Sleep Impact on Perception, Memory, and Emotion in Adults and the Effects of Early-Life Experience

C H A P T E R

39 Sleep Impact on Perception, Memory, and Emotion in Adults and the Effects of Early-Life Experience Monica Lewin*,†,‡, Regina M. Sullivan*,‡, Donald A. Wilson*,‡ *Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, United States †Sackler Neuroscience Graduate Program, NYU School of Medicine, New York, NY, United States ‡Department of Child and Adolescent Psychiatry, NYU School of Medicine, New York, NY, United States

Sleep plays a critical role in emotional regulation, learning, and memory. In adults, disrupting, restricting, or altering sleep can lead to impairments in a wide variety of cognitive and emotional functions. Now, evidence has begun to accumulate suggesting that sleep disturbances during early development can have equally profound and long-lasting consequences. In particular, work from our lab and others explores how early-life adverse events can disrupt sleep across the life span, thus contributing to a variety of negative cognitive and behavioral outcomes. These findings raise the possibility that interventions targeting sleep may have therapeutic value for children or adults exposed to early-life adverse events. Here, we describe sleep and sleep ontogeny and then describe the role of sleep in normal and pathological brain function. Finally, we explore how early-life adverse events and sleep disturbances may reciprocally interact to produce a range of psychopathological outcomes.

I SLEEP, PERCEPTION, AND MEMORY A An Introduction to Sleep As early as the year 200 AD, the Greek physician Galen theorized that sleep was necessary to regulate the temperament, functioning to balance the body’s “humors.” Since Galen, however, sleep was thought to be a passive state: an intermediate between wakefulness and death, during which intellectual and physical functions are suspended (Macnish, 1834). Ivan Pavlov described sleep as an

Handbook of Sleep Research, Volume 30 ISSN: 1569-7339 https://doi.org/10.1016/B978-0-12-813743-7.00039-6

“inhibition” that spreads over the cerebrum and midbrain. Indeed, sleep is a state during which the cerebrum is unresponsive to the environment; however, in no way is sleep an “off” switch for neural processes. The first use of EEG during human sleep by Hans Berger in 1928 revealed coordinated neural activity during sleep, but it was not until the discovery of rapid eye movement (REM) sleep by Asterinsky, Kleitman, and Dement between 1953 and 1957 that sleep was perceived as an active state. Their discovery of wake-like, low-voltage, high-frequency oscillations during REM sleep began a deeper investigation into neural processes occurring in sleep. Asterinsky and colleagues discovered five distinct sleep stages in humans. These included REM sleep and non-REM (NREM) sleep stages 1–4. Stage 1 of NREM sleep represents the lightest 2%–5% of sleep and is characterized by low-voltage, mixed-frequency waves often accompanied by slow, rolling eye movements. Stage N2, indicated by the appearance of K-complexes and sleep spindles, is the most abundant component of sleep. Guidelines released by the American Academy of Sleep Medicine (AASM) since 2008 no longer distinguish between NREM stages 3 and 4 and instead combine them into the category “slow-wave sleep.” Slow-wave sleep (SWS) is composed of low-frequency, high-voltage oscillations called delta waves. Throughout the night, the sleeper will cycle through these stages approximately every 90–120 minutes. During the first half of the night, the sleeper will spend a greater proportion of time in SWS, with less time spent in REM sleep; the second half

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of the night is spent predominantly in stage 2, with an increased proportion of REM sleep. Although a detailed description of the numerous changes in somatic physiology, neural activity, and neuromodulation that occur during sleep is outside the scope of this chapter, it is worthwhile to note certain changes that illustrate the difference between NREM and REM (Table 39.1). The transition from wake to NREM sleep is accompanied by a loss of aminergic and cholinergic neuromodulatory tone, inhibited thalamocortical relay of sensory information, and a suppression of activity in frontal and limbic regions. During REM sleep, activity in lateral prefrontal areas continue to be suppressed, yet cholinergic tone rises again as in wake, and the occipital cortex, medial prefrontal cortex, and limbic areas are reactivated (Braun et al., 1997; Maquet et al., 1996). Because of the several wake-like features present in REM, it is sometimes referred to as “paradoxical sleep.” If we consider that key areas involved in visualization, memory, and emotion are highly active during this state, it is unsurprising that individuals awoken from REM report vivid, cohesive, and emotionally charged dreams. REM is commonly known to be the dreaming sleep state, but dreams do also occur during NREM, although NREM dreams tend to be brief, with less sensory richness and more mundane content (Siclari et al., 2017; Stickgold, Malia, Fosse, Propper, & Hobson, 2001).

B Effects of Sleep on Waking Function In both humans and animal models, sleep has been shown to be critical to a vast array of cognitive functions. In humans, partial or total sleep deprivation (TSD) impairs several aspects of cognitive performance, motor performance, and mood (Pilcher & Huffcutt, 1996), resulting in detriments to vigilance, attention, memory, verbal processing, logical reasoning, decision-making, and more (Bonnet & Arand, 2003; Ellenbogen, 2005; Maski & Kothare, 2013; Yoo, Gujar, Hu, Jolesz, & Walker, 2007). Memory in particular has proved to be an extremely rich area of sleep research. Sleep not only prepares the brain to accurately encode a memory but also serves a variety of functions in postacquisition processing. TABLE 39.1 Changes in Neuromodulatory Tone and Functional Activation Characteristic of NREM and REM Sleep States State

Neuromodulatory tone

Functional activation

NREM

# Cholinergic # Aminergic

#Thalamus, BG, BF, ACC, PFC

REM

""Cholinergic # Aminergic

"Thalamus, amygdala, ACC, hippocampus, occipital cortex ##PFC

BG ¼ basal ganglia; BF ¼ basal forebrain; ACC ¼ anterior cingulate cortex; PFC ¼ prefrontal cortex.

