Sleep Medicine Reviews 14 (2010) 219226

Contents lists available at ScienceDirect

Sleep Medicine Reviews

journal homepage: www.elsevier.com/locate/smrv

PHYSIOLOGICAL REVIEW

The emotional brain and sleep: An intimate relationship

Marie Vandekerckhove a, b, *, Raymond Cluydts b, c
a
b

Dept. Psychiatry, Jan Paljn Hospital, Koningin Fabiolalaan 57, 9000 Gent, Belgium
Dept. Biological Psychology, University of Brussels, Pleinlaan 2, 1050 Brussels, Belgium

a r t i c l e i n f o

s u m m a r y

Article history:
Received 4 September 2009
Received in revised form
12 January 2010
Accepted 12 January 2010
Available online 1 April 2010

Research ndings conrm our own experiences in life where daytime events and especially emotionally
stressful events have an impact on sleep quality and well-being. Obviously, daytime emotional stress may
have a differentiated effect on sleep by inuencing sleep physiology and dream patterns, dream content
and the emotion within a dream, although its exact role is still unclear. Other effects that have been
found are the exaggerated startle response, decreased dream recall and elevated awakening thresholds
from rapid eye movement (REM)-sleep, increased or decreased latency to REM-sleep, increased REMdensity, REM-sleep duration and the occurrence of arousals in sleep as a marker of sleep disruption.
However, not only do daytime events affect sleep, also the quality and amount of sleep inuences the
way we react to these events and may be an important determinant in general well-being. Sleep seems
restorative in daily functioning, whereas deprivation of sleep makes us more sensitive to emotional and
stressful stimuli and events in particular. The way sleep impacts next day mood/emotion is thought to be
affected particularly via REM-sleep, where we observe a hyperlimbic and hypoactive dorsolateral
prefrontal functioning in combination with a normal functioning of the medial prefrontal cortex,
probably adaptive in coping with the continuous stream of emotional events we experience.
2010 Elsevier Ltd. All rights reserved.

Keywords:
Sleep
REM-sleep
Emotion
Emotion regulation
Emotional adaptation
Brain

Introduction
Even though the relationship between pre-sleep emotional
experiences and quality of sleep, as well as the reason why we
sleep, seems intuitively evident, until recently this topic has gotten
increased attention. The scarce amount of research is surprising
given the importance of sleep in emotional well-being and the
occurrence of disturbed sleep in many psychological and psychiatric disorders. In this review, the scope will concentrate on the
relationship between emotion and sleep, particularly rapid eye
movement (REM)-sleep and its emotion modulatory and even
emotion regulatory functions in especially healthy individuals.
In the rst part, we review how to understand how emotional
situations affect sleep and how sleep affects emotional processing
of affective information. In the second part, the discussed ndings
are evaluated in light of neurophysiological insights.
Research ndings appear to conrm our own life-experience
where daytime events, especially emotionally stressful events, have

* Corresponding author. Dept. Biological Psychology, University of Brussels,

Pleinlaan 2, 1050 Brussels, Belgium. Tel.: 32 2629 15 94/9240 98 70; fax: 32 9240
98 75/2629 24 89.
E-mail addresses: marie.vandekerckhove@vub.ac.be (M. Vandekerckhove),
raymond.cluydts@vub.ac.be (R. Cluydts).
c
Tel.: 32 2629 25 29; fax: 32 2629 24 89.
1087-0792/$ see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.smrv.2010.01.002

an impact on the quality of our sleep and well-being. Daytime

emotional stress may have a twofold effect on sleep: rst by
inuencing sleep physiology and second by inuencing dream
patterns, dream content and the emotion within a dream, although
its exact role still is unclear. Even social phenomena such as reduced
social support and increased patterns of avoidance in a persons
emotion regulation, appear to result in psychological distress and
sleep complaints.1 Furthermore, the association between cortical
and emotional arousal and disrupted sleep in individuals with
insomnia suggests a strong relationship between daytime events
and disrupted sleep. As a matter of evidence, it is clear that the
individuals response and coping with the emotional stress associated with daytime events involves the capacity to de-arouse or
disengage from active wake processing interfering with the normal
initiation of sleep processes. Sleep latency, especially REM-sleep
alterations or abnormalities, have been related to variables associated with the affective state of individuals during the day.2
Watching aversive lms before sleep for instance, has been reported to inuence emotional experiences in the rst REM-periods of
the night.3 Reported effects of emotion and of pre-sleep mood and
stress on sleep include: decreased dream recall and elevated
awakening thresholds from REM-sleep,4 increased or decreased
latency to REM-sleep, increased REM-density, REM-sleep duration,5
occurrence of arousals in sleep as a marker of sleep disruption6 as
well as disturbances in sleep continuity.

