Relationship Between Emotions, Sleep and Well-Being

Abstract

In recent decades, increasing investigation on sleep has led to the definition and characterization of its vital functions and features. In addition to its well-known role of sleep in memory consolidation, one crucial function of sleep is emotion regulation. In adolescence, emotion regulation is not fully developed, leading to heightened emotional experience and increased risk of unwanted psychological/behavioural outcomes. During adolescence, the development of emotion regulation is contingent on the complete maturation of the prefrontal cortex, acting as a top-down inhibitor of subcortical structures like the amygdala. However, biopsychosocial factors prevent adolescents from obtaining adequate amounts of sleep, and lack of sleep can specifically affect emotion regulation, observable at the psychological/behavioural level as increased negative affect, disrupted well-being and frank psychopathology.

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© Springer Nature Switzerland AG 2019
A. Pingitore et al. (eds.), Adolescent Health andWellbeing,
https://doi.org/10.1007/978-3-030-25816-0_8
A. Zaccaro · C. Conversano · E. Lai · A. Gemignani (*)
Department of Surgical, Medical and Molecular Pathology and Critical Care Medicine,
University of Pisa, Pisa, Italy
e-mail: angelo.gemignani@unipi.it
8
Relationship Between Emotions, Sleep
andWell-Being
AndreaZaccaro, CiroConversano, ElisaLai,
andAngeloGemignani
8.1 Psychophysiological Functions ofSleep
Sleep is a natural, universal phenomenon present in all living organisms, main-
tained across all steps of phylogenetic evolution and also observable in species
without a centralized nervous system, like jellysh [1]. Even if sleep is a state
dened by the cessation of nalized behaviour and a strong disconnection from the
sensory environment, it is not a passive phenomenon [2], but it is a highly active
process as vital as respiration or digestion. Sleep is not a unitary phenomenon, but
it is composed of a dynamic sequence of stages that show high degrees of inter- and
intra-individual variability. In the last few decades, the long-standing question
‘why do we sleep?’ has received several answers. Since the development of the
electroencephalogram (EEG) by Hens Berger in 1929, sleep has been continuously
investigated in humans, leading to the denition of rapid eye movement (REM)
sleep and non-REM (NREM) sleep, which in turn is divided in three stages, related
to the increase of sleep depth (i.e. increase of awakening threshold): N1, N2 and
N3. The alternation between sleep stages follows a sequence of cycles during the
night, lasting nearly 90min each (N1-N2-N3 REM; reviewed in [3]). It is now well
established that sleep is fundamental for neuronal detoxication, tissue restoration,
conservation of energy, enhancement of the immune system and, nally, increasing
neuronal plasticity [4]. In order to develop a model of sleep function, the synaptic
homeostasis hypothesis has been developed [5, 6]. According to this theory,
experience- dependent learning during the day is related to the increase of cortical

154
synaptic weight (i.e. wakefulness promotes activity-dependent strengthening of
synaptic connections). Conversely, during the night, sleep reverses plasticity rules,
thus promoting the activity-dependent weakening of connections, leading to
homeostatic down selection of synapses actuated during the day. In this way, sleep
basically resets synaptic weight in the central nervous system, allowing the brain to
learn again during the following day [5, 6]. Together, these functions are related to
slow waves (including sleep slow oscillations (SSO) and K-complexes, very slow,
triphasic slow waves with a frequency between 0.5 and 1Hz, mainly detectable at
the frontal level; see [7, 8]), and sleep spindles. Slow waves are low frequency
(0.5–4Hz), high amplitude oscillations generated in the cortex that are critically
dependent on the activity of subcortical structures, like the thalamus [9, 10], and
the olfactory bulb [11]. Slow waves are abundant in the rst part of the night (early
sleep) and reduce exponentially during the night, but are increased after sleep
deprivation, indicating an important role in homeostatic regenerative functions of
sleep [3]. Sleep spindles are brief, fast oscillations, lasting 1–2s, with a frequency
of 11–16 Hz. They are generated through thalamocortical loops and are mainly
related to declarative memory consolidation during sleep [12, 13]. Sleep is also
fundamental for enhancing learning-related processes, sustained by local slow-
wave power (i.e. slow-wave activity) and SSO. Basically, increased daytime,
performance- related, synaptic activity in cortical regions (e.g. activity in visuomo-
tor cortices related to the performance of a visuospatial learning task) will be
reected in increased slow-wave activity/SSO in the same regions during the fol-
lowing night [14].
Beyond memory consolidation, one of the main roles of sleep is emotion regu-
lation, although the identity of the specic sleep stages, features and mechanisms
involved in this process is currently a hot research topic. Several studies have iden-
tied REM sleep as fundamental [15, 16]. In fact, REM sleep is not only associ-
ated with the consolidation of conditioned fear memories [17], but also with the
unbinding of (‘hot’) emotional aspects of a memory from the (‘cold’) memory
itself [18], thus facilitating the extinction of conditioned fear. In other words, REM
sleep, and particularly the total amount of EEG theta activity, can separate emo-
tionally relevant components of a memory (its ‘visceral charge’) from emotionally
irrelevant ones [19, 20], resulting in a dissipation of subjective emotional intensity
and in the consolidation of the information itself, as a sort of ‘overnight therapy’
[21, 22]. The neurophysiological substrate of this process has been identied as the
active inhibition of the amygdala through top-down prefrontal cortex (PFC) con-
nections [23], causing a reduction of the activity of the amygdala, paralleled by an
increase of the activity of the hippocampus (the ‘sleep to forget and sleep to
remember’ model [21]).
Even if theoretical connections between homeostatic functions of sleep and emo-
tion regulation have never been directly investigated, they take on particular impor-
tance when considering a critical developmental period like adolescence.
A. Zaccaro et al.