Methodology Studies of sleep’s role in memory processing are typically conducted by training subjects on a memory task and collecting a baseline measure of recall before subjecting the subject to either a sleep or wake condition and/or measuring or manipulating the subject’s sleep in some fashion. Following the sleep period, subjects will be retested on the task to assay any changes in memory compared with a control condition or group. Manipulations during sleep can include depriving the subject of nighttime sleep entirely, or selectively depriving them of a specific sleep stage, to observe any resulting effects on memory recall. At one time, selective deprivation of SWS or REM sleep was a popular tool used to identify the role of these stages. However, deprivation studies faced early criticism for nonspecific detrimental effects on cognitive function and, in the case of animal studies, the confounding effects of stress induced by the method of sleep restriction. In response, researchers capitalized on the differential sleep stage composition of the first and latter halves of the night to investigate the role of specific sleep stages in memory. In doing so, they revealed that SWS-rich early sleep and REM-rich late sleep each benefit a different type of memory (Fowler, Sullivan, & Ekstrand, 1973; Plihal & Born, 1999; Yaroush, Sullivan, & Ekstrand, 1971). An alternate approach to intervening in the subject’s sleep involves observing sleep composition following the learning experience using polysomnographic recordings. Subjects’ baseline sleep composition after a learning experience is compared with their sleep at baseline, and/ or postlearning sleep parameters are correlated to memory recall. Finally, some studies implement methods that manipulate sleep; these may involve the enhancement of sleep-related oscillations, pharmacological interventions, or targeted memory reactivation during a sleep stage of interest (Barnes & Wilson, 2014b; Bendor & Wilson, 2012; Marshall, Helgadottir, Molle, & Born, 2006; Rasch, Buchel, Gais, & Born, 2007).

C Stages of Memory Processing Debate on whether sleep may protect memory from outside interference, versus actively stabilize, consolidate, enhance, or generalize memories, is still active (Ellenbogen, Payne, & Stickgold, 2006). Following acquisition (called encoding), new memories are malleable, subject to interference by competing or disrupting information. If they are able to avoid this, memories will become stabilized over time (McGaugh, 2000). One theory in the role of sleep in memory is that sleep provides an opportunity for memories to stabilize in the absence of interference from external stimuli (Wixted, 2004).This kind of stabilization may involve the transfer of memory traces from the hippocampus to cortex (Gais et al., 2007; Lewis & Durrant, 2011; Takashima et al., 2006),

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sometimes called system consolidation (Dudai, Karni, & Born, 2015). However, sleep may be required for an aspect of memory consolidation that involves enhancement without further practice (Walker, 2005). Enhancement may be evident in the recovery of seemingly lost memories, improvement of a skill, or by extracting insight through the process of consolidation. Sleep has been shown to facilitate the integration of newly learned information into existing schema (Tamminen, Payne, Stickgold, Wamsley, & Gaskell, 2010), bridgerelated experiences together to create abstract conceptual knowledge (Ellenbogen, Hu, Payne, Titone, & Walker, 2007; Graveline & Wamsley, 2017; Wagner, Gais, Haider, Verleger, & Born, 2004), or to extract the “gist” of recently learned information (Lewis & Durrant, 2011; Payne et al., 2009). While the majority of sleep-related memory functions focus on retaining, consolidating, or enhancing memory representations, sleep may simultaneously function to induce forgetting of certain memory representations (Stickgold & Walker, 2013). This may reflect the homeostatic role of sleep in regulating synaptic plasticity (Tononi & Cirelli, 2013). Several of these mechanisms of memory consolidation are hypothesized to originate from a fundamentally Hebbian system in which memory representations are reactivated during sleep. Experience-dependent replay during SWS has been consistently replicated in animals ( Ji & Wilson, 2007; Lewis & Durrant, 2011; Wilson & McNaughton, 1994). Replay may also occur during REM sleep (Laureys et al., 2001; Louie & Wilson, 2001; Maquet et al., 2000), and task-related dream content has been associated with enhanced memory at testing, but a clear mechanism of REM-dependent memory enhancement has not been established (Hennevin, Hars, Maho, & Bloch, 1995; Walker & Stickgold, 2004). However, a defined theory of SWS-dependent memory systems has been proposed wherein during SWS, slow oscillations (<1 Hz) are generated by the prefrontal cortex. Their up and down phases are composed of massive, simultaneous activation and quiescence, respectively. During these up states, 11–15 Hz events called sleep spindles are generated by the thalamus and propagated to the neocortex. Simultaneously, high-frequency events generated by the hippocampus, called sharp-wave ripples, occur nested within the cortical spindle troughs. These coordinated events are thought to selectively trigger reactivation of memory representations during postlearning sleep (Diba & Buzsaki, 2007; Khodagholy, Gelinas, & Buzsaki, 2017; Sirota & Buzsaki, 2005) while simultaneously inducing the depression of irrelevant memory traces (Tononi & Cirelli, 2006, 2013). Indeed, all three of these events—slow oscillations, spindles, and sharp waves—have been correlated with enhanced memory consolidation.

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While most work on sleep-dependent memory consolidation in animal models has focused on the hippocampus and thalamocortical systems, the basic mechanisms may reflect general principles across systems. For example, the olfactory system is an evolutionarily old system, involving olfactory sensory neuron input to the olfactory bulb (a forebrain cortical structure), which in turn projects directly to the olfactory cortex, a three-layered archicortical structure, with no intervening thalamic relay (Linster & Cleland, 2003). The piriform cortex displays sharp waves during NREM sleep (Murakami, Kashiwadani, Kirino, & Mori, 2005; Wilson, 2010), and single-unit activity during sharp waves is shaped by recent olfactory experience (Barnes & Wilson, 2014a, 2014b). Similar to processes in hippocampus, piriform cortex sharp waves during NREM sleep appear to allow replay of recently learned odor associations and influence both the strength and accuracy of odor memory (Barnes & Wilson, 2014a, 2014b). See below for more details.

D Different Sleep Stages for Different Memories Ultimately, whether sleep serves to preserve, enhance, or integrate memories and which stage is responsible appear to depend on the kind of memory being tested. Human memory can be broadly divided into two major categories: declarative and nondeclarative (Squire, 2004; Fig. 39.1). Declarative memory refers to conscious and verbally accessible fact-based memories, including episodic memory for autobiographical events, spatial memories, and semantic memory for items of general knowledge.

FIG. 39.1 Classification of memory types associated with sleepdependent consolidation.

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In contrast, nondeclarative memories encompass a wide range of types of learning, ranging from simple kinds of learning like conditioning, perceptual learning, and priming to more complex types of procedural memory and motor skill learning.

