Sleep and Affect: Assessment, Theory, and Clinical Implications

490 Pages·2015·7.51 MB·English

by  Kimberly Babson

SLEEP AND AFFECT
Assessment, Theory, and Clinical
Implications
SLEEP AND
AFFECT
Assessment, Theory, and
Clinical Implications
Edited by
K A. b
imberly Abson
National Center for PTSD and Center for Innovation to Implementation, VA Palo Alto Health
Care System, Menlo Park, CA, USA & Department of Psychiatry and Behavioral Sciences,
Stanford School of Medicine, Stanford, CA, USA
m t. F
Atthew eldner
Department of Psychological Science, University of Arkansas, Fayetteville, AR, USA &
Laureate Institute for Brain Research, Tulsa, OK, USA
AMSTERDAM (cid:127) BOSTON (cid:127) HEIDELBERG (cid:127) LONDON
NEW YORK (cid:127) OXFORD (cid:127) PARIS (cid:127) SAN DIEGO
SAN FRANCISCO (cid:127) SINGAPORE (cid:127) SYDNEY (cid:127) TOKYO
Academic Press is an imprint of Elsevier
Academic Press is an imprint of Elsevier
32 Jamestown Road, London NW1 7BY, UK
525 B Street, Suite 1800, San Diego, CA 92101-4495, USA
225 Wyman Street, Waltham, MA 02451, USA
The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK
© 2015 Elsevier Inc. All rights reserved.
Front cover credit: “Sleep Stage N3” by NascarEd - Own work. Licensed under Creative
Commons Attribution-Share Alike 3.0 via Wikimedia Commons -http://commons.wikimedia.
org/wiki/File:Sleep_Stage_N3.png#mediaviewer/File:Sleep_Stage_N3.png
No part of this publication may be reproduced or transmitted in any form or by any means,
electronic or mechanical, including photocopying, recording, or any information storage
and retrieval system, without permission in writing from the publisher. Details on how
to seek permission, further information about the Publisher’s permissions policies and
our arrangements with organizations such as the Copyright Clearance Center and the
Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions.
This book and the individual contributions contained in it are protected under copyright by
the Publisher (other than as may be noted herein).
Notices
Knowledge and best practice in this field are constantly changing. As new research
and experience broaden our understanding, changes in research methods, professional
practices, or medical treatment may become necessary.
Practitioners and researchers must always rely on their own experience and knowledge
in evaluating and using any information, methods, compounds, or experiments described
herein. In using such information or methods they should be mindful of their own safety
and the safety of others, including parties for whom they have a professional responsibility.
To the fullest extent of the law, neither the Publisher nor the authors, contributors, or
editors, assume any liability for any injury and/or damage to persons or property as a
matter of products liability, negligence or otherwise, or from any use or operation of any
methods, products, instructions, or ideas contained in the material herein.
British Library Cataloguing in Publication Data
A catalogue record for this book is available from the British Library
Library of Congress Cataloging-in-Publication Data
A catalog record for this book is available from the Library of Congress
ISBN: 978-0-12-417188-6
For information on all Elsevier publications
visit our website at http://store.elsevier.com/
Foreword
Interrelationships between Sleep and Affect
Edward Pace-Schott
Harvard Medical School and Massachusetts General Hospital, Boston, MA, USA
Sleep and Affect: Assessment, Theory, and Clinical Implications provides the
first comprehensive review of the emerging synthesis between the affec-
tive neurosciences and sleep psychology and medicine. Researchers fre-
quently hypothesize that normal sleep helps regulate emotions in healthy
humans (e.g., Cartwright, Luten, Young, Mercer, & Bears, 1998; Dahl
& Lewin, 2002; Deliens, Gilson, & Peigneux, 2014; Germain, Buysse, &
Nofzinger, 2008; Goldstein & Walker, 2014; Kramer, 1993; Levin & Nielsen,
2007; Soffer-Dudek, Sadeh, Dahl, & Rosenblat-Stein, 2011; Walker, 2009;
Walker & van der Helm, 2009). The bulk of the empirical evidence sup-
porting this assertion has emerged only recently, however, and it rep-
resents a dynamic and expanding field of inquiry brought together in this
volume. After introducing key concepts and methodologies in each field,
the book discusses the interactions between sleep and the full complement
of negative and positive emotions, while explaining the clinical implica-
tions of those interactions. Some relationships between sleep and emotion
have been widely studied, especially in the context of mood and anxi-
ety disorders, whereas researchers are only beginning to examine others,
such as the possible link between sleep quality and anger. Once we have
considered the more general interactions between sleep and emotion, we
explore how these interactions manifest in special populations such as
children and adolescents, among whom sleep problems may presage and
even contribute to later psychiatric disorders. Importantly, this volume
deals with sleep and emotion across the spectrum of mental health from
the normal covariance of mood and sleep to the pathological extremes.
