferrara M, Iaria G, De Gennaro L, Guariglia C, et al. The role of
sleep in the consolidation of route learning in humans: a behavioural
study. Brain Res Bull 2006;71:4-9.
94. Goder R, Boigs M, Braun S, Friege L, et al. Impairment of visuospatial memory is associated with decreased slow wave sleep in
schizophrenia. J Psychiatr Res 2004;38:591-599.
95. Goder R, Fritzer G, Gottwald B, Lippmann B, et al. Effects of
olanzapine on slow wave sleep, sleep spindles and sleep-related
memory consolidation in schizophrenia. Pharmacopsychiatry 2008;
41:92-99.
96. Destexhe A, Sejnowski TJ. Thalamocortical assemblies: how ion
channels, single neurons, and large-scale networks organize sleep
oscillations. New York: Oxford University Press; 2001.
97. Schabus M, Hodlmoser K, Gruber G, Sauter C, et al. Sleep spindlerelated activity in the human EEG and its relation to general
cognitive and learning abilities. Eur J Neurosci 2006;23:17381746.
98. Ferini-Strambi L, Ortelli P, Castronovo V, Cappa S. Increased
periodic arousal fluctuations during non-REM sleep are associated
to superior memory. Brain Res Bull 2004;63:439-442.
99. Rauchs G, Schabus M, Parapatics S, Bertran F, et al. Is there a link
between sleep changes and memory in Alzheimer’s disease? Neuroreport 2008;19:1159-1162.
100. Goder R, Scharffetter F, Aldenhoff JB, Fritzer G. Visual declarative
memory is associated with non-rapid eye movement sleep and sleep
cycles in patients with chronic non-restorative sleep. Sleep Med
2007;8:503-508.
101. Empson JA, Clarke PR. Rapid eye movements and remembering.
Nature 1970;227:287-288.
102. Tilley AJ. Retention over a period of REM or non-REM sleep.
Brit J Psychol 1981;72:241-248.
103. Drosopoulos S, Wagner U, Born J. Sleep enhances explicit recollection in recognition memory. Learn Mem 2005;12:44-51.
104. Drosopoulos S, Windau E, Wagner U, Born J. Sleep enforces the
temporal order in memory. PLoS ONE 2007;2:e376.
105. Hu P, Stylos-Allan M, Walker MP. Sleep facilitates consolidation
of emotional declarative memory. Psychol Sci 2006;17:891-898.
106. Sterpenich V, Albouy G, Boly M, Vandewalle G, et al. Sleep-related
hippocampo-cortical interplay during emotional memory recollection. PLoS Biol 2007;5:e282.
107. Atienza M, Cantero JL. Modulatory effects of emotion and sleep
on recollection and familiarity. J Sleep Res 2008;
108. Payne JD, Stickgold R, Swanberg K, Kensinger EA. Sleep preferentially enhances memory for emotional components of scenes.
Psychol Sci 2008;19:781-788.
109. Walker MP, Brakefield T, Hobson AJ, Stickgold R. Dissociable
stages of human memory consolidation and reconsolidation. Nature
2003;425:616-620.
110. Morin A, Doyon J, Dostie V, Barakat M, et al. Motor sequence
learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 2008;31:1149-1156.
111. Walker MP, Brakefield T, Morgan A, Hobson JA, et al. Practice
with sleep makes perfect: sleep-dependent motor skill learning.
Neuron 2002;35:205-211.
112. Korman M, Raz N, Flash T, Karni A. Multiple shifts in the representation of a motor sequence during the acquisition of skilled
performance. PNAS USA 2003;100:12492-12497.
Kryger_6453_Ch 29_main.indd 346
113. Kuriyama K, Stickgold R, Walker MP. Sleep-dependent learning
and motor-skill complexity. Learn Mem 2004;11:705-713.
114. Korman M, Doyon J, Doljansky J, Carrier J, et al. Daytime sleep
condenses the time course of motor memory consolidation. Nat
Neurosci 2007;10:1206-1213.
115. Buchegger J, Fritsch R, Meier-Koll A, Riehle H. Does trampolining
and anaerobic physical fitness affect sleep? Percept Mot Skills
1991;73:243-252.
116. Gais S, Plihal W, Wagner U, Born J. Early sleep triggers memory
for early visual discrimination skills. Nature Neurosci 2000;3:
1335-1339.