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Acute stress
In some studies, investigating the effects of especially acute
stress exposure on sleep in healthy persons found that REM-sleep
alterations are more frequent than nREM-alterations. For instance,
in a study of Germain and others,7 they found that acute stress
exposure where subjects had been told that they had to give
a speech in the morning and that their performance would be
evaluated, resulted in an increase in REM-density across REMperiods, a decrease in late-night average REM-count and a slower
rate of increase across successive REM-periods immediately after
the stress exposure. The result that the average REM-density
increased is in line with some previous studies on the effects of acute
stress exposure.8,9 However, in other studies, acute stress exposure
has been associated inconsistently with increased percentage of
REM-density and REM-sleep duration10,11 or alterations within
REM- or nREM-sleep. Hall and coworkers12 correctly claim that the
pathways in which stress affects sleep and produces frequent
awakenings from sleep, lightens NREM-sleep, or affects the quantitative and qualitative components of REM-sleep are not as well
dened. In the case of clinical disorders subsequent to the experience of a traumatic life event, such as posttraumatic stress disorder,
also only a few studies investigated posttraumatic stress disorder
directly after the traumatic life event. In one such study investigating three patients hospitalized for acute combat fatigue, sleep
was fragmented, of short duration and characterized by high
motoric reactivity. REM-sleep had been found to be rare and short.13
Transient or chronic stress
REM-sleep alterations also have been found in people undergoing transient or chronic life events with and without comorbid
depression.9 With depression, a prolonged duration of the rst
REM-period, an increased density of eye movements, REMpercentage, and total sleep time have been reported.13,14 Also, in
suicide-attempters, an increase in REM-activity and REM-sleep
duration over the entire night and in the rst REM-sleep period
have been found.15 These abnormalities in patients with depression
in the rst non-REM/REM-sleep cycle16 have been related to the
dysfunctions in the emotional and cognitive processing in clinical
disorders such as depression.17 Also, a reduced REM-sleep latency
has been identied as an objective indicator of depressive disorder
and suicide.18 Furthermore, increased risk for relapse in depressive
persons and in alcoholics has been found to be related to increased
REM-density.8,19 Furthermore, at pre- and post-treatment psychotherapy, affect intensity in depressed men has been correlated
signicantly and positively with phasic REM-sleep measures,
characterized by REM-bursts.17,20 A decrease in REM-density, on the
other hand, has been correlated with remission with therapy and
reductions in negative affect intensity in depression.8,17,21 Phasic
REM-sleep decreases over the course of psychotherapeutic treatment in depressed patients, in comparison with more tonic aspects
of REM-sleep involving REM-sleep latency, wherein change may be
a marker of manifestations of depression.21 In correspondence,
failure to remit with psychotherapy in depressive persons has been
correlated with increased REM-density.14,8
In summary, abundant evidence conrms a relationship
between the emotional experiences we have during the day and
changes in sleep physiology, in particular modied, enhanced or
decreased REM-sleep.
Sleep and its impact on emotional well-being
Not only do daytime events affect sleep, the quality and amount
of sleep also inuences the way we react to these events and may

be an important determinant in general well-being. A good night of

rest seems to help us to feel good and to be able to cope with the
emotional challenges of the next day, especially with emotionally
painful events. Sleep seems restorative in daily functioning,
whereas deprivation of sleep makes us particularly more sensitive
to emotional and stressful stimuli and events. Even more, sleep
seems to buffer the relationship between stress and negative affect.
Probably, it plays a facilitating role in the processing and the
regulation of emotional stress. As we discussed previously, REMsleep in particular is affected by emotional events in daily life; the
way sleep impacts next day mood/emotion is thought to be
particularly affected via REM-sleep. REM-sleep appears to modulate our daily mood as well as to facilitate the integration of
affective life events into long-term memory.18,22 As a consequence,
sleep deprivation, and especially REM-sleep deprivation, has
a strong impact on the way we process, consolidate and buffer our
daily experiences. Globally, the effects of sleep deprivation have
been described on different levels of functioning, especially on the
cognitive (attention, memory), psychomotor or sensorimotor
(balance) level of functioning and on the level of mood (irritability,
dysphoria, malaise).23,24 Focusing on the emotional effects, they
also might be more obvious in daily life than the cognitive or motor
effects of chronic sleep restriction and acute sleep deprivation in
healthy individuals and animals. After a sleepless night or several
sleepiness nights, the experiences of feeling drowsiness,
awkwardness, getting irritated quickly and feeling down are
a common phenomenon. As both phenomena negatively inuence
each other, a vicious dysfunctional, even psychopathological, circle
might develop. Sleep disturbances not only restrict our daily
happiness, but even may have a prognostic meaning in predicting
mental well-being, emotional reactivity, adaptation to negative
affect and the evolution of affective disorders. Without enough
healthy sleep, negative emotional reactivity seems to be enhanced
signicantly and positive reactions to positive events often are
subdued.25 Adaptation to stress induced by an emotionally
arousing lm not only inuences sleep but has, as described before,
also been found to be reduced after REM-deprived sleep compared
with non-REM deprived or normal sleep.26 Enhanced signs of
anxiety to stressful stimuli after deprivation of REM-sleep in
comparison with non-REM-deprivation have been reported in
healthy subjects after reviewing the lm. The REM-deprived group
was signicantly more anxious after the second viewing of the lm
(autopsy) than the non-REM-deprived group. These ndings were
conrmed by Zohar et al.,25 who investigated the relationship
between sleep loss and emotional reactivity in medical residents
who were monitored for 57 days every 6 months over a two-year
period. The results show that sleep loss not only intensied negative emotions, but even diminished positive emotions following
a goal thwarting or goal enhancing event. Also, in animal studies,
suppression of REM-sleep during the second and third week of
postnatal development in rats using an antidepressant drug such as
clomipramine or a hypertensive like clonidine, showed enhanced
anxiety, decreased sexual activity and disturbed sleep among the
neonatally REM-sleep deprived animals.27 As a consequence, the
neonatal treated rats showed reductions in the cerebral cortex and
brainstem in adulthood. Another study in which REM-sleep in rats
was suppressed in a similar way as in the preceding study, the rats
showed depressive symptoms like despair behaviour, reduced
pleasure seeking and increased alcohol preference.28
Also, in studies with children and adolescents it has been shown
that sleep deprivation increases depression, confusion, and anger,29
subjective feelings of frustration and irritability/aggression.30 Even
after two nights of sleep deprivation, a signicant increase in
psychopathology scores in particular have been found for somatic
complaints, anxiety, depression and paranoia.31

