Sleep and emotional processing

doi:10.1016/j.smrv.2017.12.005

Sleep Medicine Reviews

Volume 40, August 2018, Pages 183-195

https://doi.org/10.1016/j.smrv.2017.12.005 Get rights and content

Summary

A growing body of literature suggests that sleep plays a critical role in emotional processing. This review aims at synthesizing current evidence on the role of sleep and sleep loss in the modulation of emotional reactivity, emotional memory formation, empathic behavior, fear conditioning, threat generalization and extinction memory. Behavioral and neurophysiological evidence suggesting that rapid-eye movement (REM) sleep plays an important role in emotional processing is also discussed. Furthermore, we examine the relations between sleep and emotions by reviewing the functional neuroimaging studies that elucidated the brain mechanisms underlying these relations. It is shown that sleep supports the formation of emotional episodic memories throughout all the stages that compose memory processing. On the contrary, sleep loss deteriorates both the encoding of emotional information and the emotional memory consolidation processes.

Research is also progressively providing new insights into the protective role of sleep in human emotional homeostasis and regulation, promoting adaptive next-day emotional reactivity. In this respect, evidence converges in indicating that lack of sleep significantly influences emotional reactivity. Moreover, notwithstanding some contradictory findings, the processing of emotionally salient information could mainly benefit from REM sleep. However, some crucial aspects of sleep-dependent emotional modulation remain unclear.

Introduction

Although the critical and active role of sleep in the processes of memory consolidation and integration is nowadays largely acknowledged, we still lack any consensus about the specific role of sleep in affective and emotional processing. Nevertheless, several recent behavioral and neuroimaging studies revealed the alterations imposed by sleep loss to emotional reactivity [1], ∗[2], [3] and emotional memory [4], ∗[5], [6], ∗[7], [8]. This review aims to provide a synthesis of these recent findings in healthy humans, with the goal of analyzing the role of sleep in the different components of emotional processing. In the first section, we discuss the main behavioral and psychophysiological studies that investigated the role of sleep in the processes of encoding and consolidation of emotional memory. Subsequently, we examine how sleep modulates emotion regulation. In particular, we will review relevant studies about the effects of sleep on emotional reactivity and on more complex emotional processes, such as those involved in the identification of facial emotions and empathy. Moreover, we discuss the role of sleep in fear conditioning memory, threat generalization and extinction memory. In the second section, we address the specific role of REM sleep in the consolidation of emotional memory and in the modulation of emotional reactivity, focusing on the specific physiological REM features that prompted some researchers to suggest its crucial involvement in emotional processing. In the third section, we further examine the relations between sleep and emotions by reviewing the functional neuroimaging studies that elucidated the brain mechanisms underlying these relations. We will observe how these studies have identified, especially during REM sleep, the activation of specific brain areas that are involved in human emotional processing, providing new insights into the protective role of sleep in human emotional homeostasis and regulation.

Section snippets

The relations between sleep and emotions: behavioral and psychophysiological studies

The sleep deprivation paradigm has been extensively applied to investigate the relations between sleep and learning/memory consolidation by means of different experimental approaches ∗[9], [10]. Within this general framework, the beneficial effect of sleep on declarative and procedural memory has been robustly demonstrated [11].

Substantial evidence has been also provided that sleep specifically contributes to emotional memory consolidation ∗[7], [12], ∗[13], [14], [15], while sleep deprivation

REM sleep and emotional memory processing

Since its discovery [108], REM sleep has been closely linked to human emotion, being almost invariantly associated with reports of emotionally intense, vivid dreams [109]. A large literature now suggests that the link between REM sleep and emotion, rather than only a phenomenological coincidence, is substantial [110].

Based on the neuromodulator state during REM sleep (i.e., high acetylcholinergic tone), it has been proposed that during this sleep stage, memories within the neocortex, subjected

Sleep and emotions: insights into the brain mechanisms by neuroimaging studies

In recent years neuroimaging studies have suggested that brain areas implicated in emotional memory functions during wakefulness are reactivated during sleep [90]. The earlier PET studies indeed demonstrated specific neuronal network activity throughout REM sleep within the amygdala, entorhinal cortex and anterior cingulate cortex [128], [129], [91], [130]. The increased activity during REM sleep of the emotion-related brain regions has been substantiated by fMRI [91] and EEG–fMRI

Critical points and future avenues of research

The relationship between sleep and emotional processing has received recent scientific interest, with a variety of evidence accumulated so far, supporting an active role of sleep or of specific sleep stages in the processing of salient episodic memories and in emotional regulation. To date, several questions remain unanswered, since research produced contradictory results. Several factors that potentially contributed to generating contrasting results should be considered. First, the

Conclusions

Research on the relations between sleep and emotional processing has accompanied the exponential growth of sleep research in the last two decades. A large body of evidence supports the notion that sleep is critical for the formation of episodic memories including emotionally-valenced information throughout all the stages of this process.