People often take for granted the fact that sleep profoundly affects
one’s emotional state. In most cases, a good night of sleep improves mood,
along with other subjective experiences of mind-body health such as rest-
edness and stamina. In fact, the absence of such benefits can be associated
with symptoms of sleep or psychiatric disorders, referred to as nonre-
storative sleep or anxious awakenings. As a tried and true adage of folk
psychology, the individual expects to be a different person after a good
night’s sleep. So, what takes place across sleep in healthy individuals to
produce such a reliable change? In part, improved mood is expected to
result from sleep based on Borbely’s two-process model (Borbely, 1982)
in which sleep propensity results from an interaction between circadian
xiii
xiv FOREWORD
and sleep-homeostatic factors. For example, circadian rhythms, such as
the preawakening rise in cortisol (Kalsbeek et al., 2012) and the cortisol
awakening response (Federenko et al., 2004), are believed to prepare us
for the challenges of the new day, and these processes could promote a
sense of vigor upon awakening. Similarly, having slept away homeostatic
sleep pressure and reduced levels of endogenous somnogens, such as
adenosine (Porkka-Heiskanen & Kalinchuk, 2011), in the central nervous
system (CNS), one might expect to experience improved mood, which can
be further boosted by the adenosine-receptor antagonist, caffeine (Fisone,
Borgkvist, & Usiello, 2004). An abrupt change in the forebrain’s neuro-
modulatory milieu also coincides with abundant REM sleep late in the
sleep period, during which monoamines, such as serotonin, are at their
nadir, ending when the individual wakes, at which time they return to
high levels (Pace-Schott & Hobson, 2002). Such state-dependent changes
are undoubtedly important for producing a mild morning euphoria (with
notable exceptions being many adolescents and evening chronotypes!).
Other nightly changes promote enduring aspects of emotional health
regardless of waking mood, however. Such changes have now become
long-overdue subjects of many scientific investigations, such as those ad-
dressing the sleep-dependent consolidation of emotional memories, and
this volume provides the first systematic compendium of their findings.
These new investigations into sleep and emotion are increasingly nec-
essary, given the well-documented trend toward voluntary curtailment
of sleep in Western societies, a trend that may be broadly problematic
for physical, mental, and, especially, emotional health. From the 1950s
to the first decade of this century, average sleep duration in adults has
decreased from over 8 to under 7 h per night (Van Cauter, Knutson,
Leproult, & Spiegel, 2005). Recent research has shown that many phys-
iological systems are negatively influenced by insufficient sleep (Van
Cauter et al., 2007). For example, sleep deprivation is associated with
endocrine abnormalities such as elevated evening cortisol (Leproult,
Copinschi, Buxton, & Van Cauter, 1997), immunological abnormalities
such as increased inflammatory markers (Mullington, Haack, Toth,
Serrador, & Meier-Ewert, 2009; Pejovic et al., 2013), and heightened risk
of cardiovascular disease (Solarz, Mullington, & Meier-Ewert, 2012).