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For depressive complaints, sleep deprivation was even associated with a mild increase in depressive thinking by including
feelings of powerlessness, failure, worthlessness, inadequacy, lack
of self-esteem and decreased life satisfaction. In line with these
ndings, social interpersonal functioning as investigated by Killgore and colleagues32 has been found affected. They found
a signicant decline in perceived emotional intelligence affecting
three major areas of functioning, including intrapersonal awareness, interpersonal skills and stress management.32 In another
study of this research group,33 sleep deprivation was associated
with an increase of extrapunitive responses that reected the
tendency to direct blame or hostility towards people or objects in
the environment. In other words, a decrease to accept blame for
a frustrating circumstance was found.
However, while summarizing these effects of sleep on
emotional functioning, a few opposing ndings have been reported,
too. Surprisingly, in a study of Wagner and coworkers,34 emotional
reactivity was enhanced on (familiar) affective pictures following
sleep during the late, REM-sleep rich part of the night in comparison with the effects of early sleep and wake periods. Wagner and
coworkers suggested that the increased negative valence ratings of
old pictures after late sleep suggest that REM-sleep enhances
aversive reactivity towards these stimuli. After a total night of 7 h of
sleep, the effect of increased emotional reactivity was even more
enhanced, suggesting a cumulative effect of REM-sleep periods
during early sleep and the longer REM-sleep periods during late
sleep. They concluded that some ndings conrm the relieving or
cathartic effect of REM-sleep. Replication of these results, given
most opposing results and thus confounding effects, is necessary.
However, in line with these former research ndings, are the effects
of sleep deprivation on depression. Total or partial sleep deprivation, or selective restriction of REM-sleep in depression, showed
that these acute sleep manipulations often lead to a temporary
improvement in energy and mood with a regression towards
depression after any subsequent sleep.35 The improvement of
mood has been found even stronger in evening types assessed by
the Hamilton Depression Rating (HDR) Scale.36 In line with the
discussed ndings, it also has been found that sleep deprivation is
followed by nights of increased REM-sleep and SWS (Slow Wave
Sleep).37 This rebound effect suggests that a certain amount of
these sleep stages is needed. Although the reason why it is necessary is still unclear, these ndings nearly consistently let us assume
that REM-sleep may have an adaptive emotion modulatory function, whereas in accordance with this function, deprivation of REMsleep reduces this adaptive functioning.
REM-dreaming as emotion modulatory function?
Characteristic to emotional stress is that it may inuence
dreaming and dream content as has been shown after watching
a stressful lm shortly before sleep.38 Dream content includes
a series of images, thoughts, affects, emotions and sensations. The
emotional character of dream content leads to the question of
whether it plays a role in the regulation or adaptation of emotion. Or,
can we suggest that the dream is just another series of brain
processes among others combining memories and experienced
emotions? Several studies suggest an enhanced role of REM-sleep in
more emotional processing tasks in comparison with non-REMsleep. In a review, Payne & Nadel20 conclude that dream content
varies as a function of sleep stage or time of night. Dreams seem to be
more vivid and emotionally loaden during REM-sleep in comparison
with dreaming in other sleep stages like NREM-dreaming where
they have been found to be more of a thought-like cognitive
nature.38 In REM-sleep, mentation has been found to be more
expressive of motives and emotions,40,41 emotional vividness,