In the context of emotional processing, negative memories seem to be more resistant to the effect of sleep loss during the encoding phase, probably because such

Conflicts of interest

The authors do not have any conflicts of interest to disclose.

References∗ (147)

S.S. Yoo et al.
The human emotional brain without sleep – a prefrontal amygdala disconnect
Curr Biol
(2007)
D. Tempesta et al.
Emotional memory processing is influenced by sleep quality
Sleep Med
(2015)
D. Tempesta et al.
The effect of sleep deprivation on the encoding of contextual and non-contextual aspects of emotional memory
Neurobiol Learn Mem
(2016)
M.P. Walker
Cognitive consequences of sleep and sleep loss
Sleep Med
(2008)
U. Wagner et al.
Brief sleep after learning keeps emotional memories alive for years
Biol Psychiatry
(2006)
L. Genzel et al.
The role of rapid eye movement sleep for amygdala-related memory processing
Neurobiol Learn Mem
(2015)
E. Van der Helm et al.
REM sleep depotentiates amygdala activity to previous emotional experiences
Curr Biol
(2011)
J. Westermann et al.
System consolidation during sleep – a common principle underlying psychological and immunological memory formation
Trends Neurosci
(2015)
K. Kaida et al.
Role of sleep for encoding of emotional memory
Neurobiol Learn Mem
(2015)
E.A. Phelps
Human emotion and memory: interactions of the amygdala and hippocampal complex
Curr Opin Neurobiol
(2004)

P. Holland et al.

Emotional memory: selective enhancement by sleep

Curr Biol

(2007)

S. Diekelmann et al.

The whats and whens of sleep-dependent memory consolidation

Sleep Med Rev

(2009)

D. Oudiette et al.

Fear not: manipulating sleep might help you forget

Trends Cogn Sci

(2014)

D.I. Schouten et al.

State of the art on targeted memory reactivation: sleep your way to enhanced cognition

Sleep Med Rev

(2017)

N. Cellini et al.

Sleep before and after learning promotes the consolidation of both neutral and emotional information regardless of REM presence

Neurobiol Learn Mem

(2016)

G. Deliens et al.

Sleep unbinds memories from their emotional context

Cortex

(2013)

P.L. Franzen et al.

Sleep deprivation alters pupillary reactivity to emotional stimuli in healthy young adults

Biol Psychol

(2009)

S. Groch et al.

The role of REM sleep in the processing of emotional memories: evidence from behavior and event-related potentials

Neurobiol Learn Mem

(2013)

T.J. Cunningham et al.

Psychophysiological arousal at encoding leads to reduced reactivity but enhanced emotional memory following sleep

Neurobiol Learn Mem

(2014)

J.J. Pilcher et al.

Sleep deprivation affects reactivity to positive but not negative stimuli

J Psychosom Res

(2015)

P.J. Lang et al.

Emotion, motivation, and anxiety: brain mechanisms and psychophysiology

Biol Psychiatry

(1998)

J.F.A. Schwarz et al.

Shortened night sleep impairs facial responsiveness to emotional stimuli

Biol Psychol

(2013)

W.D.S. Killgore et al.

Sleep deprivation impairs recognition of specific emotions

Neurobiol Sleep Circadian Rhythms

(2017)

W.D.S. Killgore et al.

Sleep deprivation reduces perceived emotional intelligence and constructive thinking skills

Sleep Med

(2008)

M. Haack et al.

Sustained sleep restriction reduces emotional and physical well-being

Pain

(2005)

M.M. Menz et al.

The role of sleep and sleep deprivation in consolidating fear memories

Neuroimage

(2013)

V.I. Spoormaker et al.

The neural correlates and temporal relationship between shock exposure, disturbed sleep and impaired consolidation of fear extinction

J Psychiatr Res

(2010)

Y. Nir et al.

Dreaming and the brain: from phenomenology to neurophysiology

Trends Cogn Sci

(2010)

S. Lissek et al.

Classical fear conditioning in the anxiety disorders: a meta-analysis

Behav Res Ther

(2005)

J.M. Armfield

Cognitive vulnerability: a model of the etiology of fear

Clin Psychol Rev

(2006)

S. Mineka et al.

The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders

Acta Psychol

(2008)

M.R. Milad et al.

Fear extinction in rats: implications for human brain imaging and anxiety disorders

Biol Psychol

(2006)

M.G. Craske et al.