155
8.2 Adolescence, Emotions andEmotion Regulation
Adolescence is a critical developmental age that starts with sexual maturation
(puberty) and ends with the achievement of the social roles of young adulthood,
usually taking place between 12 and 17years old. It has been dened as an age
characterized by both strengths and vulnerabilities, and is a critical period of devel-
opment of emotion regulation [24]. During this stormy period, the central nervous
system undergoes a slow process of maturation, with several functional and ana-
tomical modications, most importantly, a massive neuronal pruning [25]. This
slow maturing process is most evident within the prefrontal cortices, begins during
childhood and continues until early adulthood, resulting in the development of high-
order psychological functions [25, 26]. Accordingly, adolescence is characterized
by heightened emotional experiences, which are probably caused by the different
maturation trajectories of cortical (prefrontal) and subcortical (amygdala) brain
structures, leading to a diminished ability to regulate emotions [27].
Emotions are highly salient and fundamental qualities of our conscious life,
which can modulate attention to stimuli, interrupt cognitive or behavioural pro-
cesses and trigger actions in the outer world [28, 29]. In order to adapt success-
fully to the environment, humans have the ability to regulate emotions, applying
strategies that modulate, consciously and unconsciously, emotional experience
and expression [30], in order to use emotions as resources in decision-making
processes within complex social contexts [24, 31]. Emotion regulation begins as
the individual acknowledges a new event or situation, and interprets it in the con-
text of his goals [32, 33]. Subsequently, attempts to adaptively regulate the new
emotion take place in an iterative way, modulated by environmental feedback,
according to the following stages: (1) situation selection, (2) situation modica-
tion, (3) attentional deployment, (4) cognitive change (e.g. reappraisal) and (5)
response modulation (e.g. behavioural suppression) [32]. At the neurophysiologi-
cal level, successful emotion regulation in adults is mainly related to increased
PFC activity and decreased amygdala activity [34–36], while emotion dysregula-
tion is related to decit of the top-down inhibition of the amygdala by the PFC [37,
38]. However, emotion regulation has been linked to an expanded prefrontal net-
work, comprising the dorsolateral, dorsomedial, ventrolateral, and the posterior
prefrontal cortices, the anterior cingulate cortex and the inferior parietal regions
[39] (Fig.8.1).
Emotion regulation increases with age, from childhood to adulthood [34, 40–42],
with a critical period occurring during adolescence [43]. Alterations in this process
can lead to the development of severe psychopathological conditions in adulthood.
In fact, emotion disturbance and dysregulation are transdiagnostic processes
observed in almost all forms of psychopathology, both internalizing and external-
izing [44, 45]. As described next, sleep has a fundamental role in the successful
development of these abilities.
8 Relationship Between Emotions, Sleep andWell-Being

