The reason sleep deprivation alters emotional reactivity

Losing Neutrality: The Neural Basis of Impaired Emotional Control without Sleep.
Simon EB, Oren N, Sharon H, Kirschner A, Goldway N, Okon-Singer H, Tauman R, Deweese MM, Keil A, Hendler T.
Journal of Neurosci. 2015 Sep 23;35(38):13194-205. 

Sleep deprivation has been shown recently to alter emotional processing possibly associated with reduced frontal regulation. Such impairments can ultimately fail adaptive attempts to regulate emotional processing (also known as cognitive control of emotion), although this hypothesis has not been examined directly. Therefore, we explored the influence of sleep deprivation on the human brain using two different cognitive-emotional tasks, recorded using fMRI and EEG. Both tasks involved irrelevant emotional and neutral distractors presented during a competing cognitive challenge, thus creating a continuous demand for regulating emotional processing. Results reveal that, although participants showed enhanced limbic and electrophysiological reactions to emotional distractors regardless of their sleep state, they were specifically unable to ignore neutral distracting information after sleep deprivation. As a consequence, sleep deprivation resulted in similar processing of neutral and negative distractors, thus disabling accurate emotional discrimination. As expected, these findings were further associated with a decrease in prefrontal connectivity patterns in both EEG and fMRI signals, reflecting a profound decline in cognitive control of emotion. Notably, such a decline was associated with lower REM sleep amounts, supporting a role for REM sleep in overnight emotional processing. Altogether, our findings suggest that losing sleep alters emotional reactivity by lowering the threshold for emotional activation, leading to a maladaptive loss of emotional neutrality.

REM sleep and memory processing

The role of rapid eye movement sleep for amygdala-related memory processing.
Genzel L, Spoormaker V, Konrad BN, Dresler M.
Neurobiol Learn Mem. 2015 Jan 28.

Over the years, rapid eye movement (REM) sleep has been associated with general memory consolidation, specific consolidation of perceptual, procedural, emotional and fear memories, brain maturation and preparation of waking consciousness. More recently, some of these associations (e.g. general and procedural memory consolidation) have been shown to be unlikely, while others (e.g. brain maturation and consciousness) remain inconclusive. In this review, we argue that both behavioral and neurophysiological evidence supports a role of REM sleep for amygdala-related memory processing: the amygdala-hippocampus-medial prefrontal cortex network involved in emotional processing, fear memory and valence consolidation shows strongest activity during REM sleep, in contrast to the hippocampus-medial prefrontal cortex only network which is more active during non-REM sleep. However, more research is needed to fully understand the mechanisms.

Lucidity and consciousness in dreams

Measuring consciousness in dreams: The lucidity and consciousness in dreams scale
Ursula Vossa, Karin Schermelleh-Engela, Jennifer Windtc, Clemens Frenzeld, Allan Hobsone
Consciousness and Cognition, Volume 22, Issue 1, March 2013, Pages 8–21 

Both lucid and non-lucid dreams are an important contrast condition for theories of waking consciousness, giving valuable insights into the structure of conscious experience and its neural correlates during sleep. However, the precise differences between lucid and non-lucid dreams remain poorly understood. The construction of the Lucidity and Consciousness in Dreams scale (LuCiD) was based on theoretical considerations and empirical observations. Exploratory factor analysis of the data from the first survey identified eight factors that were validated in a second survey using confirmatory factor analysis: INSIGHT, CONTROL, THOUGHT, REALISM, MEMORY, DISSOCIATION, NEGATIVE EMOTION, and POSITIVE EMOTION. While all factors are involved in dream consciousness, realism and negative emotion do not differentiate between lucid and non-lucid dreams, suggesting that lucid insight is separable from both bizarreness in dreams and a change in the subjectively experienced realism of the dream.

REM sleep necessary for emotional memory consolidation

The role of REM sleep in the processing of emotional memories: Evidence from behavior and event-related potentials
S. Groch, I. Wilhelm, S. Diekelmann, J. Born
Neurobiology of Learning and Memory, Volume 99, January 2013, Pages 1–9