Optimizing inhibitory learning during exposure therapy

Behav Res Ther

(2008)

S.G. Hofmann

Cognitive processes during fear acquisition and extinction in animals and humans: implications for exposure therapy of anxiety disorders

Clin Psychol Rev

(2008)

D. Zohar et al.

The effects of sleep loss on medical residents' emotional reactions to work events: a cognitive-energy model

Sleep

(2005)

D. Tempesta et al.

Lack of sleep affects the evaluation of emotional stimuli

Brain Res Bull

(2010)

V. Sterpenich et al.

Sleep-related hippocampo-cortical interplay during emotional memory recollection

PLoS Biol

(2007)

V. Sterpenich et al.

Sleep promotes the neural reorganization of remote emotional memory

J Neurosci

(2009)

D. Tempesta et al.

Emotional working memory during sustained wakefulness

J Sleep Res

(2014)

S. Gais et al.

Declarative memory consolidation: mechanisms acting during human sleep

Learn Mem

(2004)

S.J. Sara

Sleep to remember

J Neurosci

(2017)

P. Hu et al.

Sleep facilitates consolidation of emotionally arousing declarative memory

Psychol Sci

(2006)

S.A. Cairney et al.

Complementary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation

Cereb Cortex

(2015)

M. Atienza et al.

Modulatory effects of emotion and sleep on recollection and familiarity

J Sleep Res

(2008)

J. Morgenthaler et al.

Selective REM-sleep deprivation does not diminish emotional memory consolidation in young healthy subjects

PLoS One

(2014)

E. Van der Helm et al.

Sleep deprivation impairs the accurate recognition of human emotions

Sleep

(2010)

V. Guadagni et al.

The effects of sleep deprivation on emotional empathy

J Sleep Res

(2014)

M.R. Milad et al.

Fear extinction as a model for translational neuroscience: ten years of progress

Annu Rev Psychol

(2012)

Y.D. Van Der Werf et al.

Sleep benefits subsequent hippocampal functioning

Nat Neurosci

(2009)

S.S. Yoo et al.

A deficit in the ability to form new human memories without sleep

Nat Neurosci

(2007)

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Findings suggest that worry and rumination are intimately linked with sleep and highlight the protective role that better sleep may play in reducing older adults' everyday perseverative thinking.
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More severe depression symptoms were associated with higher physical activity intensity and poorer sleep quality after controlling sociodemographic variables. However, upon introducing the interaction between physical activity and sleep in the regression to assess evidence for moderation, we found that high physical activity was a risk factor for worsened depression symptoms among individuals with poor quality sleep but not among those with good sleep quality. The effects of physical activity were also partially explained by variations in educational attainment.
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¹: DT and VS contributed equally to this work.

^∗: The most important references are denoted by an asterisk.

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Physiological ReviewSleep and emotional processing

Summary

Introduction

Section snippets

The relations between sleep and emotions: behavioral and psychophysiological studies

REM sleep and emotional memory processing

Sleep and emotions: insights into the brain mechanisms by neuroimaging studies

Critical points and future avenues of research

Conclusions

Conflicts of interest

Curr Biol

Sleep Med

Neurobiol Learn Mem

Sleep Med

Biol Psychiatry

Neurobiol Learn Mem

Curr Biol

Trends Neurosci

Neurobiol Learn Mem

Curr Opin Neurobiol

Curr Biol

Sleep Med Rev

Trends Cogn Sci

Sleep Med Rev

Neurobiol Learn Mem

Cortex

Biol Psychol

Neurobiol Learn Mem

Neurobiol Learn Mem

J Psychosom Res

Biol Psychiatry

Biol Psychol

Neurobiol Sleep Circadian Rhythms

Sleep Med

Pain

Neuroimage

J Psychiatr Res

Trends Cogn Sci

Behav Res Ther

Clin Psychol Rev

Acta Psychol

Biol Psychol

Behav Res Ther

Clin Psychol Rev

The effects of sleep loss on medical residents' emotional reactions to work events: a cognitive-energy model

Sleep

Lack of sleep affects the evaluation of emotional stimuli

Brain Res Bull

Sleep-related hippocampo-cortical interplay during emotional memory recollection

PLoS Biol

Sleep promotes the neural reorganization of remote emotional memory

J Neurosci

Emotional working memory during sustained wakefulness

J Sleep Res

Declarative memory consolidation: mechanisms acting during human sleep

Learn Mem

Sleep to remember

J Neurosci

Sleep facilitates consolidation of emotionally arousing declarative memory

Psychol Sci

Complementary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation

Cereb Cortex

Modulatory effects of emotion and sleep on recollection and familiarity

J Sleep Res

Selective REM-sleep deprivation does not diminish emotional memory consolidation in young healthy subjects

PLoS One

Sleep deprivation impairs the accurate recognition of human emotions

Sleep

The effects of sleep deprivation on emotional empathy

J Sleep Res

Fear extinction as a model for translational neuroscience: ten years of progress

Annu Rev Psychol

Sleep benefits subsequent hippocampal functioning

Nat Neurosci

A deficit in the ability to form new human memories without sleep

Nat Neurosci

Physiological Review
Sleep and emotional processing