E Role of Sleep in Declarative Memory Consolidation In 1924, Jenkins and Dallenbach sought to test the effect of sleep on Ebbinghaus’ theory of memory decay. They found that subjects’ memory for the pronunciation of nonsense syllables was doubled if the delay interval contained sleep, compared with the same duration of wake. As a result, the majority of early investigation focused on sleep’s effects on human declarative memory, using tasks assessing recall for paired associates, vocabulary, and more (Smith, 2001). Several other early studies (Benson & Feinberg, 1975; Van Ormer, 1933) showed better retention of short stories, nonsense syllables, and paired associates after periods of sleep compared with periods of wake. It became relatively well established that declarative memories will be better retained if studied before bed and recalled the next morning, rather than learning them in the morning and testing them that night. More recently, this kind of paradigm faced criticism for potential confounds due to sleep pressure and circadian influences on performance. To avoid this, researchers began to use extended delay retention periods or daytime naps to control for sleep debt and circadian factors (Mednick et al., 2002; Wamsley, Tucker, Payne, & Stickgold, 2010). These studies confirm that sleep occurring shortly after the learning period will produce better memory at testing. It was initially hypothesized that declarative memory was being rehearsed during the vivid, wake-like dreams of REM sleep. However, experiments using REM deprivation provided mixed results (Vertes & Eastman, 2000). Following this, split-night experiments were conducted using memory for lists of paired associates (declarative memory) and mirror tracing (procedural memory) (Fowler et al., 1973; Plihal & Born, 1999; Yaroush et al., 1971). These experiments determined that SWS benefits declarative memories and that REM enhances nondeclarative memories. This finding has, for the most part, held up in the face of additional investigation. However, since no learning task can truly engage any single-memory system in isolation, many studies have produced conflicting results. For example, several kinds of complex learning experiences have been found to induce increases in REM sleep in the following nights (Mandai, Guerrien, Sockeel, Dujardin, & Leconte, 1989; Smith & Lapp, 1991). Furthermore, recall for both declarative and nondeclarative tasks have also been correlated with NREM stage 2 sleep or sleep spindle

density, and declarative memory for emotional content appears to be preferentially consolidated by REM sleep rather than SWS (see below). Although a direct causal role of SWS in declarative memory consolidation has not established, a strong link between SWS and declarative memory is apparent. For example, patients with primary insomnia experience a reduction in SWS, which is correlated with impaired memory consolidation (Backhaus et al., 2006); similarly, the aging-associated decline in declarative memory consolidation is correlated with a cooccurring decline in SWS (Backhaus et al., 2007). In healthy adults, overnight declarative memory retention is correlated with greater proportions of SWS (Backhaus et al., 2006). Additionally, potentiating slow-wave activity (SWA) during SWS has been shown to enhance declarative memory retention (Marshall et al., 2006; Marshall, Molle, Hallschmid, & Born, 2004; Ngo, Martinetz, Born, & Molle, 2013; Prehn-Kristensen et al., 2014). Declarative memories are assumed to be hippocampusdependent and later transferred to cortical structures. In nonhuman animal models, declarative-like memory is modeled by using hippocampus-dependent learning tasks. Several tasks using spatial learning have demonstrated that postlearning SWS is critical for memory consolidation. As previously mentioned, hippocampal and cortical reactivation following spatial learning has been shown during SWS in animals (Peigneux et al., 2004).

F Role of Sleep in Nondeclarative Memory Consolidation There also appears to be an important role for sleepdependent enhancement of nondeclarative memory. Specifically, consolidation of motor skill learning, motor sequence learning, and perceptual learning appear to involve REM and stage 2 NREM sleep (Smith, 2001; Stickgold, 2005), although the involvement of REM is, again, highly controversial (Saxvig et al., 2008; Tilley & Empson, 1978). Successful learning of tasks with any procedural component has been shown to increase REM sleep content and change the frequency or density of REMs in proceeding sleep periods, and in animals, learning in both appetitive and aversive tasks has also been demonstrated to involve REM sleep (Albert, Cicala, & Siegel, 1970; Hennevin et al., 1995; Smith & Butler, 1982). After learning, rodents show an increase in REM sleep, and REM deprivation during the immediate postlearning sleep period can block sleep-related improvement on the task. However, several studies show that human procedural memory enhancement relies on stage N2, rather than REM. A commonly used measure of procedural/motor learning is performance on a serial reaction time task, in which finger tapping accuracy

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and speed will improved after sleep (Walker, Brakefield, Morgan, Hobson, & Stickgold, 2002). In fact, the improvement over sleep appears to exceed that that can be accomplished with additional practice. Improvements in this task were associated with time in stage N2 and sleep spindle density. In nonhuman animal models, NREM can play a critical role in consolidation of associative memory and perceptual learning. For example, NREM sleep is involved in both the strength and the accuracy of olfactory associative memory consolidation. NREM sleep promotes at least two state changes conducive to memory consolidation in the olfactory system (and other systems). First, the olfactory cortex becomes relatively less responsive to sensory input (Barnes, Chapuis, Chaudhury, & Wilson, 2011; Murakami et al., 2005; Wilson & Yan, 2010). In other sensory systems, this isolation from sensory inputs occurs at the thalamus. In olfaction, where information relay may not involve the thalamus, the reduced responsiveness may occur due to synaptic depression of the olfactory bulb input to the olfactory cortex. The second state change is enhancement in both intra- and intercortical connectivity, allowing distributed cortical neurons to link during sharp-wave-driven odor replay (Wilson, 2010). Imposing additional odor replay during NREM sleep, for example, of a learned aversive odor, enhances the strength of that learned aversion, while the same imposed replay during waking induces extinction (Barnes & Wilson, 2014b). Furthermore, imposing noise input to the olfactory cortex during posttraining NREM by activating normally suppressed olfactory bulb input disrupts accuracy of odor memory consolidation, resulting in fear generalization (Barnes & Wilson, 2014b). Finally, disrupting the normal enhancement in intra- and intercortical connectivity that occurs during posttraining NREM also impairs the accurate consolidation of odor fear (Barnes & Wilson, 2014b). In addition to olfaction, sleep also plays a role in visual and auditory perceptual learning. A series of experiments tested visual adaptation in subjects asked to wear perceptually distorting lenses. Subjects who adapted to the task demonstrated an increase in REM sleep, and their dreams contained more motor and visual content than subjects who did not adapt as completely (De Koninck, Prevost, & Lortie-Lussier, 1996; Zimmerman, Stoyva, & Reite, 1978). In addition to visual perceptual learning, auditory learning also results in REM sleep increases (Verschoor & Holdstock, 1984).