Emotional memories are vividly remembered for the long-term. Rapid eye movement (REM) sleep has been repeatedly proposed to support the superior retention of emotional memories. However, its exact contribution and, specifically, whether its effect is mainly on the consolidation of the contents or the processing of the affective component of emotional memories is not clear. Here, we investigated the effects of sleep rich in slow wave sleep (SWS) or REM sleep on the consolidation of emotional pictures and the accompanying changes in affective tone, using event-related potentials (ERPs) together with subjective ratings of valence and arousal. Sixteen healthy, young men learned 50 negative and 50 neutral pictures before 3-h retention sleep intervals that were filled with either SWS-rich early or REM sleep-rich late nocturnal sleep. In accordance with our hypothesis, recognition was better for emotional pictures than neutral pictures after REM compared to SWS-rich sleep. This emotional enhancement after REM-rich sleep expressed itself in an increased late positive potential of the ERP over the frontal cortex 300–500 ms after stimulus onset for correctly classified old emotional pictures compared with new emotional and neutral pictures. Valence and arousal ratings of emotional pictures were not differentially affected by REM or SWS-rich sleep after learning. Our results corroborate that REM sleep contributes to the consolidation of emotional contents in memory, but suggest that the affective tone is preserved rather than reduced by the processing of emotional memories during REM sleep.

Sleep enhances emotional memories, preserves emotional intensity

Processing of emotional reactivity and emotional memory over sleep.
Baran B, Pace-Schott EF, Ericson C, Spencer RM.
Journal of Neuroscience. 2012 Jan 18;32(3):1035-42. 

Sleep enhances memories, particularly emotional memories. As such, it has been suggested that sleep deprivation may reduce posttraumatic stress disorder. This presumes that emotional memory consolidation is paralleled by a reduction in emotional reactivity, an association that has not yet been examined. In the present experiment, we used an incidental memory task in humans and obtained valence and arousal ratings during two sessions separated either by 12 h of daytime wake or 12 h including overnight sleep. Recognition accuracy was greater following sleep relative to wake for both negative and neutral pictures. While emotional reactivity to negative pictures was greatly reduced over wake, the negative emotional response was relatively preserved over sleep. Moreover, protection of emotional reactivity was associated with greater time in REM sleep. Recognition accuracy, however, was not associated with REM. Thus, we provide the first evidence that sleep enhances emotional memory while preserving emotional reactivity.

Neuropsychology of dreams

Rev Neurol. 2012 Jul 16;55(2):101-10. 
Tirapu-Ustarroz J.

Dreams are a universal human experience and studying them from the point of view of neuroscience, consciousness, emotions and cognition is quite a challenge for researchers. Thus, dreams have been addressed from a number of different perspectives ranging from philosophy to clinical medicine, as well as psychiatry, psychology, artificial intelligence, neural network models, psychophysiology or neurobiology.

The main models are grounded on the biological function of dreams, especially those based on processes involving the consolidation of memory and forgetting, and models of simulation. Similarly, current models are developed upon the neurobiology and the neuropsychology of the REM phases of sleep and how they are differentiated from wakefulness. Thus, neurobiologically speaking, dreams are related to the role of acetylcholine and, neuropsychologically, to the activation of the limbic and paralimbic regions, the activation of the basal ganglia, the activation of cortical areas with a specific modality (especially Brodmann's areas 19, 22 and 37) and the deactivation of the ventromedial, parietal and dorsolateral prefrontal cortex and posterior cingulate.

Dreams can be considered a state of consciousness that is characterised by a reduced control over their content, visual images and activation of the memory, and which is mediated by motivational incentives and emotional salience.

Sleep depotentiates prior emotional experiences/painful memories

REM Sleep Depotentiates Amygdala Activity to Previous Emotional Experiences
Current Biology, 23 November 2011 (Link)
Els van der Helm, Justin Yao, Shubir Dutt, Vikram Rao, Jared M. Saletin, Matthew P. Walker

Highlights:

• Sleep decreases amygdala activity to prior waking emotional experiences 
• The amygdala decrease is associated with reestablished prefrontal connectivity 
• These neural changes are accompanied by overnight reductions in subjective reactivity 
• Reductions in both brain and behavioral reactivity are associated with REM physiology 

Summary: Clinical evidence suggests a potentially causal interaction between sleep and affective brain function; nearly all mood disorders display co-occurring sleep abnormalities, commonly involving rapid-eye movement (REM) sleep. Building on this clinical evidence, recent neurobiological frameworks have hypothesized a benefit of REM sleep in palliatively decreasing next-day brain reactivity to recent waking emotional experiences. Specifically, the marked suppression of central adrenergic neurotransmitters during REM (commonly implicated in arousal and stress), coupled with activation in amygdala-hippocampal networks that encode salient events, is proposed to (re)process and depotentiate previous affective experiences, decreasing their emotional intensity. In contrast, the failure of such adrenergic reduction during REM sleep has been described in anxiety disorders, indexed by persistent high-frequency electroencephalographic (EEG) activity; a candidate factor contributing to hyperarousal and exaggerated amygdala reactivity. Despite these neurobiological frameworks, and their predictions, the proposed benefit of REM sleep physiology in depotentiating neural and behavioral responsivity to prior emotional events remains unknown. Here, we demonstrate that REM sleep physiology is associated with an overnight dissipation of amygdala activity in response to previous emotional experiences, altering functional connectivity and reducing next-day subjective emotionality.