117. Fenn KM, Nusbaum HC, Margoliash D. Consolidation during
sleep of perceptual learning of spoken language. Nature 2003;425:
614-616.
118. Gaab N, Paetzold M, Becker M, Walker MP, et al. The influence
of sleep on auditory learning: a behavioral study. Neuroreport
2004;15:731-734.
119. Matarazzo L, Franko E, Maquet P, Vogels R. Offline processing
of memories induced by perceptual visual learning during
subsequent wakefulness and sleep: a behavioral study. J Vis 2008;8:
71-79.
120. Gais S, Rasch B, Wagner U, Born J. Visual-procedural memory
consolidation during sleep blocked by glutamatergic receptor antagonists. J Neurosci 2008;28:5513-5518.
121. Walker MP, Stickgold R, Jolesz FA, Yoo S-S. The functional
anatomy of sleep-dependent visual skill learning. Cereb Cortex
2005;15:1666-1675.
122. Mednick S, Nakayama K, Stickgold R. Sleep-dependent learning: a
nap is as good as a night. Nat Neurosci 2003;6:697-698.
123. Mednick SC, Nakayama K, Cantero JL, Atienza M, et al. The
restorative effect of naps on perceptual deterioration. Nat Neurosci
2002;5:677-681.
124. Karni A, Tanne D, Rubenstein S, Askenasy JJM, et al. Dependence
on REM sleep of overnight improvement of a perceptual skill.
Science 1994;265:679-682.
125. Backhaus J, Junghanns K. Daytime naps improve procedural motor
memory. Sleep Med 2006;7:508-512.
126. Smith C, MacNeill C. Memory for motor task is impaired by stage
2 sleep loss. J Sleep Res 1992;21:139.
127. Cohen DA, Robertson EM. Motor sequence consolidation: constrained by critical time windows or competing components.
Exp Brain Res 2007;177:440-446.
128. Peters KR, Smith V, Smith CT. Changes in sleep architecture following motor learning depend on initial skill level. J Cogn Neurosci
2007;19:817-829.
129. Cohen DA, Pascual-Leone A, Press DZ, Robertson EM. Off-line
learning of motor skill memory: a double dissociation of goal and
movement. PNAS USA 2005;102:18237-18241.
130. Gomez Beldarrain M, Astorgano AG, Gonzalez AB, GarciaMonco JC. Sleep improves sequential motor learning and performance in patients with prefrontal lobe lesions. Clin Neurol
Neurosurg 2008;110:245-252.
131. Siengsukon CF, Boyd LA. Sleep enhances implicit motor skill
learning in individuals poststroke. Top Stroke Rehabil 2008;15:
1-12.
132. Marinelli L, Crupi D, Di Rocco A, Bove M, et al. Learning and
consolidation of visuo-motor adaptation in Parkinson’s disease. Parkinsonism Relat Disord 2009;15:6-11.
133. Karni A, Sagi D. Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. PNAS USA
1991;88:4966-4970.
134. Atienza M, Cantero JL, Stickgold R. Posttraining sleep enhances
automaticity in perceptual discrimination. J Cogn Neurosci 2004;
16:53-64.
135. Gottselig JM, Hofer-Tinguely G, Borbely AA, Regel SJ, et al. Sleep
and rest facilitate auditory learning. Neuroscience 2004;127:
557-561.
136. Roth DA, Kishon-Rabin L, Hildesheimer M, Karni A, et al.
A latent consolidation phase in auditory identification learning:
time in the awake state is sufficient. Learn Mem 2005;12:159164.
137. Dumay N, Gaskell MG. Sleep-associated changes in the mental
representation of spoken words. Psychol Sci 2007;18:35-39.
138. Hotermans C, Peigneux P, Maertens de Noordhout A, Moonen G,
et al. Early boost and slow consolidation in motor skill learning.
Learn Mem 2006;13:580-583.
8/24/2010 7:23:51 PM
139. Fischer S, Hallschmid M, Elsner AL, Born J. Sleep forms memory
for finger skills. PNAS USA 2002;99:11987-11991.
140. Peigneux P, Maquet P, Meulemans T, Born J. Striatum forever
despite sequence learning variability: a random effect analysis of
PET data. Hum Brain Mapp 2000;10:179-194.