G Sleep in Emotional Memory Consolidation Emotional memory appears to be particularly sensitive to sleep-dependent processes. Pretraining sleep deprivation has been shown to impair the processing of emotional information at the encoding stage

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(Alfarra, Fins, Chayo, & Tartar, 2015) and decrease performance in emotional learning paradigms (Bonnet & Arand, 2003; Ellenbogen, 2005; Maski & Kothare, 2013; Yoo et al., 2007). Memory for items with emotional content tends to be enhanced over memory for neutral stimuli (Phelps, 2004), where the degree of amygdala activation is positively correlated to recall (Cahill et al., 1996). One hypothesis for this differential effect of deprivation on emotional memory is that the sleep-deprived brain enters a state of prefrontal hypofunction and thus is unable to suppress amygdala hyperactivity (Yoo et al., 2007). Additionally, sleep-deprived subjects show increased functional connectivity between the amygdala and locus coeruleus, associated with a 60% increase in amygdala activation in response to emotionally negative stimuli (Yoo et al., 2007). After sleep deprivation, encoding is broadly impaired for both neutral and positive valence emotional content, but memory for negative valence items remains intact (Walker & van der Helm, 2009). Thus, sleep loss appears to create a negative memory bias, which could contribute to the formation of mood and anxiety disorders. We will discuss this topic further in the following section. In animal models, selective REM sleep deprivation creates a very similar pattern of impairment in encoding. Pretraining REM sleep deprivation disrupts the acquisition of negative associations, including taste aversion and passive and active avoidance learning (McGrath & Cohen, 1978; Smith, 1985). After REM sleep deprivation, hippocampal neurons are less excitable, and synaptic plasticity (such as long-term potentiation) that can be formed under these conditions rapidly deteriorates (Davis, Harding, & Wright, 2003). Sleep after a learning experience is also critical to the retention of emotional memories. After a period of intense learning, the sleep of both humans and animals will have increases in REM sleep and REM density. Rodent models show that sleep, both REM and NREM, immediately after training is critical for emotional learning and memory (Barnes et al., 2011; Graves, Heller, Pack, & Abel, 2003; Smith, 1985); sleep deprivation during the hours immediately posttraining will impair memory retention at later test (Graves et al., 2003). This may be due to the time course of norepinephrine release after an emotionally arousing learning experience, which changes the function of thalamocortical information transmission (Sara, 2017; Vanderheyden et al., 2015; Vanderheyden, Poe, & Liberzon, 2014), though note this is also true of olfactory fear memory, which does not include thalamocortical transmission (Barnes et al., 2011). In humans, memory for emotional stimuli has been linked to REM as well. Numerous studies have found that memory for emotionally charged stimuli is enhanced after sleep and is correlated with the time spent in REM sleep. This may be due to the hypercholinergic state associated with REM sleep

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(Hutchison & Rathore, 2015); posttraining infusions of cholinergic agonists into the rodent amygdala has been shown to enhance memory for tasks with affective salience, and antagonists in the consolidation phase impair memory (McGaugh, 2004). As REM sleep abnormalities and hyperarousal during sleep are hallmarks of depression and posttraumatic stress disorder (PTSD), respectively, sleep-dependent emotional memory processing may have significant implications for the development of psychopathology.

II SLEEP AND PSYCHOPATHOLOGY A A Learning Model of Sleep and Psychopathology According to current cognitive-behavioral perspectives in clinical psychology, mood and anxiety disorders are characterized by maladaptive thought patterns and behaviors (Beck, 1970; Beck, 2008). Although they can be initiated by environmental or biological precipitating factors, these dysfunctional schema appear to be at least partially causal: training the patient to adopt more adaptive patterns of cognition and behavior is overwhelmingly successful in reversing numerous psychopathological states (Butler, Chapman, Forman, & Beck, 2006). Now, imagine the cognitive and behavioral landscape of the individual suffering from chronic sleep disturbance. The underslept individual is irritable, and emotional reactivity to mild stressors is heightened (Minkel et al., 2012; Talbot, McGlinchey, Kaplan, Dahl, & Harvey, 2010). Cortisol levels rise in response to chronic partial sleep loss, among other endocrine dysfunctions (Leproult, Copinschi, Buxton, & Van Cauter, 1997; Spiegel, Leproult, & Van Cauter, 1999), and the brain’s emotional response to stimuli is altered in a variety of ways (Alfarra et al., 2015; Goldstein & Walker, 2014; Yoo et al., 2007), including increased amygdala reactivity in response to and in anticipation of negative stimuli. The dispiriting effects of the day’s negative experiences are amplified, and the positive events lose their ability to motivate (Zohar, Tzischinsky, Epstein, & Lavie, 2005). As mentioned previously and in other chapters, sleep is critical for emotional memory encoding and consolidation. After sleep loss, memories with positive or neutral valence fail to encode, but memory for negative events will be spared, consolidated, and generalized (Walker & van der Helm, 2009). The underslept individual’s homeostatic forces result in REM rebound, augmenting REM sleep and reducing REM latency (Brunner, Dijk, Tobler, & Borbely, 1990). Negative emotional memories may be preferentially consolidated early in the night. Upon waking, memory for recent events is dominated by negative experiences and aversive associations.

Thus, as the chronically sleep-deprived individual learns about the world through their daily experiences, this negative memory bias will be reflected in a dismal and pessimistic worldview, behavioral avoidance, and increasingly negative patterns of cogitation. There may be excessive apprehensive in anticipation of the stimuli recently learned to be aversive (Goldstein et al., 2013), causing withdrawal from social interactions and avoidance of challenging tasks for fear of failure. Thus, the individual enters a self-perpetuating downward spiral, creating prime conditions for the pathogenesis of depression or generalized anxiety (Beck, 1970; Beck, 2008). With this perspective in mind, it may be unsurprising to learn that nearly all neuropsychiatric disorders have some relationship to sleep dysfunction (Benca, Obermeyer, Thisted, & Gillin, 1992; Harvey, 2001; Wulff, Gatti, Wettstein, & Foster, 2010; Wulff, Porcheret, Cussans, & Foster, 2009). Psychiatric illness is strongly comorbid with both primary sleep disorders and secondary sleep complaints (Breslau, Roth, Rosenthal, & Andreski, 1996; Ford & Kamerow, 1989), where roughly half of individuals reporting sleep problems in the National Comorbidity Survey Replication also met criteria for one or more DSM-IV disorders (Roth et al., 2006). The questions that remain, then, are many. Does sleep disturbance produce psychopathology, or is it a side effect of mental illness? How does sleep disturbance occur? Can treating sleep produce relief from daytime symptoms of these afflictions?