Similarly, sleep deprivation is associated with metabolic abnormalities
contributing to obesity, insulin resistance, and, ultimately, type II di-
abetes (Knutson, Spiegel, Penev, & Van Cauter, 2007). Sleep disorders
such as obstructive sleep apnea and insomnia are linked to hypertension
(Fernandez-Mendoza et al., 2012; Palagini et al., 2013) and elevated sym-
pathetic nervous system activity (Zhong et al., 2005). Notably, many of
these physiological abnormalities can be reversed by naps or recovery
sleep (Pejovic et al., 2013; Vgontzas et al., 2007). Although emotional state
is intimately linked to physiological homeostasis in both the p eripheral
FOREWORD xv
nervous system and CNS (Craig, 2002; Damasio, 2003), the effect of in-
sufficient sleep on physiological aspects of normal emotional regulation
has only begun to attract inquiry.
CNS function and cognition are similarly impacted by insufficient
sleep. Loss of vigilance, especially at unfavorable circadian periods for
maintenance of wakefulness, leads to a large number of automobile, pub-
lic transportation, and industrial accidents (Garbarino, Nobili, Beelke, De
Carli, & Ferrillo, 2001). In the elderly, sleep disturbances may be a risk
factor for incident cognitive impairment (Blackwell et al., 2011). Cognitive
skills such as working memory, short-term memory, and logical reasoning
are especially disrupted by sleep deprivation (Chee & Chuah, 2008). Such
functions rely on the prefrontal regions of the brain and include execu-
tive processes such as decision-making and behavioral inhibition (Chee
& Chuah, 2008; Drummond, Paulus, & Tapert, 2006; Killgore, Balkin, &
Wesensten, 2006). These prefrontal areas include the major loci of emotion
regulation (Ochsner & Gross, 2005; Schiller & Delgado, 2010). Thus, sleep
loss also impacts cognitive processes for which emotional information is
essential, such as moral reasoning (Killgore et al., 2007), emotional intelli-
gence (Killgore et al., 2008), and affect-guided decision-making (Killgore
et al., 2006).
The following brief overview of some recent findings on sleep and emo-
tion will whet the reader’s appetite for the extensive treatment provided
later in the book. Many of these studies have used total sleep deprivation
(TSD) and sleep restriction protocols. TSD can reportedly impair recog-
nition of facial emotion (van der Helm, Gujar, & Walker, 2010), and sleep
restriction slows the expression of facial emotions (Schwarz et al., 2013).
Similarly, even mild sleep restriction can impair emotional regulation in
children (Gruber, Cassoff, Frenette, Wiebe, & Carrier, 2012), and normal
variation in sleep quality can affect an individual’s high-level ability to
reappraise negative stimuli in normal adults (Mauss, Troy, & Lebourgeois,
2013). Functional neuroimaging studies have shown distinct effects of
TSD on the neural circuits involved in emotion regulation (Gujar, Yoo,
Hu, & Walker, 2011; Yoo, Gujar, Hu, Jolesz, & Walker, 2007). Following
TSD, activation is reduced in regions, such as the ventromedial prefron-
tal c ortex (vmPFC), that inhibit expression of negative emotion (Thomas
et al., 2000; Yoo et al., 2007) but increased in the amygdala in response to
emotional stimuli (Yoo et al., 2007). Moreover, sleep deprivation disrupts
the functional connectivity between the vmPFC and the amygdala (Yoo
et al., 2007). A recent fMRI study has further shown that the sleep debt
accrued by prolonged sleep restriction can produce a similar hyperres-
ponsivity of the amygdala, while reducing its functional connectivity with
the vmPFC (Motomura et al., 2013).