141. Cajochen C, Knoblauch V, Wirz-Justice A, Krauchi K, et al.
Circadian modulation of sequence learning under high and low
sleep pressure conditions. Behav Brain Res 2004;151:167-176.
142. Spencer RM, Sunm M, Ivry RB. Sleep-dependent consolidation of
contextual learning. Curr Biol 2006;16:1001-1005.
143. Albouy G, Sterpenich V, Balteau E, Vandewalle G, et al. Both the
hippocampus and striatum are involved in consolidation of motor
sequence memory. Neuron 2008;58:261-272.
144. Butler LT, Berry DC. Understanding the relationship between
repetition priming and mere exposure. Br J Psychol 2004;95:
467-487.
145. Wagner U, Hallschmid M, Verleger R, Born J. Signs of REM sleep
dependent enhancement of implicit face memory: a repetition
priming study. Biol Psychol 2003;62:197-210.
146. Rauchs G, Lebreton K, Bertran F, Pelevin A, et al. Effects of partial
sleep deprivation on within-format and cross-format priming. Sleep
2006;29:58-68.
147. Wagner U, Fischer S, Born J. Changes in emotional responses to
aversive pictures across periods rich in slow-wave sleep versus rapid
eye movement sleep. Psychosom Med 2002;64:627-634.
148. Peigneux P, Schmitz R, Willems S. Cerebral asymmetries in sleepdependent processes of memory consolidation. Learn Mem 2007;
14:400-406.
149. Salzarulo P, Lairy GC, Bancaud J, Munari C. Direct depth recording of the striate cortex during REM sleep in man: are there PGO
potentials? EEG Clin Neurophysiol 1975;38:199-202.
150. Peigneux P, Laureys S, Fuchs S, Delbeuck X, et al. Generation of
rapid eye movements during paradoxical sleep in humans. Neuroimage 2001;14:701-708.
151. Wehrle R, Czisch M, Kaufmann C, Wetter TC, et al. Rapid eye
movement-related brain activation in human sleep: a functional
CHAPTER 29 • Memory Processing in Relation to Sleep 347
magnetic resonance imaging study. Neuroreport 2005;16:853857.
152. Ioannides AA, Corsi-Cabrera M, Fenwick PB, del Rio Portilla Y,
et al. MEG tomography of human cortex and brainstem activity in
waking and REM sleep saccades. Cereb Cortex 2004;14:56-72.
153. Amzica F, Steriade M. Progressive cortical synchronization of
ponto-geniculo-occipital potentials during rapid eye movement.
Neuroscience 1996;72:309-314.
154. Smith C. Changes in density of REM sleep following acquisition of
cognitive procedural tasks in humans. Actas Fisiol 2001;7:27.
155. Bodizs R, Bekesy M, Szucs A, Barsi P, et al. Sleep-dependent hippocampal slow activity correlates with waking memory performance
in humans. Neurobiol Learn Mem 2002;78:441-457.
156. Buzsaki G. Theta oscillations in the hippocampus. Neuron
2002;33:325-340.
157. Buzsaki G, Carpi D, Csicsvari J, Dragoi G, et al. Maintenance and
modification of firing rates and sequences in the hippocampus: does
sleep play a role. In: Maquet P, Smith C, Stickgold R, editors. Sleep
and brain plasticity. Oxford, UK: Oxford University Press; 2003.
p. 247-269.
158. De Gennaro L, Ferrara M. Sleep spindles: an overview. Sleep Med
Rev 2003;7:423-440.
159. Schabus M, Dang-Vu TT, Albouy G, Balteau E, et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid
eye movement sleep. PNAS USA 2007;104:13164-13169.
160. Amzica F, Steriade M. Integration of low-frequency sleep oscillations in corticothalamic networks. Acta Neurobiol Exp 2000;60:
229-245.
161. Steriade M. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 2000;101:243-276.
162. Milner CE, Fogel SM, Cote KA. Habitual napping moderates
motor performance improvements following a short daytime nap.
Biol Psychol 2006;73:141-146.
163. Molle M, Marshall L, Gais S, Born J. Learning increases human
electroencephalographic coherence during subsequent slow sleep
oscillations. Proc Natl Acad Sci U S A 2004;101:13963-13968.
L
Kryger_6453_Ch 29_main.indd 347
8/24/2010 7:23:51 PM