The memory function of sleep

Nature Reviews Neuroscience 11, 114-126 (February 2010) 
Susanne Diekelmann & Jan Born

Sleep has been identified as a state that optimizes the consolidation of newly acquired information in memory, depending on the specific conditions of learning and the timing of sleep. Consolidation during sleep promotes both quantitative and qualitative changes of memory representations. Through specific patterns of neuromodulatory activity and electric field potential oscillations, slow-wave sleep (SWS) and rapid eye movement (REM) sleep support system consolidation and synaptic consolidation, respectively. During SWS, slow oscillations, spindles and ripples - at minimum cholinergic activity - coordinate the re-activation and redistribution of hippocampus-dependent memories to neocortical sites, whereas during REM sleep, local increases in plasticity-related immediate-early gene activity - at high cholinergic and theta activity - might favour the subsequent synaptic consolidation of memories in the cortex.

A theory of protoconsciousness

REM sleep and dreaming: towards a theory of protoconsciousness
Nature Reviews| Neuroscience volume 10 | November 2009 | 803
J. Allan Hobson

Dreaming has fascinated and mystified humankind for ages: the bizarre and evanescent qualities of dreams have invited boundless speculation about their origin, meaning and purpose. For most of the twentieth century, scientific dream theories were mainly psychological. Since the discovery of rapid eye movement (REM) sleep, the neural underpinnings of dreaming have become increasingly well understood, and it is now possible to complement the details of these brain mechanisms with a theory of consciousness that is derived from the study of dreaming. The theory advanced here emphasizes data that suggest that REM sleep may constitute a protoconscious state, providing a virtual reality model of the world that is of functional use to the development and maintenance of waking consciousness.

The Role of Sleep in Emotional Brain Processing

Cognitive neuroscience continues to build meaningful connections between affective behavior and human brain function. Within the biological sciences, a similar renaissance has taken place, focusing on the role of sleep in various neurocognitive processes and, most recently, on the interaction between sleep and emotional regulation. This review surveys an array of diverse findings across basic and clinical research domains, resulting in a convergent view of sleep-dependent emotional brain processing. On the basis of the unique neurobiology of sleep, the authors outline a model describing the overnight modulation of affective neural systems and the (re)processing of recent emotional experiences, both of which appear to redress the appropriate next-day reactivity of limbic and associated autonomic networks. Furthermore, a rapid eye movement (REM) sleep hypothesis of emotional-memory processing is proposed, the implications of which may provide brain-based insights into the association between sleep abnormalities and the initiation and maintenance of mood disturbances.

2-stage models of sleep and memory

Evidence for 2-stage models of sleep and memory: Learning-dependent changes in spindles and theta in rats
Stuart M. Fogel, Carlyle T. Smithb, Richard J. Beninger
Brain Research Bulletin 79 (2009) 445–451

What processes are involved in the formation of enduring memory traces? Sleep has been proposed to play a role in memory consolidation and the present study provides evidence to support 2-stage models of sleep and memory including both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Previous research has shown REM sleep increases following avoidance learning and memory is impaired if REM deprivation occurs during these post-training periods indicating that REM sleep may have a role in memory consolidation processes. These discrete post-training periods have been termed REM sleep windows (RSWs). It is not known whether the electroencephalogram has unique characteristics during the RSW. Further investigation of the RSW was one of the primary goals of this study. We investigated the epidural-recorded electrophysiological learning-related changes following avoidance training in rats. Theta power increased in the learning group during the RSW, suggesting that theta is involved in memory consolidation during this period. Sleep spindles subsequently increased in slow wave sleep (SWS). The results suggest that both NREM and REM sleep are involved in sleep-dependent memory consolidation, and provide support for existing 2-stage models. Perhaps first theta increases to organize and consolidate material via hippocampal–neocortical dialogue, followed by subsequent refinement in the cortex by spindles during SWS.

Hippocampal theta oscillations are traveling waves

Hippocampal theta oscillations are traveling waves.
Lubenov EV, Siapas AG
Nature 2009;459(7246):534-9.