221

intensity or complexity, which leads us to suggest a qualitative

difference between REM and NREM mentation and processing,
where REM-sleep has a more clear emotional dream-like character
in comparison with NREM-dreaming.42 InQ research of Cartwright
and coworkers, the role of daytime emotion in sleep and in REMdream functioning has been investigated several times. For instance,
they investigated people who divorced recently from a marital
partner. Subjects were awakened in the sleep lab several minutes
after REM-sleep onset for dream collection.10 Each participant was
assessed for depression at baseline and at 1-year follow-up. Sleep
was monitored for three nights at each assessment point. Dream
characteristics appear to respond adaptively during life events, but
delayed when subjects are depressed. One year later, 72% of the 39
participants classied as suffering from depression could be classied correctly as remitted or not remitted based on the presence of
negative/unpleasant dreams during awakenings from REM-sleep at
baseline. Subjects who were not depressed at the time of divorce or
later on had few negative dreams throughout the night and subjects
who were depressed at the time of divorce but were not one year
later, had a higher percentage of negative dreams early in the night
and less late at night. The direction of the relationship was that the
more expression of negative affect in dream reports arising from
REM-awakenings during the rst half of the night, the less likely the
person suffered from depression one year later.
In another study, Cartwright and coworkers10 did similar
research on a non-depressed group of normal students. Before and
after each night of sleep, they lled out a mood scale. The second
night they were awakened after several minutes of each REMperiod and asked to report what they had been experiencing. The
students who were more depressed showed better moods after
dreaming. Even the content of dreaming was inuenced by the
presence of a negative mood before sleep. The dreams contained
more negative affect and less positive affect early in the night, with
the negative ones decreasing and the positive ones increasing. This
effect could not be found when there was no negative mood before
sleep. Cartwright and coworkers concluded that a depressive mood
correlates with negative dream content and that the modulatory
function of REM-sleep dreaming appears when a negative mood is
moderate.
Similarly, in a study of Foulkes,39 he found that when subjects
reported in a spontaneous way about their dreams there was a bias
towards the recall of emotionally unpleasant, more dramatic,
especially anxious loaded contents. On the other hand, in a study of
Fosse et al.,43 emotion in sleep was investigated by the use of
instrumental awakenings. Subjects themselves had to score
segments of their reports for the presence of emotions. Combining
rst-person ratings with instrumental awakenings from REM, they
found more positive emotions (joy/elation) reported compared to
negative emotions. The authors warned that this might reect
characteristics of the group.43 In contrast, other studies using this
method of instrumental awakening reported more negative
emotions such as anger and fear.10,44 Even when we take into
account that dream reports are always given in a waking state and
therefore are constrained by the actual state of the person as well as
the cognitive and linguistic abilities of the individual, we notice in
most studies a clear tendency towards reporting of negative
emotions.
Sleep and emotion on the neurophysiological level
Limbic system
Emotion modulatory functions of sleep involves the limbic and
extended limbic system. Sleep neuroimaging studies in humans
have shown that neuronal activity in amygdala and anterior

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paralimbic cortices, including the medial prefrontal cortex, varies

across the sleepwake cycle. Of particular relevance to the anatomy
of REM-sleep are the forebrain structures that are essential to
motivation and emotion-lateral hypothalamic- and limbic areas
including the amygdaloid complex.4547 In REM-sleep, enhanced
activations have been found in the pontine tegmentum, thalamic
nuclei, primary visual cortex, both amygdaloid complexes, hippocampal formation, anterior cingulate cortex and parietal operculum.46,48,49 Also, Payne and Nadel20 found activations in the
amygdala and parahippocampal gyrus that may be related to dream
generation during REM-sleep but did not nd hippocampal activation, as Maquet and coworkers did. On the other hand, Braun
et al.45 conrmed the ndings of Maquet and coworkers of REMrelated brainstem, limbic and paralimbic activations. In REM-sleep
compared to delta NREM-sleep and to pre- and post-sleep waking,
they showed relative activation of the pons, midbrain, anterior
hypothalamus, the hippocampus, the caudate, the anterior cingulate, and medial prefrontal, caudal orbital, parahippocampal and
inferior temporal cortices. Also, posterior cortices in temporooccipital areas are activated related to the visual character of
dreaming. Hippocampal and parahippocampal areas, together with
the occipital area, have been found to be more active during the
processing of visual stimuli and the recall of images.50 Structures
such as the medial temporal lobe, especially the hippocampus, are
involved in the formation of a temporally ordered retrieval storage
for neocortically stored information. Integration of semantic
explicit memory content as well as masked or unmasked more
episodic autobiographical recollection in dream content may be
mediated by a distributed frontotemporoparietal system.51 The
right parietal operculum, which is activated during REM-sleep, can
be related to spatial imagery active in the processing of situations
and memories in dreaming.46 Hippocampus-independent declarative memories of lower emotional valence seem to rely on early
nocturnal sleep when slow-wave sleep (SWS) prevails and cortisol
release is minimal.52 Nonconscious nondeclarative memory such as
procedural memory (i.e., knowing how), as well as implicit
affective processing and learning within dreaming, seems to be less
dependent on medial temporal lobe structures and more on
sensorimotor and limbic regions such as the amygdala. The amygdala and the hippocampus are among the most active brain
structures during REM-sleep, a condition which is likely to favor
amygdalahippocampal interactions compared to NREM-sleep.
More amygdala-dependent emotional memory is supported by
late sleep, when REM-sleep predominates. Emotion processing,
emotion regulation and integration into memory not only involve
the processing of emotional information during wakefulness, but
especially reprocessing during the night. The mediotemporal and
limbic system is known to inuence these emotion processes night
and day.
Amygdala
REM-related brain activation is rich in afferentation from the
amygdala and those areas that are deactivated in REM-sleep are
poor in afferentiation.46 Activation of the amygdala varies across
the sleepwake cycle, with higher neuronal ring rates during
wakefulness and REM-sleep compared to NREM-sleep.46 More
specically, in a recent fMRI-study53 during phasic REM-periods,
the thalamocortical network including limbic and parahippocampal areas, is particularly active. The amygdala, deep inside
the antero-inferior region of the temporal lobe, connects with the
hippocampus, the septal nuclei, the prefrontal area and the medial
dorsal nucleus of the thalamus. These connections make it possible
for the amygdala, together with these other brain structures, to play
an important role in assigning affective meaning and signicance to