B Sleep Deprivation, Restriction, and Fragmentation Sleep restriction or fragmentation produces a myriad of detrimental effects on mood, cognition, and performance, many of which resemble psychopathologylike symptoms in emotional regulation and cognition (Bonnet & Arand, 2003; Durmer & Dinges, 2005; KahnGreene, Killgore, Kamimori, Balkin, & Killgore, 2007; Pilcher & Huffcutt, 1996). Sleep disturbance can occur organically or be induced behaviorally as a result of occupational or lifestyle factors; these circumstances can also be induced in laboratory settings. An individual can completely eschew sleep for a temporary period, resulting in full nights of sleep loss (TSD); he or she can be deprived of a particular sleep stage, for example, REM, which may occur in syndromes where a specific sleep stage is interrupted by biological factors or suppressed by medications; sleep may be fragmented throughout the night due to medical or biological causes; and finally, and most commonly, individuals can accumulate sleep debt through chronically restricted sleep times. TSD has been shown to produce immediate effects on neural and behavioral measures of cognitive performance, executive function, and mood (Bonnet & Arand,

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2003; Durmer & Dinges, 2005; Pilcher & Huffcutt, 1996). Neuroimaging show that TSD produces reduced (taskrelated and/or resting state activation) activity in the prefrontal cortex that corresponds to reduced executive functioning. Furthermore, 56 hours of TSD produced elevated symptoms of anxiety, depression, and paranoia (KahnGreene et al., 2007). In addition, completing a low-stress task after 48hrs sleep deprivation resulted in elevated subjective stress levels and negative mood relative to rested controls (Minkel et al., 2012). However, there appears to be interindividual variation in the degree of tolerance to sleep loss (Van Dongen, Maislin, & Dinges, 2004). Cases of prolonged TSD outside of the laboratory are rare, occurring mostly in specific occupational sectors such as health care or transportation, but chronic partial sleep deprivation is extremely common (Bonnet & Arand, 1995). On average, the healthy adult requires between 7 and 9 hours of sleep for full functioning (Bonnet & Arand, 1995). As sleep is restricted below this amount, sleep debt will accumulate, and the individual will approach levels of neurocognitive impairment indistinguishable to TSD (Banks & Dinges, 2007). During chronic partial sleep restriction, SWS time is mostly preserved, while losses occur in NREM stage 2 and REM sleep. For example, chronic partial sleep deprivation (Van Dongen, Maislin, Mullington, & Dinges, 2003) restricting time in bed to 6 hours reduced nightly N2 sleep by 1 hour and REM sleep by about 24 minutes. Restricting time in bed to 4 hours reduced nightly N2 sleep by 2 hours and REM by 47 minutes. The same study compared the dose-dependent effects of sleep loss on neurocognitive performance and found that vigilance and reaction times were near-linearly related to increasing cumulative time spent awake in excess of about 16 hours. Thus, contrary to widespread belief, 6 or 4 hour periods of sleep are not sufficient to completely restore cognitive function. Also contrary to popular wisdom, subjects did not eventually “get used to” the reduction in sleep. In fact, cognitive functions, especially attentional vigilance and working memory, continued to decline as the subjects accrued additional hours of sleep debt and, over time, eventually reached levels of impairment resembling several days of TSD. In spite of this continual performance decay, individuals in the 6 and 4 hour sleep conditions report only slightly increased levels of subjective sleepiness. The fact that self-assessment of alertness does not reflect actual impairment makes sleep loss particularly dangerous. For example, an individual suffering from severe sleep debt may feel alert enough to operate heavy machinery, but their psychomotor vigilance will likely be impaired. In reality, this is an extremely frequent occurrence; an estimated 13% of workplace injuries can be attributed to sleep problems (Uehli et al., 2014). Several other studies have replicated the detrimental effects of chronic sleep loss on psychomotor vigilance (Durmer & Dinges, 2005).

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Chronic partial sleep restriction appears to particularly impact mood (Pilcher & Huffcutt, 1996). A linear relationship with cumulative sleep debt has been found for ratings of decreased vigor, confusion, tension, and overall mood disturbance (Dinges et al., 1997). Sleep fragmentation may occur via several medical conditions with symptoms that interrupt sleep. Prominently, primary sleep disorders result in fragmentation throughout the night, or in specific sleep stages. Obstructive sleep apnea (OSA) is characterized by periods of interrupted breathing, which can occur hundreds of times throughout the night. In OSA, the exertion and muscle tone restoration required to resume breathing results in neurological arousals and repetitive disruption of the sleep cycle. Episodes of apnea may occur most frequently in REM sleep, when muscle tone is lowest, and in some cases may create stage-specific sleep restriction. As a result, the sleep of the apneic patient is unrefreshing. Within adults, OSA produces symptoms of excessive daytime sleepiness, irritability, and impairments in concentration and vigilance. In children, OSA frequently presents with symptoms of inattention, hyperactivity, and impulsivity that mirror ADHD and OSA treatment via surgical tonsillectomy and adenectomy is able to reverse these symptoms (Sedky, Bennett, & Carvalho, 2014). Studies have taken care to demonstrate that the daytime effects of OSA are due to sleep fragmentation, rather than hypoxemia (Colt, Haas, & Rich, 1991). Other primary sleep disorders disrupting sleep include restless legs syndrome (RLS) and periodic limb movement disorder (PLMD). RLS is a disorder characterized by discomfort and an urge to move the legs. These sensations are generally increasingly severe at night, resulting in fragmented sleep. PLMD is a separate but often cooccurring disorder in which patients experience stereotyped, involuntary movements of the arms or legs in periodic intervals across the night. Movement episodes associated with PLMD will only occur during NREM sleep, and not REM, due to the inhibition of muscle tone. Both of these disorders are associated with sleep fragmentation and daytime impairments and are also frequently comorbid with ADHD (Cortese et al., 2005; Picchietti, England, Walters, Willis, & Verrico, 1998). In addition to ADHD, these disorders of sleep fragmentation are associated with comorbidities across the spectrum of neuropsychiatric illness. In a study drawing from a large Veterans Health Administration database, OSA was associated with significantly higher incidence of comorbid PTSD, depression, bipolar disorders, anxiety, dementia, and psychosis, in descending order of relative odds compared with the nonapnea group (Sharafkhaneh, Giray, Richardson, Young, & Hirshkowitz, 2005). Longitudinal studies have shown that both OSA and RLS are risk factors for the development of new depression

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(Li et al., 2012; Peppard, Szklo-Coxe, Hla, & Young, 2006). RLS and PLMD are also associated with PTSD, panic disorder, GAD, and elevated subclinical anxiety symptoms (Cho et al., 2009; Scholz et al., 2011; Winkelmann et al., 2005).