156
8.3 Sleep andSleep Deprivation inAdolescence
Across the life span, emotion regulation increases in tandem with continuous change
in sleeping patterns, with a reduction in both NREM and REM sleep, and total sleep
time. In particular, sleep in adolescence is marked by a progressive reduction of
EEG signal amplitude and power (up to 40%) across all EEG frequency bands,
which is related to age and puberty stage [46–49]. At the same time, adolescent
sleep is related to the progressive increase of sleep spindles in peak frequency and
EEG coherence in multiple frequencies, which have been related to the myelination
of long-range connections in thalamocortical networks [47, 48, 50–52]. An MRI
study has conrmed that this reduction in EEG power during sleep in adolescence
is correlated with massive pruning of grey matter [53]. With EEG, Kurth etal. [54]
found that progressive reduction of slow-wave activity has a posterior-to-anterior
gradient, which follows precisely the local reductions of grey matter, as another
study longitudinally assessed with MRI [55].
These data suggest an important link between slow waves and sleep spindles in
brain maturation during adolescence, in particular in the PFC, which develops later
than other brain cortices, and is crucial for emotion regulation. In the scientic
Fig. 8.1 Emotion generation and regulation in the adolescent brain. In blue, functional decrease
of activity; in red, functional increase of activity. DLPFC dorsolateral prefrontal cortex, VLPFC
ventrolateral prefrontal cortex, INS insula, IPC inferior parietal cortex, DmPFC dorsomedial pre-
frontal cortex, VmPFC ventromedial prefrontal cortex, ACC anterior cingulate cortex, AMY amyg-
dala, St ventral striatum. Adapted from Ochsner etal. [39] and Gross [32]. (Authors thank Dr.
Sergio Frumento for having adapted the gure)
A. Zaccaro et al.

157
literature, links between poor sleep and emotion dysregulation have been inten-
sively investigated in adults (for reviews, see [18, 56–62]), but how poor sleep
specically impacts adults and adolescents is still unknown [63]. Unfortunately,
even if the recommended sleep time for adolescents is 9h per night, the National
Sleep Foundation team has stated that adolescents do not get the adequate amount
of sleep, sleeping only 6–7 h per night [64] (Fig. 8.2). The reasons for this are
complex and biopsychosocial in nature [65]: (1) the physiology of the hormone
melatonin in adolescence is completely different from childhood, with its releasing
shifted later during the evening [66]; this, together with increased ability to resist
sleep pressure, lead adolescents to be ‘owls’ (i.e. evening type), going to bed later
in the night; (2) school start time is often set very early in the morning (7:30 to
8:30), forcing awakening much earlier than the recommended 9h of sleep (i.e. the
so-called ‘social jetlag’ [67]); and (3) the occurrence of familiar and social major
risk factors, as aversive family environment, evening light exposure, computer use
and tobacco and caffeine use, lead to signicantly reduced sleep time [68].
Collectively, prolonged poor sleep conditions are important risk factors for psycho-
pathology in adolescence and, conversely, psychopathology itself is highly related
to co-morbid sleep problems (near 95% [69]). Moreover, poor sleep is related to
several cognitive, behavioural and emotional alterations (for reviews, see [70–73]),
8 hours: may be
appropriate
7 hours: not recommended
10 hours:
recommended
<7 hours:
adolescent’s sleep
Fig. 8.2 Number of hours the adolescents should sleep per day and how much they actually sleep.
Adapted from Hirshkowitz etal. [64]. (Authors thank Dr. Sergio Frumento for having adapted the
gure)
8 Relationship Between Emotions, Sleep andWell-Being