experiential stimuli initiating emotional arousal and affective

learning. Affective meaning initiates the handling and coping of
demanding situations such as the cognitive control of stress and
major affective processes. Although the amygdala clearly tends to
respond to stimuli that predict threats or to threatening stimuli
such as fearful or angry faces, a more general role is to modulate the
organisms overall state of vigilance, wakefulness and, in the face of
ambiguous stimuli, to potentiate higher order cortical structures for
subsequent information processing.54 Due to this overall anatomical connectivity, the amygdala also is in a particularly good position to inuence key regions involved in cardiovascular regulation
like the hypothalamus and the parabrachial complex in the brainstem. More specically, the central nucleus of the amygdala with
afferent and efferent connections with the parabrachial area and
dorsal raphe nuclei appears to be associated with activation of the
area involved not only in emotional processing but also in the
regulation of sleep and wakefulness. In particular, as discussed
before, phasic REM-sleep has been considered as the EEG-variable
inuenced by day-to-day limbic changes in emotional state.2 Phasic
REM-sleep measured by REM-activity and REM-density is dened
by the presence of phenomena correlated with ponto-geniculooccipital spike activity. The REM-related activation of the primary
visual cortex without visual input from the retina provides neural
evidence for the ponto-geniculo-occipital waves (PGO-waves) and
a link between REM-sleep and dreaming. PGO-waves are related to
sensory-motor integration, dreaming, learning and development of
the visual system.55 Electrical stimulation of the central nucleus of
the amygdala during REM-sleep has been found to increase PGOwave amplitude, whereas stimulation during non-REM-sleep
decreases PGO-wave frequency. The results indicate that the
amygdala not only has a central role in emotion processing but also
is involved in the modulating brainstem neural mechanisms
underlying alertness during sleep and wakefulness.

Cingulate cortex
Among these limbic areas with their extensive connections with
the amygdala, the anterior cingulate cortex active during REMsleep generally functions as a mediator between acts of attention
and emotion and affective consciousness. The anterior cingulate
activity accompanies the representation and affective awareness of
almost all stimuli. It contributes to the affective character and
motivational salience of dreaming, expressed in the ctive actions
during dreaming. Premotor areas of the anterior cingulate cortex
might even integrate dream movement and emotion.56 More
specically, the precuneus and midline cingulate regions appear to
be connected functionally with all types of awareness of stimuli and
reective self-aware processing or self-related information processing across all sensory modalities. Related to this function, the
hypoactivation of the precuneus, next to and traditionally considered as a totality with the posterior cingulate cortex adjacent to the
medial parietal cortex, helps partly to explain why there is little
access of episodic memories.57 Together with the deactivation of
the dorsolateral cortex, activation of the hippocampus, the right
inferior parietal lobe a brain region involved in spatial imagery
construction and the processing of emotionally inuenced
memories in REM-sleep, we can speculate that the underactivation
of the precuneus also explains the rather non-self-reective character of dreaming, with only fragmented self-related episodic/
autobiographical memory retrieval activation during sleep due to
a global lack of directed self-reective processes. Self-reective
processes and propositional representations of the experiences of
the self in awareness or self-awareness not only require the
posterior cingulate cortex but also higher executive processes

M. Vandekerckhove, R. Cluydts / Sleep Medicine Reviews 14 (2010) 219226

requiring dorsolateral prefrontal involvement in particular, which

is deactivated in REM-dreaming.
Inferior parietal lobe
Maquet et al.47 reported activation of the right parietal operculum during REM-sleep, despite general deactivation in much of
the parietal cortex. The inferior parietal lobe may be involved in the
visualization of a ctive situational dream space in the total experience of dreaming. It may have a role in various aspects of mental
and spatial imagery like mental moving through a spatial contextual environment. Within dreaming, the individual falls together
with his own actions while there is little or no space left for mental
perspective taking. The deactivation of the temporo-parietal junction may reect diminished functioning of social perspective
taking, in identifying the goals or intentions behind behaviors in
particular as well as the switch between rst and third person
perspective and theory of mind (e.g.,58). During REM-sleep, the low
activation of the right temporo-parietal junction may be related to
a loosening of the distinction between rst and third level
perspectives. It is only in a retrograde dream report that the self can
participate in the dream action both in a rst-person (i.e., the self
sees and acts) and in a third-person (i.e., the dreamer sees the self
acting in the dream) perspective. Especially perspective-taking
relevant social emotions such as jealousy, pride, embarrassment,
infatuation, sexual love, shame, guilt and pride often are reported in
dreaming.59
The (dorsolateral) prefrontal cortex
The prefrontal lobes commonly are deemed to be the seat of the
highest mental function, playing a prominent role in engendering
higher levels of awareness. Interacting closely with other brain
areas such as the amygdala, the parietal and cingulate cortex, the
prefrontal cortex, especially medial regions, play a central role in
the representations of the self,60 the processes of being aware of
oneself and ones perspectives in the world. The frontal lobes allow
us self-regulation in function of our self-referential anticipation of
future possibilities in the context of personal attributions, goals and
aspirations. In REM-sleep, reective thought and self-reection
anticipating future goals and situations seem to be absent or rather
minimal. The reective self permits us to be aware of oneself,
opposed to the rather unknowing non-reective experience of
oneself during sleep and during dream activity. Also, in the selection of information entering consciousness and self-reection, the
organization of information awareness and memory and
the searching after specic memories, as well as the initiation and
the maintenance of higher intentional behaviors, the executive
capacities of the prefrontal cortex and the dorsolateral prefrontal
cortex in particular are of major importance. During REM-sleep,
activity in the dorsolateral prefrontal cortex and locus coeruleus
drops to the lowest levels of the day, as a consequence, the feedback
these areas normally give is disenabled.61 The dorsolateral frontal
cortex receives input from the motor cortex as well as from the
multimodal sensory convergence areas of the parietal and temporal
lobes. Within sleep and dreaming, it seems as if there is no clear
selective information process entering in awareness that might be
served by the dorsolateral prefrontal cortex, whereas the caudal
dorsal cortex is more involved in visual control and the ventral and
rostral prefrontal cortex in episodic control (e.g., the selection of
information according to events that occurred in the past).47 In
a state of being awake, the dorsolateral cortex can evaluate and
regulate information from the affective-somatic sensory system to
the motor cortex to increase a response, whereas during sleep due
to its inactivity, there is a relative lack of intentional and coherent