C Comorbidity, Endophenotypes, Risk As described previously, directly disrupting sleep produces cognitive and emotional disturbances that bear strong resemblance to psychiatric illness. Furthermore, several types of somatic pathology known to fragment sleep also greatly increase the risk of later psychopathology. In fact, nearly all psychiatric illnesses are associated with sleep changes (Benca et al., 1992) and sleep complaints (Breslau et al., 1996). Sleep disturbances occur at all stages of disease, including prodrome and remission, and have been repeatedly shown to increase the risk of new-onset psychopathology. Whether these sleep disturbances are simply an unrelated aspect of disease prodrome or whether they may be a precipitating factor for the development of illness is not certain, but treatments targeting sleep do appear to improve daytime functioning for psychiatric patients with comorbid sleep problems. Here, we will briefly describe these relationships in several of psychiatric populations. Affective disorders are historically linked to sleep disturbances. Sleep changes are a diagnostic criterion for each of the mood disorders listed in the DSM. Subjectively, patients with a major depressive disorder report significantly more insomnia, nocturnal awakenings, and nonrestorative sleep (Peterson & Benca, 2006). Depression may present with either insomnia or hypersomnia, though the latter is more common in the case of depression with atypical features and bipolar depression. In the case of bipolar disorder, the DSM-5 now requires fluctuations in sleep or energy to be present for diagnosis. Although sleep disturbances have been shown to occur in all stages of bipolar disorder, including remission (Salvatore et al., 2008), a key symptom of mania is markedly reduced sleep time and a reported decrease for the need of sleep. During a manic episode, patients may sleep for a few hours a night, or not sleep at all, for days at a time. However, even small reductions in sleep time have been shown to predict the onset of a manic or hypomanic episode in bipolar individuals (Wehr, Sack, & Rosenthal, 1987). Studies of patients with adult and pediatric bipolar disorder find that reduced sleep need was correlated with worse daytime functioning, and patients who exhibit sleep disturbances are significantly more impaired than those who do not (Baroni, Hernandez, Grant, & Faedda, 2012; Etain et al., 2017). Not only is sleep loss a known symptom of the illness, but also sleep loss itself is likely to be a primary causal factor in the genesis of mania (Wehr et al., 1987). In confirmation of this, experimental sleep deprivation in depressed bipolar

patients has been shown to induce both transient and sustained switches to manic or hypomanic states in a majority of patients (Wehr et al., 1987). Polysomnographic findings of individuals suffering from mood disorders show increased sleep latency with reduced sleep efficiency, total sleep time, and SWS% (Benca et al., 1992). Additionally, changes in REM have been suggested as a specific biomarker of depression, as depressed patients show reduced REM latency, increased REM%, and greater REM density (Baglioni et al., 2016; Benca et al., 1992). Certain sleep changes are stable over the course of remission and relapse (Argyropoulos & Wilson, 2005), which may suggest that individuals with preexisting sleep abnormalities could be more susceptible to depression. As mentioned earlier, the increases in REM sleep and short REM latency present in these individuals may lead to a disproportionate enhancement of negative memories. Conversely, an alternate explanation for this trait-like REM enhancement may be that it is a direct result of intensive learning of negative associations made throughout the day. Generally, antidepressant drugs have been shown to suppress REM and prolong REM latency, counteracting two hallmark features of depression (Winokur et al., 2001). The increased aminergic tone (serotonin, dopamine, and norepinephrine) produced by these drugs is thought to inhibit REM-promoting nuclei (Argyropoulos & Wilson, 2005). This effect can be seen as early as 1 week into treatment, leading many researchers to speculate that the REM-suppressive effects of these drugs contribute to their efficacy. However, the relationship between sleep architecture and drug response appears to be mixed, with antidepressants showing a wide range of effects on sleep continuity, slow-wave oscillation power, and REM (Argyropoulos & Wilson, 2005). In both unipolar depression and bipolar disorder, sleep disturbance is associated with greater symptom severity and increased suicidality (Liu et al., 2007; Malik et al., 2014; Urrila et al., 2012). Insomnia is extremely prevalent in depression, affecting between 50 and 95 of depressed individuals. A history of insomnia increases the risk of developing new depression by approximately fourfold and is correlated to illness severity and recurrence of future depression (Franzen & Buysse, 2008). Several studies aimed at depressed patients with comorbid insomnia have shown that cognitive-behavioral therapy for insomnia (CBT-I) or hypnotic drugs concurrent with typical treatment produces more rapid treatment response, better remission rates, and improvements in depressive symptoms (Fava et al., 2006; Manber et al., 2011; Taylor & Pruiksma, 2014). This strategy has also shown to be effective in euthymic bipolar patients with comorbid insomnia; treatment with CBT-I was able to produce improvements in cognitive performance (working memory and verbal learning) by decreasing time in extended periods of wake

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III TRAUMA, SLEEP, AND PSYCHOPATHOLOGY IN DEVELOPMENT

and reducing variability in sleep duration (Kanady, Soehner, Klein, & Harvey, 2017). Clearly, regular and sufficient sleep is crucial for individuals with bipolar disorder, even in periods of remission or euthymia. Future studies are needed to evaluate the therapeutic value of sleep-targeting interventions for patients without a concurrent diagnosis of insomnia. Insomnia is also highly comorbid with anxiety disorders ( Jansson-Frojmark & Lindblom, 2008; Soehner & Harvey, 2012; van Mill, Hoogendijk, Vogelzangs, van Dyck, & Penninx, 2010), PTSD (Germain, 2013), and ADHD (Cortese, Faraone, Konofal, & Lecendreux, 2009). The links between ADHD and sleep include both ADHD symptomology (Owens, 2005) and network activity (Castellanos & Proal, 2012). As with depression, in many cases, targeting sleep either pharmacologically or through behavioral therapy helps alleviate the symptoms of the comorbid primary psychopathology. A summary of the wealth of data on these associations is beyond the scope of this chapter but are partially summarized in Table 39.2.

III TRAUMA, SLEEP, AND PSYCHOPATHOLOGY IN DEVELOPMENT A bidirectional relationship between psychopathology/trauma and sleep disturbance has been established in adults. Sleep disruption during development, however, could be particularly insidious, given the important role of sleep in shaping neural circuits and synaptic connectivity. For example, traumatic experiences in childhood have been shown to produce sleep disturbances, both acutely and persistently throughout the life span. Early trauma has been reliably associated with later life psychiatric disturbance; a major putative mechanism of this is likely to be exaggerated stress response and altered amygdala function. However, sleep may also be bidirectionally involved in this elevated risk. Sleep disturbance induced by adverse early-life events may lead to later psychiatric disturbance. Alternatively (or concurrently), TABLE 39.2 In Psychiatric Patients With Comorbid Insomnia, Treatments Targeting Sleep May Also Reduce Symptoms of Psychopathology Psychiatric population

CBT-I

Nighttime pharmacotherapy

Enhancement of SWA

Depression

✓

✓

?

