**5. Sleep and psychological functions**

Herein, we will review existing data about sleep's role in functions different from the above described memory and cognitive ones. These include consolidation of affect, emotional regulation and dreaming mental states. As will be shown, the mechanisms, trough which sleep serves these psychological processes are distinctly different from those involved in its memory and cognitive functions. It is to be emphasized, however, that mostly REM sleep has been so far consistently and reliably associated with these human psychological processes. REM sleep characteristics are implicated for both normal psychological processes and psychopathology. Thus, REM sleep and its mental content incorporated in the cooccurring dreaming production have been proposed to aid resolution of personal emotional, affective and social conflicts (Cartwright et al., 2006; McNamara et al., 2001; 2005; 2010). Notably, REM sleep mechanisms and mental signatures have also been proposed to be involved in the pathogenesis of a number of psychopathological conditions, including posttraumatic stress disorder, anxiety, depression, schizophrenia, etc. (Benca et al., 1992; Gottesmann, 2010; Kirov & Brand, in press; Wagner et al., 2006; Walker, 2009; Walker & van der Helm, 2009). These observations are conceptualized in the so-called continuity hypothesis, according to which cognitive and emotional experiences generated, developed and used during wakefulness do continue to evolve during dreaming in REM sleep (Dumhoff & Hall, 1996; Pesant & Zadra, 2006). A recent study tested this hypothesis in both congenitally paraplegic and deaf-mute persons and matched controls. Surprisingly, perceptual representations, even of modalities not experienced during wakefulness, were quite common in dream reports not only in the control persons but also in the handicapped subjects (Voss et al., 2011). These interesting results give support to a protoconsciousness theory of REM sleep dreaming state that was recently forwarded by Hobson (2009). The REM sleep-dream protoconsciousness hypothesis proposes that development and maintenance of waking consciousness and other high-order brain functions (secondary consciousness) depends on brain activation during REM sleep (primary consciousness, i.e., simple awareness that includes perception and emotion in sleep), thus implicating for phylogenic aspects of dreaming. Accordingly, the neurobiology of REM sleep and cooccurring dreaming mentality reflect more basic (i.e., threaten, feeding, sexual, etc.) features not only in humans but also in lower species (Hobson, 2009). Interestingly, this view seems to have much in common with a previously proposed hypothesis about the psychological functions of REM sleep as an interactive genetic programming brain state (Jouvet, 1998). These two views (Hobson, 2009; Jouvet, 1998) predict that human experience during wakefulness is given more basic biological characteristics during REM sleep, which may have important adaptation roles. Also, they well fit with a more recent opinion about the memory functions of REM sleep, according to which memories consolidated during SWS undergo further transformation during REM sleep in terms of placing them in a more general and individually specific context (Walker & Stickgold, 2010).

### **5.1 Overview of human EEG data**

168 Neuroimaging – Cognitive and Clinical Neuroscience

with the magnitude of an SD-driven increase in ventromedial prefrontal activation as well as by an SD-driven decrease in anterior insula activation during decision making

Regarding the above described neuroimaging findings together, it can be concluded that sleep is of critical importance for almost all, if not for all types of cognitive processes, including decision making. However, which mechanisms are responsible for substantial

Herein, we will review existing data about sleep's role in functions different from the above described memory and cognitive ones. These include consolidation of affect, emotional regulation and dreaming mental states. As will be shown, the mechanisms, trough which sleep serves these psychological processes are distinctly different from those involved in its memory and cognitive functions. It is to be emphasized, however, that mostly REM sleep has been so far consistently and reliably associated with these human psychological processes. REM sleep characteristics are implicated for both normal psychological processes and psychopathology. Thus, REM sleep and its mental content incorporated in the cooccurring dreaming production have been proposed to aid resolution of personal emotional, affective and social conflicts (Cartwright et al., 2006; McNamara et al., 2001; 2005; 2010). Notably, REM sleep mechanisms and mental signatures have also been proposed to be involved in the pathogenesis of a number of psychopathological conditions, including posttraumatic stress disorder, anxiety, depression, schizophrenia, etc. (Benca et al., 1992; Gottesmann, 2010; Kirov & Brand, in press; Wagner et al., 2006; Walker, 2009; Walker & van der Helm, 2009). These observations are conceptualized in the so-called continuity hypothesis, according to which cognitive and emotional experiences generated, developed and used during wakefulness do continue to evolve during dreaming in REM sleep (Dumhoff & Hall, 1996; Pesant & Zadra, 2006). A recent study tested this hypothesis in both congenitally paraplegic and deaf-mute persons and matched controls. Surprisingly, perceptual representations, even of modalities not experienced during wakefulness, were quite common in dream reports not only in the control persons but also in the handicapped subjects (Voss et al., 2011). These interesting results give support to a protoconsciousness theory of REM sleep dreaming state that was recently forwarded by Hobson (2009). The REM sleep-dream protoconsciousness hypothesis proposes that development and maintenance of waking consciousness and other high-order brain functions (secondary consciousness) depends on brain activation during REM sleep (primary consciousness, i.e., simple awareness that includes perception and emotion in sleep), thus implicating for phylogenic aspects of dreaming. Accordingly, the neurobiology of REM sleep and cooccurring dreaming mentality reflect more basic (i.e., threaten, feeding, sexual, etc.) features not only in humans but also in lower species (Hobson, 2009). Interestingly, this view seems to have much in common with a previously proposed hypothesis about the psychological functions of REM sleep as an interactive genetic programming brain state (Jouvet, 1998). These two views (Hobson, 2009; Jouvet, 1998) predict that human experience during wakefulness is given more basic biological characteristics during REM sleep, which may have important adaptation roles. Also, they well fit with a more recent opinion about the memory functions of REM sleep, according to which memories consolidated during SWS undergo further transformation during REM sleep in terms of placing them in a more

deficits of the many cognitive functions seen after sleep deprivation is still elusive.

general and individually specific context (Walker & Stickgold, 2010).