223

movement. In particular, in REM-sleep, the deactivation of the

anterior prefrontal areas and of the dorsolateral prefrontal cortex
may explain the little notion of directed and relevant goal-oriented
behavior or self-regulation and the loss of working memory and
logic reasoning.62,47 During dreaming, the sequence of dream
events cannot be controlled. Sleep especially is characterized by the
lack of own intentional instrumental behavior or retrieval of clear
or intact episodic memories. The retrieval of episodic information,
for instance, is dependent on a proper functioning of the (dorsolateral) prefrontal cortex and several other related brain structures
like the medial temporal area.51 As a consequence, some fragments
or aspects of memories as residues are noticeable in dreaming
through the activation of the medial temporal lobes, but do not
result in an exact realistic unfolding of an autobiographical event
with an episodic character in time and context. Due to its important
general control functioning, deactivation of the prefrontal cortex
also explains the destructive effects of sleep deprivation. Prefrontal
cortex activation is reduced signicantly even after 24 h of
continuous wakefulness.63 Accompanied by decreased prefrontal
activation is the decrease in prefrontal related functions. As we
discussed before, sleep deprivation results in dysfunctional
prefrontal topdown processing and control. A night of sleep
deprivation decreases performance on neuropsychological tasks
subserved by the prefrontal cortex.56 However, other studies did
not conrm these decits in executive function following one
nights sleep deprivation, which may be due to their adaptation on
a normal sleep deprived state of living.64 As illustrated previously,
lack of sleep inappropriately modulates the human emotional brain
response to negative aversive stimuli. Prefrontal regions usually are
held to comprise central components of the highest order control
and modulatory system for emotion. They contribute to reality
monitoring and top-down levels of control, which explains the loss
of reality and onlogical character of dreams. We hypothesize that
the diminished prefrontal control may enable the sleeping brain to
increase signicantly the adaptive and necessary processing of
emotions related to ongoing or unnished negative life experiences. We suggest that the relatively non-disturbed affective
working through of emotional information, not only during
daytime but also during the night, might be possibly more adaptive
in facilitating especially painful emotional processing and stress
regulation (cf. Vandekerckhove, Houthuys, Weiss, De Valck, Cluydts
et al. in preparation).
Furthermore, during REM-sleep we notice reactivation in other
important emotion regulation areas such as the caudal orbital and
medial prefrontal area.45,62 With the onset of REM-sleep, accompanied with continued deactivation of anterior and lateral portions
of the prefrontal cortex, posterior prefrontal areas and parts of the
ventromedial, limbic-related prefrontal cortex and closely associated the medial subcortex and cortex, have been found reactivated
sometimes to levels that exceed those of waking.
Ventromedial prefrontal cortex
There have been only a few studies that focused on the relationship between the human ventromedial prefrontal cortex and
natural sleep, especially REM-sleep. The ventromedial prefrontal
cortex consists primarily of the orbitofrontal cortex and the anterior cingulate cortex, and also is known as the limbic cortex
important in decision making and social judgment.56 In particular,
the orbitofrontal cortex enables the more complex higher order
abstract processing of the neocortex to be integrated with the
lower order somatic and emotional functions of the deeper
structures, integrating input from the limbic area and the cortex.
This area receives input from different sensory modalities whereby
pathways between the amygdala and the orbitofrontal cortex may

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M. Vandekerckhove, R. Cluydts / Sleep Medicine Reviews 14 (2010) 219226