PTSD

✓

✓

Anxiety

✓

✓

ADHD

✓

✓

Bipolar disorder

✓

✓

✓

601

the hyperarousal and emotional disturbance induced by these adverse developmental events may result in sleep disturbance as a secondary outcome.

A Trauma and Psychopathology Broadly, psychiatric disorders are thought to arise through an interaction between diathesis and stress (Salomon & Jin, 2013). However, the experience of extreme stress itself, if it occurs during development, appears to form a diathesis for later psychiatric illness. Individuals exposed to significant childhood adversity have been reliably shown to be at increased risk for later life psychopathology (Gershon, Sudheimer, Tirouvanziam, Williams, & O’Hara, 2013; Kessler et al., 2010; Norman et al., 2012; Teicher & Samson, 2013). An estimated 30% of psychiatric disorders can be attributed to adverse childhood experiences (Afifi et al., 2008). Studies of childhood adversity may include a diversity of traumatic stressors, but traumatic experiences relating to dysfunctional relationships with the caregiver, such as abuse and neglect, appear to be most deleterious. This has been modeled in animal research; most commonly, early-life trauma is induced via either prolonged deprivation of maternal care and nutrition, maternal maltreatment, or maternal odor-aversive conditioning paradigms. Although, as in humans, the developmental timing of the trauma appears to produce variations in behavioral disturbance (Teicher & Samson, 2013), animals subjected to these early stress paradigms demonstrate symptoms of psychopathology in later life (Opendak, Gould, & Sullivan, 2017), including depressive and anxiety-like behaviors in adolescence and adulthood (Aisa, Tordera, Lasheras, Del Rio, & Ramirez, 2007; Opendak et al., 2017; Raineki et al., 2015; Raineki, Cortes, Belnoue, & Sullivan, 2012; Tractenberg et al., 2016). They are abnormally combative in response to threat cues, for example, they will approach the source of a predator odor rather than hiding or freezing (Perry & Sullivan, 2014). This resembles what is found in human victims of early-life abuse, who have an elevated incidence of aggressive and antisocial behavior (Lyons-Ruth, 2008).

B How Does This Occur? Acutely, a mammal’s response to stress includes increases in HPA axis function and the release of glucocorticoids, which are generally beneficial to prepare an animal to contend with an extended stressor. The response will also include sympathetic activation of adrenaline in the periphery and increases in noradrenergic signaling from the locus coeruleus, to initiate a fightor-flight response. However, in early postnatal development, approximately in the first two weeks after birth, rodent pups enter a “stress nonresponsive period” in which the HPA axis is unresponsive to most stressors

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(Sapolsky & Meaney, 1986; Schapiro, 1968). In spite of this, certain stressors, particularly alterations in maternal care, are able to overcome this inhibition, resulting in premature increases in the neuroendocrine stress response (Francis & Meaney, 1999; Rice, Sandman, Lenjavi, & Baram, 2008; Rincón-Cortes & Sullivan, 2014). This alters the development of the system, resulting in a modified response to future stressors. Prematurely increasing corticosterone levels in early life, either exogenously or via stressful rearing conditions, causes age-inappropriate expression of fear learning and amygdala activation (Moriceau, Roth, Okotoghaide, & Sullivan, 2004; Moriceau, Shionoya, Jakubs, & Sullivan, 2009). Early-life stress exposure appears to facilitate the learning of future aversive or fearful associations, which may predispose the individual to later psychopathology (Quinn, Skipper, & Claflin, 2014). Both increased and decreased amygdala volume have been found in humans who have experienced extreme stress (Ressler, 2010); rat pups exposed to early-life traumatic experiences show increased amygdala reactivity to later stress as adults (Sanders & Anticevic, 2007). Maltreated individuals have altered neural reactivity (McCrory et al., 2011), impaired emotional regulation in response to interpersonal hostility (Pollak, Vardi, Putzer Bechner, & Curtin, 2005), and hypervigilance to threat-related cues (Dalgleish, Moradi, Taghavi, Neshat-Doost, & Yule, 2001; Parker, Nelson, and Bucharest Early Intervention Project Core Group, 2005; Pollak et al., 2005). This kind of negative attentional bias has been associated with increased anxiety (Beck & Clark, 1997; Shackman, Shackman, & Pollak, 2007) and may predispose these individuals to psychopathology. While glucocorticoid hormones are beneficial for transient stress responses, they also function to suppress cellular growth and proliferation, immune, and antiinflammatory responses (Teicher, Andersen, Polcari, Anderson, & Navalta, 2002). Exposure to stress during early life has been shown to induce deleterious neuroanatomical and functional alterations. Early-life stress is particularly detrimental to brain regions with a protracted ontogeny and development. Early-life stress reduces GABA-A receptor density in the amygdala and LC and reduces adrenergic and GC receptors that mediate negative feedback in the stress response (Teicher et al., 2002). As a result, the neural response to emotional stimuli is exaggerated in victims of early-life trauma as previously described. Anatomical neuroimaging studies have shown that victims of early-life trauma may have reductions in interhemispheric white matter, hippocampal volume, and cortical development (Teicher et al., 2002). Early-life stress has been shown to reduce parvalbumin (PV) expressing GABAergic cells in some rodent models (Belzung, El Hage, Moindrot, & Griebel, 2001; Brenhouse & Andersen, 2011).

Taken together, these findings provide evidence for early-life stress as a toxic neurodevelopmental insult. Indeed, aspects of early-life adverse events bear resemblance to other forms of neurotoxic developmental insult, such as fetal alcohol spectrum disorder (FASD). Developmental exposure to ethanol induces widespread GABAergic cell loss throughout the forebrain (Lewin et al., 2018; Smiley et al., 2015) and is similarly associated with cognitive, emotional, and sleep-related difficulties (Chen, Olson, Picciano, Starr, & Owens, 2012; Goril, Zalai, Scott, & Shapiro, 2016; Troese et al., 2008; Wilson et al., 2016). Recently, Lewin et al. (2018) demonstrated an effect similar to Brenhouse and Andersen (2011) in which pharmacological blockade of PV cell death prevented the development of cognitive and behavioral deficits induced by early-life ethanol exposure. The few studies that examine coexisting FASD and traumatic childhood experience show that these combined neural insults increase the likelihood for cognitive deficits and produce more severe behavioral pathology than either FASD or early-life adverse events alone (Price, Cook, Norgate, & Mukherjee, 2017).