Unlike normal emotion regulation, psychopathology appears to be
strongly linked to the sleep disturbances that are ubiquitous in affective
xvi FOREWORD
and anxiety disorders (Ford & Cooper-Patrick, 2001; Harvey, 2008, 2011;
Kobayashi, Boarts, & Delahanty, 2007; Mellman, 2006, 2008; Peterson &
Benca, 2006; Riemann, Berger, & Voderholzer, 2001). Among the anxiety
disorders, poor sleep quality (e.g., low efficiency, prolonged onset latency)
is common in posttraumatic stress disorder (PTSD), generalized anxiety
disorder (GAD), and panic disorder (Mellman, 2006, 2008). Moreover, the
comorbidity of insomnia with both GAD (Monti & Monti, 2000; Ohayon,
1997) and major depressive disorder (MDD) (Staner, 2010) is extremely
high. Among specific sleep stages, decreased slow-wave sleep (SWS) is
seen in both depression (Peterson & Benca, 2006; Steiger & Kimura, 2010)
and PTSD (Kobayashi et al., 2007). REM abnormalities, often interpreted
as elevated REM pressure, are also widely reported in MDD and include
shortened REM latency and increased REM density (Modell & Lauer,
2007; Steiger & Kimura, 2010; Tsuno, Besset, & Ritchie, 2005). Elevated
REM density is also seen in PTSD (Kobayashi et al., 2007). In MDD, TSD
produces a transient antidepressant effect. In mania, sleep loss can pro-
duce a similar, albeit pathological, directionality of mood change by trig-
gering manic episodes (Harvey, 2008, 2011). In striking contrast, TSD has
been shown to have a mood-lowering effect in healthy individuals (Haack
& Mullington, 2005; Zohar, Tzischinsky, Epstein, & Lavie, 2005).
Sleep may regulate emotion via its influences on emotional memory.
Given the increasing interest in the sleep dependency of memory con-
solidation over the past decade (Diekelmann & Born, 2010; Diekelmann,
Wilhelm, & Born, 2009; Stickgold, 2005; Walker & Stickgold, 2006), reports
of sleep effects on emotional memory have multiplied. For example, the
consolidation of emotional memory is enhanced by nocturnal sleep (Baran,
Pace-Schott, Ericson, & Spencer, 2012; Hu, Stylos-Allan, & Walker, 2006;
Wagner, Gais, & Born, 2001; Wagner, Hallschmid, Rasch, & Born, 2006)
as well as by daytime naps (Nishida, Pearsall, Buckner, & Walker, 2009).
Sleep can also promote the offline reorganization of emotional memory: A
night of sleep enhances the trade-off in which an emotionally salient fore-
ground image is selectively recalled over a neutral background (Payne,
Chambers, & Kensinger, 2012; Payne, Stickgold, Swanberg, & Kensinger,
2008). Functional neuroimaging studies show distinct effects of TSD on the
neural circuits involved in emotional memory (Menz et al., 2013; Payne &
Kensinger, 2011; Sterpenich et al., 2007). There is differential activation in
key components of the brain’s emotional circuitry during recall of emo-
tional stimuli depending upon whether or not sleep occurred after encod-
ing. For example, the successful recall of emotional stimuli was associated
with greater activation of the amygdala, hippocampus, and vmPFC in a
group that slept versus one that was deprived of sleep following learning,
and this group difference remained 6 months later (Sterpenich et al., 2007,
2009). Such findings provide a possible brain basis for an earlier behav-
ioral study showing that superior performance on an emotional verbal
FOREWORD xvii
memory task, measured shortly following postlearning sleep vs. contin-
ued wakefulness, was maintained for a full 4 years (Wagner et al., 2006).
Another fMRI study has suggested that the retrieval of an emotional
memory after a night of sleep engaged a more discrete and integrated set
of limbic structures than retrieval of the same memory following a day
awake (Payne & Kensinger, 2011).