(Venkatraman et al., 2011).

**5. Sleep and psychological functions** 

Notably, human REM sleep has been so far shown to consolidate declarative (episodic or semantic) memory only when items have emotional salient components, and only when these emotional components have negative valence (Wagner et al., 2001; 2006; Nishida et al., 2009). Recently, REM sleep was shown to be very important for recalibration of the sensitivity of human brain to specific emotions (Gujar et al., 2011a).

Data concerning human sleep EEG findings about the role of REM sleep in psychological functioning are still scarce. One study investigated the effect REM sleep portion of a daily nap on episodic memory consolidation. No memorizing effects on emotionally neutral factbased information were found. However, when episodic items were associated with negative emotional components, REM sleep strongly consolidated them. Moreover, the improvement strongly and positively correlated with all, REM sleep latency, amount of REM sleep, and importantly, with the theta (4-8 Hz) REM sleep EEG signature (Nishida et al., 2009). A more recent study tested whether boosting REM sleep EEG signatures could produce overnight improvement of memory consolidation. In this study, REM sleep EEG was potentiated by delivering theta (5 Hz) anodal trans-cranial direct current stimulation during REM sleep periods in the second half of night. The stimulation did enhanced gamma (25-45 Hz) EEG activity during REM sleep, but it did not improve either declarative or procedural memory consolidation at morning recalls. Instead, this increase in gamma EEG during REM sleep resulted in a worsened mood, as assessed by positive and negative affect scale, in the morning after sleep, accompanied by worsening on working memory, as assessed by a word fluency test (Marshall et al., 2011). Collectively, these studies demonstrate that specific REM sleep EEG rhythms are involved in affective behavior.

Interestingly, a recent study demonstrated the EEG signatures of dream recall from both REM sleep (theta, 5-7 Hz EEG activity) and stage 2 of non-REM sleep (alpha, 8-12 Hz EEG activity) (Marzano et al., 2011). These findings document different modes of mentality in REM sleep versus non-REM sleep. Furthermore, they suggest that the neurophysiological mechanisms underlying encoding and recall of episodic memories may remain the same across different states of consciousness.

#### **5.2 Overview of human neuroimaging data**

The existing so far human neuroimaging studies about the role for sleep in emotional regulation demonstrate deteriorated patterns of brain activation after total sleep deprivation (SD). By using fMRI, it has been shown that a disconnection between medial prefrontal cortex and amygdala following SD has been associated with improper response to negative emotional stimuli (Yoo et al., 2007a). Further, Sterpenich et al. (2007) showed that a successful recollection of emotional stimuli elicited larger BOLD responses in the hippocampus and various cortical areas, including the medial prefrontal cortex, in a sleep control (SC) group than in a sleep deprived (SD) group. In contrast, the recollection of negative items elicited larger responses in the amygdala and in occipital areas in the SD relative to the SC group (Sterpenich et al., 2007). A later fMRI study examined the effect of a single night SD on consolidation of aversive emotional stimuli and corresponding patterns of brain activation at retest that took place six months after encoding. At retest 6 months later, the recollection of subjects allowed to sleep, compared with SD subjects, was associated with significantly larger fMRI responses in the ventral medial prefrontal cortex (vMPFC) and precuneus, areas involved in memory retrieval, and in the extended amygdala and occipital cortex, areas involved in emotion modulation at encoding. These results

The Memory, Cognitive and Psychological Functions of Sleep:

Drs. J. Yordanova and V. Kolev for their support.

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**7. Acknowledgment** 

697-704.

669-670.

204.

279(5347):91-95.

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and Schwarzenberg, Baltimore.

*Journal of Biological Rhythms*, 14(6):557-568.

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Finally, it can be concluded that the mechanisms underpinning memory, cognitive and psychological functions of sleep substantially contribute to human intelligence. Further

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investigation of the relationship between sleep and intelligence is clearly warranted.

suggest that sleep during the first postencoding night profoundly influences long-term systems-level consolidation of emotional memory and modifies the functional segregation and integration associated with recollection of affective memories in the long term (Sterpenich et al., 2009). Finally, using fMRI, it was recently demonstrated that SD amplifies reactivity throughout human mesolimbic reward brain networks in response to pleasureevoking stimuli. In addition, this amplified reactivity was associated with enhanced connectivity in the early primary visual processing pathways and extended limbic regions, yet with a reduction in coupling with medial frontal and orbitofrontal regions. These neural changes were accompanied by a biased increase in the number of emotional stimuli judged as pleasant in the sleep-deprived group, the extent of which exclusively correlated with activity in mesolimbic regions (Gujar et al., 2011b). These results may offer a neural foundation on which to consider interactions between sleep loss and emotional reactivity in a variety of mood disorders (Gujar et al., 2011b).

Collectively, the above findings demonstrate sleep-related mechanisms of emotional regulation and consolidation of affective memories that partially differ from those shown to be involved in emotionally neutral memory consolidation and in the cognitive functions of sleep. The emotional "fingerprint" seems to involve mostly connections between prefrontal cortices and amygdala. However, it still remains to be revealed which sleep portions or sleep stages might have contributed to the impaired brain activation patterns after SD responsible for the behavioral results.