C Early Life Adverse Events and Sleep Sleep/wake cycling undergoes rapid and profound changes during development. From birth to approximately 6 months of age, infants sleep tends to be distributed throughout the day, with approximately half the sleep duration in REM sleep, which is thought to be critical for brain development (Marks, Shaffery, Oksenberg, Speciale, & Roffwarg, 1995; Roffwarg, Muzio, & Dement, 1966). By the time children reach 2 years old, sleep is consolidated to primarily nighttime sleep periods, daytime sleep is reduced, and time in REM decreases to about 25%. As the brain matures, NREM SWA begins to decrease in line with critical milestones in prefrontal development (Feinberg, de Bie, Davis, & Campbell, 2011; Ringli & Huber, 2011). Around adolescence, SWA relocalizes from a more posterior source to a more anterior locus (Kurth et al., 2010), and adolescents’ endogenous circadian preference undergoes an accelerated shift toward a delayed bedtime (Carskadon, Vieira, & Acebo, 1993). The slow postnatal ontogeny of sleep and circadian rhythms makes them vulnerable to early-life adverse events (Palagini, Drake, Gehrman, Meerlo, & Riemann, 2015; Sinha, 2016). Early-life trauma has been associated with sleep disturbances both in the short term (Mysliwiec et al., 2018; Sinha, 2016) and persistently throughout the life span (Brindle et al., 2018; Chapman et al., 2011; Hall Brown, Belcher, Accardo, Minhas, & Briggs, 2016; Palagini et al., 2015). Insomnia is commonly recognized as a disorder of nighttime hyperarousal (Riemann et al., 2010). Increased glucocorticoid (GC)/hypothalamic-pituitary-adrenal (HPA)

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IV SUMMARY

axis and noradrenergic tone has been detected in both adults and children with insomnia (Fernandez-Mendoza et al., 2014; Riemann et al., 2015), and the degree of this hyperarousal is correlated to subjective and objective measures of poor sleep (Mellman, Kumar, Kulick-Bell, Kumar, & Nolan, 1995; Riemann et al., 2015). Similarly, stress and trauma produce insomnia acutely via mechanisms of central and peripheral hyperarousal (Cano, Mochizuki, & Saper, 2008; Charuvastra & Cloitre, 2009; Sinha, 2016). Early-life trauma produces elevated HPA axis function at baseline and amplified, prolonged activation in response to stressors (Rice et al., 2008; Rincón-Cortes & Sullivan, 2014; Tractenberg et al., 2016); it has also been shown to produce abnormal fluctuations in circadian corticosterone levels that persist into adulthood (Poulos et al., 2014). This hyperarousal is one possible candidate to induce the sleep disturbances seen in victims of childhood adversity. While it is established that sleep problems in adulthood can either predict or induce psychiatric illness, what happens when sleep is disrupted in childhood? Are there lasting effects of sleep alteration on the brain during this critical period of development? Longitudinal studies have shown that the presence of sleep disorders in childhood and adolescence are linked to an increased risk for the development of psychological disturbances in later life and vice versa (Gregory & O’Connor, 2002; Shanahan, Copeland, Angold, Bondy, & Costello, 2014). Early-life (<41 months) short sleep patterns predict hyperactivity and impulsivity and poor neurodevelopmental cognitive performance, at the time of school entry (Touchette et al., 2007). Nightmares and night terrors between 2.5 and 9 years old predict development of psychotic experiences at age 12 (Fisher et al., 2014). Several longitudinal studies have found that sleep problems in childhood significantly predict higher levels of depression and anxiety several years later and in adulthood (Greene, Gregory, Fone, & White, 2015; Gregory & O’Connor, 2002). Anxiety and oppositional defiance, both common in ELT populations, have a bidirectional relationship to sleep problems (Peterman, Carper, & Kendall, 2015; Shanahan et al., 2014) (Fig. 39.2).

In instances of early-life stress, the acute sleep disturbance may itself produce changes in mood that could form the diathesis for affective disorders. Poor sleep in the previous night has been shown to predict worse mood in infants and children (Bernier, Belanger, Tarabulsy, Simard, & Carrier, 2014; Mindell & Lee, 2015). Disturbed and hyperaroused sleep following early-life adverse events may also contribute to negative attentional and emotional bias seen in these children. The excessive adrenergic and GC tone present during sleep of children during or after traumatic periods may overfacilitate emotional memory encoding and consolidation (Walker & van der Helm, 2009) and thus set up future cognitive schema for negative cogitation and affective tone. In addition to mood disturbance, sleep loss may have detrimental effects on threat assessment. Adolescents and adults subjected to a semichronic (two-night) sleep restriction responded with a reduction in positive affect; additionally, during a catastrophizing task, they reported greater anxiety and rated the catastrophic events as more likely to occur. The younger adolescent group in this study (Talbot et al., 2010) also rated their personal worries as more threatening when sleepdeprived as compared with when they were rested. In pediatric insomnia, the infant or child is unable to return to sleep without caregiver intervention. This is congruent with findings in rodent models wherein maternal presence and/or attachment related cues are able to modulate corticosterone and norepinephrineinduced amygdala activation and rescue behavioral disturbances due to early-life trauma (Moriceau et al., 2009; Moriceau & Sullivan, 2006; Sevelinges et al., 2011; Shionoya, Moriceau, Bradstock, & Sullivan, 2007). However, poor sleep may impair the infant’s ability to be buffered by a sensitive caregiver (Bernier et al., 2014; Hostinar, Sullivan, & Gunnar, 2014), thus exacerbating the cycle of maladaptive attachment occurring in cases of early-life maltreatment. Thus, in early life, when the brain is undergoing critical periods of development, the effects of sleep disturbance may be even more profound.

IV SUMMARY

FIG. 39.2 Model of potential interactions between early trauma, sleep dysfunction, and psychopathology.

Sleep is critical for a variety of forms of learning and memory, as well as emotional regulation. A myriad of psychopathologies are associated with sleep disruption, and it is increasingly clear that the relationship between sleep and psychopathology is bidirectional—impairment in sleep can exacerbate psychopathology, and psychopathology can impair sleep. These interactions may be especially critical during early development when neural circuits are being fine-tuned and behavioral patterns emerge. Early-life adverse events—from exposure, to neural toxins such as ethanol, to physical abuse—have

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long-lasting consequence for sleep in both humans and animal models. These sleep impacts may contribute to resulting developmental psychopathologies, making sleep health an important potential target for therapeutic intervention.

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