Although emotional salience clearly interacts with sleep’s effects on
human declarative memory, evolutionarily ancient learning and memory
processes may be equally important for human emotion regulation. These
include processes involving simple associative memories, such as classical
conditioning, through which an emotionally neutral stimulus is paired in
time with a rewarding or punishing stimulus so that, when the emotion-
ally salient stimulus is removed, the formerly neutral stimulus elicits a
similar response (Pavlov, 1927). Following fear conditioning, another form
of associative learning, fear extinction, allows the subject to learn that the
once-feared stimulus is no longer dangerous (Hermans, Craske, Mineka,
& Lovibond, 2006; Milad & Quirk, 2012). Rather than erasing fear, extinc-
tion forms a new inhibitory memory that coexists and competes with the
neural processes of fear expression (Quirk & Mueller, 2008). Crucially, this
indicates that extinction learning represents brain plasticity that, like other
forms of memory, must consolidate following encoding in order to per-
sist for later retrieval. A similarly primitive, nonassociative form of mem-
ory, habituation, involves reduced reactivity to frequently encountered
stimuli (Grissom & Bhatnagar, 2009; Leussis & Bolivar, 2006; Thompson
& Spencer, 1966). As with its “opposite,” sensitization, habituation also
involves neuroplastic changes that must consolidate in order to persist.
Extinction memory is of particular clinical interest because its deficiency
is likely associated with the development and perpetuation of anxiety
disorders. For example, the failure to subsequently extinguish or remem-
ber the extinction of trauma-related memories and cues may perpetuate
PTSD (Pitman et al., 2012), and extinction memory is impaired in PTSD at
both the behavioral and neural level (Milad et al., 2008, 2009). Moreover,
exposure therapy, which forms therapeutic extinction memories through
in vivo, virtual reality, or imaginal exposure to fear, is the gold-standard
treatment for anxiety disorders such as PTSD, specific phobia, social pho-
bia, and obsessive compulsive disorder (Craske et al., 2008; Foa, Hembree,
& Rothbaum, 2007; McNally, 2007).
Sleep promotes consolidation of fear extinction and habituation mem-
ory. For example, in one study, researchers used electric shock to condi-
tion subjects to fear two color stimuli, but only one color stimulus was
then extinguished (Pace-Schott et al., 2009). Some subjects were subse-
quently allowed to sleep. After this period, both groups showed reduced
conditioned responding to the extinguished stimulus (extinction recall),
but only the subjects who had slept exhibited a reduced response to the
xviii FOREWORD
unextinguished stimulus (extinction generalization). Similarly, sleep has
been shown to enhance extinction memory consolidation and generaliza-
tion following simulated exposure therapy for spider phobia (Pace-Schott,
Verga, Bennett, & Spencer, 2012), a finding recently replicated using ac-
tual exposure therapy (Kleim et al., 2013). Sleep has also reportedly en-
hanced intersession habituation (Pace-Schott et al., 2011, 2014). Although
circadian rhythms may additionally influence memory for extinction and
habituation (Pace-Schott et al., 2013, 2014), other studies controlling for
this influence confirm the importance of sleep between learning and recall
(Kleim et al., 2013; Pace-Schott et al., 2011, 2014, 2012). Notably, despite
supporting more uniquely human forms of emotion regulation, such as
cognitive reappraisal of negative stimuli, higher-level associational areas,
such as the dorsomedial and dorsolateral prefrontal cortices, may not be
highly sensitive to normal variations in self-reported sleep quality (Minkel
et al., 2012), even though behavioral expression may be affected (Mauss
et al., 2013). Therefore, the effects of sleep quality on the more elemental
means of achieving emotional homeostasis, such as those that rely on au-
tonomic structures and somatovisceral feedback, may be one mechanism
by which poor sleep leads to impairments of mood.
