Homework answers / question archive / International Journal of Environmental Research and Public Health Review Mental Sleep Activity and Disturbing Dreams in the Lifespan Serena Scarpelli 1 , Chiara Bartolacci 1 , Aurora D’Atri 1 , Maurizio Gorgoni 1 and Luigi De Gennaro 1,2, * 1 2 * Department of Psychology, “Sapienza” University of Rome, Via dei Marsi, 78, 00185 Rome, Italy; serena

International Journal of Environmental Research and Public Health Review Mental Sleep Activity and Disturbing Dreams in the Lifespan Serena Scarpelli 1 , Chiara Bartolacci 1 , Aurora D’Atri 1 , Maurizio Gorgoni 1 and Luigi De Gennaro 1,2, * 1 2 * Department of Psychology, “Sapienza” University of Rome, Via dei Marsi, 78, 00185 Rome, Italy; serena

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International Journal of Environmental Research and Public Health Review Mental Sleep Activity and Disturbing Dreams in the Lifespan Serena Scarpelli 1 , Chiara Bartolacci 1 , Aurora D’Atri 1 , Maurizio Gorgoni 1 and Luigi De Gennaro 1,2, * 1 2 * Department of Psychology, “Sapienza” University of Rome, Via dei Marsi, 78, 00185 Rome, Italy; serena.scarpelli@uniroma1.it (S.S.); chiara.bartolacci@uniroma1.it (C.B.); aurora.datri@gmail.com (A.D.); maurizio.gorgoni@uniroma1.it (M.G.) IRCCS Santa Lucia Foundation, 00142 Rome, Italy Correspondence: luigi.degennaro@uniroma1.it; Tel.: +39-06-49917647; Fax: +39-06-49917711 Received: 26 June 2019; Accepted: 27 September 2019; Published: 29 September 2019 Abstract: Sleep significantly changes across the lifespan, and several studies underline its crucial role in cognitive functioning. Similarly, mental activity during sleep tends to covary with age. This review aims to analyze the characteristics of dreaming and disturbing dreams at different age brackets. On the one hand, dreams may be considered an expression of brain maturation and cognitive development, showing relations with memory and visuo-spatial abilities. Some investigations reveal that specific electrophysiological patterns, such as frontal theta oscillations, underlie dreams during sleep, as well as episodic memories in the waking state, both in young and older adults. On the other hand, considering the role of dreaming in emotional processing and regulation, the available literature suggests that mental sleep activity could have a beneficial role when stressful events occur at different age ranges. We highlight that nightmares and bad dreams might represent an attempt to cope the adverse events, and the degrees of cognitive-brain maturation could impact on these mechanisms across the lifespan. Future investigations are necessary to clarify these relations. Clinical protocols could be designed to improve cognitive functioning and emotional regulation by modifying the dream contents or the ability to recall/non-recall them. Keywords: dreaming; lifespan; sleep; cognition; children; young adults; elderly; nightmares; PTSD 1. Introduction In the last decade, studies on mental sleep activity have shown remarkable advances. Dream experience has been considered an expression of consciousness during sleep [1], although the detection of the specific instant in which mental activity is produced could be challenging. As is well known, dream research is characterized by a notable limitation: the existence of a temporal gap between dream generation and the moment in which the dream is reported. In the attempt to overcome this “asynchrony”, some authors have used the eye-signaling technique, i.e., pre-decided sequences of intentional eye movements during dreaming [2–4], to reveal the exact moment of dream production. However, while this method is successfully applied to lucid dreams, it is not applicable to the “traditional” mental sleep activity. The access to dream contents is mainly obtained from the information reported by subjects after awakening. Furthermore, multiple variables affect the possibility of obtaining a dream recall, such as the method of collection, the sleep stage upon which subjects are awakened, and the macrostructural and microstructural features of the sleep interval before dream recall (for a review, see [5]). One of the best-established theories on dreaming is the “continuity hypothesis”, firstly proposed by Hall and Norby [6]. The authors hypothesized that thoughts, behaviors, fantasies, and emotions Int. J. Environ. Res. Public Health 2019, 16, 3658; doi:10.3390/ijerph16193658 www.mdpi.com/journal/ijerph Int. J. Environ. Res. Public Health 2019, 16, 3658 2 of 23 experienced during the waking state may have their continuity in sleep. Several investigations provided empirical support for this hypothesis [7–10]. In particular, some results underlined that specific neurobiological circuits are responsible for both cognitive and emotional experiences during the waking state as well as mental sleep activity. Hence, the dysregulation of these mechanisms can affect both daytime and dream experience (for a review, see [11]). In this view, the observations by Solms [12,13] suggested that specific brain injuries affect some cognitive functions during dream imagery as much as wakefulness. For instance, “visual anoneria” was related to lesions in the visual associative cortex (ventromesial occipito-parietal cortex) and produced dream imagery with a total or partial drop in the production of visual contents. In parallel, this condition is associated with compromised visuo-spatial skills and the ability to produce mental imagery during wakefulness [13]. Another condition described by Solms [13] is “anoneirognosis”, characterized by the inability to discern dream from reality, due to lesions over medial prefrontal cortex, anterior cingulate cortex, or basal forebrain. In these patients, a general state of confusion during the waking state and dream contents can intrude into their waking thoughts [9]. Behind the relation with cognitive functioning, it should be underlined that several regions involved in emotional regulation during wakefulness are also activated during rapid eye movement, (REM) episodes associated with dream recall [14]. In particular, the limbic system and the reward dopaminergic system activation associated with dream experience during REM sleep can promote emotional processing and learning [15,16]. Recent neuroimaging findings point in this direction, showing that microstructural measures of specific limbic areas were related to qualitative and quantitative features of dream reports [15–18]. Moreover, subjects with high dream recall frequency showed greater regional cerebral blood flow (rCBF) than low recallers in the temporo-parietal junction (TPJ) during REM sleep, stage 3 NREM sleep, and wakefulness, and in the medial prefrontal cortex (mPFC) during REM sleep [19]. Both TPJ and mPFC have a crucial role in emotional and cognitive processing during wakefulness (for a review, see [20]). Specifically, the TPJ is involved in the theory of mind, empathy, and social cognition during the waking state, while the mPFC is related to awareness, introspection, attention, and identification of emotions [20]. This neurobiological evidence substantially supports the notion that some neural substrates are shared between waking emotional/cognitive functioning and dreaming. However, findings addressing how these mechanisms change across the lifespan are still lacking. Another issue concerns the role of dreaming in specific disorder, such as post-traumatic stress disorder (PTSD) and idiopathic nightmares, where dreams are abundant and contents are frequently emotional and/or bizarre (for a review, see [11]). It is still unclear whether dreams only reflect the alterations related to these disturbances or play a particular role in these pathological conditions at different ages of life. The current review aims to provide a comprehensive overview of these issues, including, for each age bracket, a summary of the micro- and macrostructural characteristics of sleep, the dream features, and the available findings on disturbing dreams. We have focused our review on nightmares and PTSD, in which the alterations of the mental sleep activity are relevant. We considered the following age ranges: (a) children and early adolescence (29 months to 16 years); (b) young adults (18–47 years, but individuals up to 60 years were part of the clinical sample in some studies (e.g., [21]); (c) older adults (50–94 years). 2. Dreaming Across the Lifespan 2.1. Children 2.1.1. Sleep Pattern Development and Cortical Maturation Sleeping could be seen as the main activity of a neonate in the first period of life. Since the first hours after the birth, sleep in newborns shows two different states with distinct behavioral and cortical activity patterns: active sleep (AS), representing the antecedent of REM sleep, characterized by rapid eyes movements, a quite stable electroencephalographic (EEG) background of mixed rapid, low amplitude Int. J. Environ. Res. Public Health 2019, 16, 3658 3 of 23 theta and alpha activity, and mainly synchronous occipital delta activity, and irregular heart rate and respiration, associated to facial and head movements [22–24]; and quiet sleep (QS), antecedent of the non-REM (NREM) sleep, with high amplitude, mixed frequency EEG, and tracé alternant EEG activity, associated with a regular cardiorespiratory pattern and few body movements [22–24]. During the first weeks of life, signs of AS and QS could occur simultaneously, during the so-called indeterminate-sleep (IS) that progressively disappears [25], pointing to the stabilization of the sleep controlling processes. In newborns, the sleep period starts with active sleep, while the entrance into the sleep cycle through NREM sleep begins at 3–6 months. The first months of life represent a critical period for brain development. The maturational trajectory of cortical areas sees the primary sensory-motor cortices developing first, and then it gradually shifts anteriorly and laterally, involving areas linked to more complex associative functions [26]. The maturation of the central nervous system is paralleled by the QS and AS stabilization and the gradual development of features characterizing the mature NREM and REM sleep, respectively. The first sign of this sleep maturation is represented by the appearance, at two months of age, of the first sleep spindles during the QS/NREM sleep, whose occurrence reaches a peak during the second half of the first years of age and then declines [27,28]. Sleep spindles are phasic events within the sigma frequency band (11–15 Hz) generated within the thalamo-cortical system [29]. A boost in spindle density [27,28] could be related to functional changes during this period occurring within the thalamo-cortical circuit. Spindle activity is involved in long-term memory consolidation [30,31] and cognitive abilities [32]. Accordingly, the developmental evolution of spindles might represent an index of maturation of the thalamo-cortical network as well as of the cognitive functions related to its functioning. At about six months, the k-complexes, phasic events with high amplitude and low frequency