serve to place sensory and affective stimuli in the appropriate

context for action. The orbitofrontal cortex controls the sympathetic and parasympathetic branches of the autonomic nervous
system and thus cardiac and respiratory responses in emotional
and stressful situations in dream-sleep. In correspondence and in
daily life, especially with the assistance of other prefrontal- as well
as limbic functions, it has an important function in social knowledge on how to behave, the selection of appropriate behavior and
emotional, social and interpersonal self-regulation.65 During sleep,
especially REM-sleep rather than NREM-sleep, together with the
amygdala and the anterior cingulate cortex, the orbitofrontal cortex
is active in emotional and social processing in particular,46,62 which
may explain the adaptive functioning of these areas in a more free
and unlimited processing of especially social and emotional events
that happened during the day characterized by the overwhelming
emotional character of many dreams.
Speechless limbic functioning during REM-sleep adaptive in
the coping with the continuous stream of emotional
life-events?
Alterations in daily life events and also in emotional and
cognitive processing during wakefulness, such as the experience of
an emotional event or depressive functioning, becomes expressed
in sleep, especially in REM-sleep.17 In correspondence, deactivation
of the prefrontal cortex not only has been found in REM-sleep, but
also has been found consistently in psychopathological states such
as depression and posttraumatic stress disorder.66 In the extreme
case, without specic prefrontal feedback regarding the level of
threat, the organism is locked in an amygdala-driven response state
longer than necessary and may activate overwhelming stressful
emotional responses associated with enhanced levels of stress
hormones. Overwhelming emotions or apparently uncontrollable
situations within dreaming, immersed with driving feelings as fear
and anxiety are satised by idiosyncratic dreaming plots, may be
the result. What happens during dreaming can thus be compared to
some extent with a posttraumatic stress disorder where a negative
correlation between amygdala and prefrontal activation in
responses to fearful versus happy faces has been found.67 In other
words, in anxiety disorders such as posttraumatic stress disorder
and depression, similarly as in sleep, we also notice an enhanced
emotional processing and thus an increased activation of the
amygdala with a low activation of the prefrontal area involved in
the modulation and inhibition of the amygdala. The amygdala and
prefrontal cortex are neurological correlates of emotional disorders
inuencing the regulation and expression of REM- and NREMsleep. A hyperactive limbic activation in combination with a hypoactivation of the prefrontal area may cause or sustain increased
affective processing. Diminished capacity of the regulatory function
of the dorsolateral cortex may result in irrational behavior, like
disinhibition of affect and behavior. During dreaming, similarly to
the processes during posttraumatic stress disorder in wakefulness,
the processed information may be organized and follow some still
unknown logic, where the brain combines certain aspects of life by
inhibiting some and selecting others, resulting in an under- or
overrepresentation of certain themes and emotions.
However, activated patterns of brain area in affect-related
disorders such as PTSD, are only partly similar to the patterns of
active brain area in REM-sleep. In REM-sleep we see at the onset of
REM-sleep, for instance, a reactivation of the medial prefrontal area
which is deactivated in PTSD or anxiety disorders. This reactivation
in REM-sleep is probably functional in the regulatory and modulatory function of REM-sleep. Generally speaking, the engagement
of the amygdala and the cingulate cortex in the emotion regulation
of painful information during the day or during sleep becomes

especially modulated and regulated by the medial prefrontal cortex

while it exerts a top-down regulatory function of amygdala functioning.68 The activation of the amygdala, the anterior cingulate
cortex, the superior parietal cortex, the superior and medial
prefrontal cortex have, as we suggest, an adaptive and healthy role
in emotion modulatory and regulatory functions, processing and
integrating traumatic and other distressing emotions and memories in REM-sleep.26
During REM-sleep relative to emotional disorders in waking time,
there is a diminished functioning of the working memory and
executive function circuit combined with an enhanced adaptive
functioning of networks subserving emotional and memory
consolidation processes necessary to cope with the events we meet
during daily life. In line with these ndings, dreaming may be
functional to process aversive experiences such as traumatic experiences, presented under strange images and fragmented episodes of
related or similar stories. REM-sleep and dreaming functions are
a crucial phase of the masked or unmasked reactivation and
reprocessing of emotions and emotional occurrences during the day.
Even more, REM-sleep has been assumed to have a role in
integrating traumatic and other distressing memories into
memory. Overnight improvement of memory is specically sleep
and not time dependent and correlates positively with the amount
of both early-night SWS- and late-night REM-sleep.69 Vividness
and emotionality also are strong determinants within the integration of memories into long-term memory and subsequent recall.
Not only emotional and other kinds of information become
consolidated in memory during sleep but, as we discussed in the
beginning, sleep also becomes changed by events that happened
before sleeping. This might lead to an increase in REM-sleep, sleep
spindle density, etc.70 As we discussed previously, not only the
representation of emotional events becomes changed but also the
architecture of subsequent sleep stages. It promotes the reactivation
of neural ensembles during subsequent sleep. Changes in motivation
and emotion are prominent aspects in mood disorders related with
alterations in limbic processing not only in daytime, but also during
REM-sleep. Every reprocessing in dreaming, such as the reconsolidation of negative stressful events visually appearing in conversions
or transformations of what has happened in the day, may be functional to integrate negative experiences into long-term memory and
may help us to be prepared for future negative experiences.
Even when we consider some opposing ndings (e.g., Wagner
and colleagues), it appears that the dream-production especially in
REM-sleep that contains vivid simulations of painful and threatening events within real life, facilitates the processing of distressing
emotions. Earlier REM-sleep onset and higher dream activity in the
initial REM-period even has been found to predict a greater
reduction of depressive symptoms after a distressing life event. It
aids the processing of negative information, making aversive events
bearable. In particular, intensication of phasic REM-sleep appears
to be a marker of dysfunctional or too little emotion regulation
during the day, indicating the need for further emotion processing
and emotion regulation during sleep. REM-sleep after stress may
function as a regulatory mechanism of waking emotional arousal.7
Also, increased phasic REM-sleep in persons suffering from stress
possibly may reect an incapacity to down-regulate experienced
emotional arousal during sleep or during the day.
As a consequence, the adaptive inuence of REM-sleep on the
regulation of emotion appears to be reduced after REM-sleep
deprivation in comparison with non-REM-deprived or undisturbed
sleep.26 Sleep deprivation interferes with the processing and integration of negative information such as painful life events into
memory, affecting psychological well-being and health. It changes
the metabolic activity within several crucial affect-regulating areas
of the brain like the medial prefrontal cortex. Without enough