To conclude this introduction to sleep and affect, we introduce an in-
teresting controversy that has already emerged on the bases of early
studies—the relative importance of different sleep stages to emotion reg-
ulation. Both the occurrence and amount of REM sleep have been asso-
ciated with enhanced emotional memory (Hu et al., 2006; Nishida et al.,
2009; Wagner et al., 2001, 2006). Based upon such evidence, Walker and
colleagues have advanced a “Sleep to Remember, Sleep to Forget” (SRSF)
model (Goldstein & Walker, 2014; Walker, 2009; Walker & van der Helm,
2009). In this model, REM serves to both consolidate the contents of an
emotional memory and to simultaneously depotentiate the emotional
charge associated with that memory. As evidence for this model, the au-
thors have shown that a daytime nap containing REM prevents an increase
in reactivity to facial expressions of a negative emotion (anger and fear)
observed following a day without such a nap (Gujar, McDonald, Nishida,
& Walker, 2010). Similarly, following exposure to negative stimuli, the
spectral power of high-frequency gamma (>30 Hz) EEG oscillations during
subsequent nocturnal REM was negatively associated with the next-day
subjective negative ratings of the previously seen stimuli, as well as with
amygdala activation measured via fMRI (van der Helm et al., 2011). The
authors suggest that higher gamma power indicates higher REM-sleep
levels of norepinephrine, a neuromodulator that normally reaches its
daily nadir during REM (Pace-Schott & Hobson, 2002), and, hence, a less
favorable physiological milieu in REM for the depotentiation of emotion.
Deliens and colleagues (Deliens, Gilson, Schmitz, & Peigneux, 2013) have
provided some support for the SRSF model, using the mood-dependent
FOREWORD xix
memory (MDM) effect, whereby memories encoded in one emotional state
are better retrieved in that same emotional state. Using a mood-i nduction
technique, participants learned word pairs in one mood and were tested
in another. When one night’s TSD followed encoding, the MDM effect re-
mained after two night’s recovery sleep, whereas if normal sleep followed
encoding, the MDM effect was eliminated. However, in a follow-up study,
the MDM effect remained following late-night, REM-rich sleep, as well as
following early-night SWS-rich sleep (Deliens, Neu, & Peigneux, 2013).
Supporting SRSF, a neuroimaging study contrasting selective REM depri-
vation (REMD) with selective NREM deprivation (NREMD) showed an
increase in behavioral reactivity to emotional images following REMD in
comparison to a baseline night, whereas no change was seen following
NREMD (Rosales-Lagarde et al., 2012).
fMRI has provided additional evidence for the involvement of REM
sleep in emotion regulation. Rosales-Lagarde et al. (2012) studied subjects
who performed an emotional reactivity task while in the scanner. The task
was repeated with the same stimuli before and after a night of REMD
or NREMD. In this task, subjects indicated behaviorally, with a defensive
choice, whether or not they felt threatened when imagining themselves
“in” an aversive photo. Those having REMD showed more defensive
choices at the second presentation of the same images, but those with
NREMD made similar choices. In addition, the expected habituation of
a large number of cortical areas was see across responses to all stimuli at
their second presentation following NREMD, whereas responses follow-
ing REMD were of the same magnitude as initial responses. Moreover, for
the contrast of perceived threatening versus nonthreatening images, ac-
tivation of visual association areas increased between sessions following
REMD but not NREMD.
Among lower-level forms of emotion regulation, Spoormaker et al.
(2010) showed that extinction recall and activation of the vmPFC were
greater in individuals who achieved REM during a 90-min afternoon nap
that followed fear conditioning and extinction learning. In a subsequent
study using all-night instrumental REMD compared to a NREMD, REMD
resulted in poorer extinction memory, an effect accompanied by differen-
tial activation of the left middle temporal gyrus. Pace-Schott et al. (2014)
showed that an index of extinction memory correlated with REM percent
during the preceding night. In animal models, experimental stressors
have been widely shown to reduce and fragment REM (Pawlyk, Morrison,
Ross, & Brennan, 2008) and a REM-related brainstem-generated potential,
the p-wave, has been shown to be essential to extinction memory (Datta &
O'Malley, 2013).
However, other studies have advanced an entirely opposite prediction
for the effects of REM on aversive memories, implicating REM in the pres-
ervation, rather than removal, of the emotional components of d eclarative