158
which lead to decreased well-being, dened as a reduction of subjective quality of
life and life satisfaction, prevalent negative mood and emotions and absence of
meaning in life [74].
A large number of cross-sectional studies showed that poor sleep is associated
with decits in emotion regulation, reduction of well-being and health-related qual-
ity of life [75–78] as well as increased anxiety [79], depression [80], aggression and
hostility [81], academic failure [82, 83], legal and illegal drug use [84, 85] and
accidents [82]. Longitudinally, poor sleep in adolescence can cause long-term
reductions in well-being and life satisfaction, increased anxiety, depression, sub-
stance use and bad educational outcomes [86–93]. To sum up, all the above-
mentioned psychological and behavioural outcomes are associated with prolonged
conditions of bad sleep (i.e. chronic sleep deprivation or ‘sleep debt’ [94]), and are
united by the lack of emotion regulation [24].
8.4 Sleep Deprivation andEmotion Dysregulation
Experimental psychophysiological studies of sleep deprivation have detected sub-
jective and objective signs of emotion dysregulation, at the level of both the central
and autonomic nervous system. In adults, one night of sleep deprivation increases
amygdala activation up to 60%, in reaction to negative pictures (e.g. weapons,
snakes, mutilations), indicating an inability to down-regulate negative emotions
[95]. Amygdala hyperactivity has been detected also after a more ecological sleep
deprivation protocol (ve nights of 4-h sleep restriction), using subliminally pre-
sented frightened faces [96]. Decreased functional connectivity between the medial
PFC and the amygdala, together with the hyperreactivity of the latter, has been
related to less than 6h of habitual sleep per night [97–99]. Moreover, sleep depriva-
tion impairs recognition of emotional facial expressions [100, 101] and increases
the distractibility caused by emotional images, paralleled by increased amygdala
activation and reduced functional connectivity with the PFC [98]. Taken together,
all these studies consider decreased inhibition of the amygdala exerted by the PFC
as a marker of emotion dysregulation after sleep deprivation. Recently, in adults
who underwent a fear consolidation experimental paradigm, Feng etal. [102] found
that sleep deprivation interferes with top-down ventromedial PFC inhibition of the
amygdala, increasing also bottom-up arousal signalling by the insular pathway
[102]. Notably, insular cortex integrates interoceptive information on the state of the
organism arising from subcortical areas, which are fundamental for adaptive emo-
tional behaviour [103–105]. These data reect an important and still under-
investigated link between altered interoception, emotion dysregulation and sleep
disorders (see [106]). In addition, suggesting an important involvement of the auto-
nomic nervous system, Franzen and collaborators found, in sleep-deprived adults,
that increased sleepiness positively correlated with involuntary pupillary responses
to negative emotional pictures [107]. Sleep deprivation also affects heart rate vari-
ability (i.e. increased the low-frequency component and decreased the high-
frequency component of heart rate variability), indicating an enhancement of
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sympathetic activity [108, 109], which has been related to psychopathology and to
reductions of exibility to emotional challenges [110, 111].
Furthermore, sleep deprivation enhances mesolimbic reward system activity,
which includes the midbrain ventral tegmental area, the striatum and the PFC
(medial PFC and orbitofrontal cortex), and has been related to increased respon-
siveness to reward-stimuli, possibly leading to impulsivity, risk-taking behaviours
and sensation seeking [60] (e.g. licit and illicit drug use; reviewed in [59]).
Specically, sleep deprivation amplies subjectively reported and objectively
detected activity (with functional MRI) throughout the human reward brain net-
work in response to pleasure-evoking stimuli, associated with a reduction of the
coupling between the mesolimbic system and the medial prefrontal and orbitofron-
tal cortices [112].
Unfortunately, unlike adults, sleep deprivation protocols in adolescence are less
numerous, because of various methodological and ethical issues [72]. However,
experiments on adolescents have found coherent results related to emotion dysregu-
lation: for example, sleep restriction protocols in adolescents decrease emotion
regulation, higher level executive functions and positive affect and increase negative
affect (e.g. tension, anxiety, hostility, confusion and fatigue) [113–117].
A number of authors have suggested that sleep deprivation can alter emotion
generation and emotion regulation via different pathways: (1) sleep deprivation may
increase negative emotions by lowering the threshold to aversive stimuli that may be
otherwise discarded [18], by decreasing motivation and ability to interpret goal-
related events [58] and by increasing the encoding of negative memories, selectively
biasing the encoding of positive and neutral ones [118]; (2) sleep deprivation may
cause a state of central and peripheral emotional hypersensitivity that impairs the
communication between brain and body, fundamental for the ‘embodied’ percep-
tion of emotions and leading to indiscriminate emotional generalization [59, 60];
(3) sleep deprivation may alter emotion regulation through behavioural tendencies
and neurophysiological changes, including situation selection (by reducing energy
and activity levels), attention (by increasing selective attention to negative stimuli),
cognitive appraisal (by promoting overgeneralized conservative responses) and
behavioural response (by increasing amplied and maladaptive emotional responses)
[58, 61].
Psychophysiological data suggest that adolescence is a particularly vulnerable
period for sleep deprivation as compared with adulthood. In this regard, using
computerized acoustic analysis, a study found that sleep-deprived adolescents
display fewer positive emotions as compared to adults [116]. Unfortunately, there
is still a paucity of experimental and longitudinal sleep deprivation studies on
adolescents, making it difcult to determine the degree to which psychophysio-
logical consequences of sleep loss overlap (or not) in adolescents and adults [63,
72]. In addition to the well-assessed role of REM sleep in emotions, an under-
investigated role, both for the correct maturation of adolescent brain and, conse-
quently, emotion regulation and well-being, may be played by specic features of
NREM sleep, like slow waves, SSO and sleep spindles [62]. Again, no study has
directly investigated adolescent NREM sleep features in relation to emotion
8 Relationship Between Emotions, Sleep andWell-Being

160
regulation (but see [119] for sleep spindles in adults). This can be a promising line
of research for the future: the study of sleep features in healthy sleep and sleep
loss may provide a unique window onto adolescent cortical maturation, emotion
regulation and well-being [62, 63].
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