Theta oscillations clock hippocampal activity during awake behaviour and rapid eye movement (REM) sleep. These oscillations are prominent in the local field potential, and they also reflect the subthreshold membrane potential and strongly modulate the spiking of hippocampal neurons. The prevailing view is that theta oscillations are synchronized throughout the hippocampus, despite the lack of conclusive experimental evidence. In contrast, here we show that in freely behaving rats, theta oscillations in area CA1 are travelling waves that propagate roughly along the septotemporal axis of the hippocampus. Furthermore, we find that spiking in the CA1 pyramidal cell layer is modulated in a consistent travelling wave pattern. Our results demonstrate that theta oscillations pattern hippocampal activity not only in time, but also across anatomical space. The presence of travelling waves indicates that the instantaneous output of the hippocampus is topographically organized and represents a segment, rather than a point, of physical space.

Improve creativity while sleeping / dreaming

REM, not incubation, improves creativity by priming associative networks
www.pnas.org/cgi/doi/10.1073/pnas.0900271106
Denise J. Cai, Sarnoff A. Mednick, Elizabeth M. Harrison, Jennifer C. Kanady, and Sara C. Mednick

The hypothesized role of rapid eye movement (REM) sleep, which is rich in dreams, in the formation of new associations, has remained anecdotal. We examined the role of REM on creative problem solving, with the Remote Associates Test (RAT). Using a nap paradigm, we manipulated various conditions of prior exposure to elements of a creative problem. Compared with quiet rest and non-REM sleep, REM enhanced the formation of associative networks and the integration of unassociated information. Furthermore, these REM sleep benefits were not the result of an improved memory for the primed items. This study shows that compared with quiet rest and non-REM sleep, REM enhances the integration of unassociated information for creative problem solving, a process, we hypothesize, that is facilitated by cholinergic and noradrenergic neuromodulation during REM sleep.

Act out your dreams

Neurology. 2009 Feb 10;72(6):551-7.
Oudiette D, De Cock VC, Lavault S, Leu S, Vidailhet M, Arnulf I.

OBJECTIVE: To document unusual, nonviolent behaviors during REM sleep behavior disorder (RBD) and evaluate their frequency in Parkinson disease (PD).

BACKGROUND: Most behaviors previously described during RBD mimic attacks, suggesting they proceed from archaic defense generators in the brainstem. Feeding, drinking, sexual behaviors, urination, and defecation have not been documented yet in RBD.

METHODS: We collected 24 cases of nonviolent behaviors during idiopathic and symptomatic RBD (narcolepsy, dementia with Lewy bodies, PD), reported or observed in videopolysomnography. The frequency of violent and nonviolent behaviors during RBD was evaluated by face to face interview of patients and their cosleepers in a prospective series of 100 patients with PD.

RESULTS: Incidental cases of nonviolent behaviors during RBD included masturbating-like behavior and coitus-like pelvic thrusting, mimicking eating and drinking, urinating and defecating, displaying pleasant behaviors (laughing, singing, dancing, whistling, smoking a fictive cigarette, clapping and gesturing "thumbs up"), greeting, flying, building a stair, dealing textiles, inspecting the army, searching a treasure, and giving lessons. Speeches were mumbled or contained logical sentences with normal prosody. In PD with RBD (n = 60), 18% of patients displayed nonviolent behaviors. In this series (but not in incidental cases), all RBD patients with nonviolent behaviors also showed violent behaviors.

CONCLUSIONS: Although they are less frequent than violent behaviors, nonviolent behaviors during REM sleep behavior disorder (RBD) fill a large spectrum including learned speeches and culture-specific behaviors, suggesting they proceed from the cortex activation. Sexual behaviors during RBD may expose patients and cosleepers to forensic consequences.

Human Emotional Memory

REM Sleep, Prefrontal Theta, and the Consolidation of Human Emotional Memory
Cerebral Cortex May 2009;19:1158--1166
Masaki Nishida, Jori Pearsall, Randy L. Buckner and Matthew P. Walker

Both emotion and sleep are independently known to modulate declarative memory. Memory can be facilitated by emotion, leading to enhanced consolidation across increasing time delays. Sleep also facilitates offline memory processing, resulting in superior recall the next day. Here we explore whether rapid eye movement (REM) sleep, and aspects of its unique neurophysiology, underlie these convergent influences on memory. Using a nap paradigm, we measured the consolidation of neutral and negative emotional memories, and the association with REM-sleep electrophysiology. Subjects that napped showed a consolidation benefit for emotional but not neutral memories. The No-Nap control group showed no evidence of a consolidation benefit for either memory type. Within the Nap group, the extent of emotional memory facilitation was significantly correlated with the amount of REM sleep and also with right-dominant prefrontal theta power during REM. Together, these data support the role of REM-sleep neurobiology in the consolidation of emotional human memories, findings that have direct translational implications for affective psychiatric and mood disorders.