M. Vandekerckhove, R. Cluydts / Sleep Medicine Reviews 14 (2010) 219226

healthy sleep, negative emotional reactivity seems to be enhanced

signicantly and positive reactions to positive events often are
subdued.25 The discussed studies of Killgore and coworkers even
suggest that sleep deprivation diminishes moral behavior,
responsible behavior, interpersonal skills and inventiveness. As we
discussed before, sleep disturbances not only restrict our daily
well-being and social functioning, but even may have a prognostic
meaning in the evolution of affective disorders like depression.
In longer periods of sleep deprivation, the brain has more difculties processing emotionally stressful and complex social events in
an adaptive way. As sleep or REM-sleep serve the modulation of
emotional and motivational drives, making the individual more
adaptively exible during wakefulness, REM-deprivation may lead to
increased excitation in many brain structures, resulting in enhanced
emotional and drive-motivated behavior.17 For instance, morning
mood improves when REM-sleep is intact but worsens after a night of
sleep deprivation.10 After deprivation of sleep, the normal regulation
of the amygdala fails. Increased activation of the amygdala and a loss of
functional connectivity with the medial prefrontal cortex occur. Sleep
deprivation is characterized by an increased attention and reactivity
towards aversive emotional information. Together with the decrease
in prefrontal activation, emotion regulatory functions become
dysfunctional. A night of sleep may therefore repair adaptive processing and functional brain activity and the integrity of the medial
prefrontal cortex-amygdala connections. Although we notice the
negative effects of sleep deprivation in healthy subjects, positive
effects of REM-deprivation on depression questions the therapeutic
function of REM-sleep. In line with Cartwright et al.,10 there might be
a oor and a ceiling effect. As a consequence of the positive effect of
REM-sleep deprivation on depression, REM-sleep should be functional
on specic and relatively normal grades of negative affect.10 The more
direct positive regulating effect of REM-sleep occurs in normal levels of
negative mood and not when higher levels of negative emotion should
be regulated.10 In major depression, a higher amount of REM-sleep,
poor sleep efciency, and reduced amounts of delta sleep have been
reported. Also, dream affect is more negative. Cartwright et al. suggest
that the loss of these unpleasant dreams and the reduction of eventual
dysfunctional REM-sleep might account for the positive effect of
REM-deprivation, whereas a longer deprivation of REM-sleep followed by a night of sleep intensies REM-sleep and dream affect. This
effect of rebound may reect the adaptive function of REM-sleep as
processing through, which may explain this mood improvement in
depression. Another possible explanation is that REM-sleep-deprivation alleviates clinical depression because it mimics selective reuptake
inhibitors (SSRI) that should be linked with increased brain derived
neurotrophic factors (BDNF) in major depression.71
In summary, these data suggest an amplied, hyperlimbic
response by limbic area to negative emotional information under
conditions of REM-sleep as well as in sleep or REM-deprivation.
Furthermore, this increased magnitude of limbic activity is associated with a loss of functional connectivity with the dorsolateral
prefrontal cortex and ventromedial prefrontal cortex during the day,
suggesting a failure of top-down, prefrontal control which, in the
case of REM-sleep deprivation, becomes repaired after a night of
normal sleep. During sleep, the ventromedial prefrontal area
becomes reactivated, which in combination with enhanced limbic
functioning, explains the inuence of REM-sleep, especially
in emotion modulatory functions and on the integration of
emotional events in sleep. Considering the discussed ndings,
we noticed an enhanced effective emotional adjustment and
amelioration of mood and well-being after intact sleep, especially
REM-sleep.
In other words, good sleep may work as a biobehavioral regulatory and restorative process regulating daily emotional experiences and allostatic loads of emotional stress.23

225

Practice points
Research findings confirm our own experiences in life where
daytime events and especially emotionally stressful events
have an impact on sleep quality and well-being:
1. Daytime emotional stress has an effect on sleep physiology by elevated awakening thresholds from REM-sleep,
increased or decreased latency to REM-sleep, increased
REM-density, REM-sleep duration and the occurrence of
arousals in sleep as a marker of sleep disruption.
2. Daytime emotional stress affects dream patterns, dream
content and the emotion within a dream as well as
decreased dream recall, although its exact role still is
unclear.
3. Not only do daytime events affect sleep, the quality and
amount of sleep also influences the way we react to
these events and may be an important determinant in
general well-being.
4. Sleep seems restorative in daily functioning, whereas
deprivation of sleep in opposition makes us particularly
more sensitive to emotional and stressful stimuli and
events.
5. The impact of sleep on next day mood/emotion is
thought to be particularly affected via REM-sleep.
6. In REM-sleep, a hyperlimbic and hypoactive dorsolateral
prefrontal functioning and a normal functioning of the
medial prefrontal cortex may explain its adaptive role in
the coping with the continuous stream of emotional
events we experience.

Research agenda
Experimental research is needed to explore the exact role of
sleep and its different stages in emotional processing,
emotional learning and emotion regulation.
Neurophysiological research is needed on the role of the
amygdala, the anterior cingulate cortex and orbitofrontal
cortex in sleep in the processing of emotion and painful life
events.

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