From physiological awakening to pathological sleep inertia: Neurophysiological and behavioural characteristics of the sleep-to-wake transition.

Sleep inertia refers to the transient physiological state of hypoarousal upon awakening, associated with various degrees of impaired neurobehavioral performance, confusion, a desire to return to sleep and often a negative emotional state. Scalp and intracranial electro-encephalography as well as functional imaging studies have provided evidence that the sleep inertia phenomenon is underpinned by an heterogenous cerebral state mixing local sleep and local wake patterns of activity, at the neuronal and network levels. Sleep inertia is modulated by homeostasis and circadian processes, sleep stage upon awakening, and individual factors; this translates into a huge variability in its intensity even under physiological conditions. In sleep disorders, especially in hypersomnolence disorders such as idiopathic hypersomnia, sleep inertia may be a daily, serious and long-lasting symptom leading to severe impairment. To date, few tools have been developed to assess sleep inertia in clinical practice. They include mainly questionnaires and behavioral tests such as the psychomotor vigilance task. Only one neurophysiological protocol has been evaluated in hypersomnia, the forced awakening test which is based on an event-related potentials paradigm upon awakening. This contrasts with the major functional consequences of sleep inertia and its potentially dangerous consequences in subjects required to perform safety-critical tasks soon after awakening. There is a great need to identify reproducible biomarkers correlated with sleep inertia-associated cognitive and behavioral impairment. These biomarkers will aim at better understanding and measuring sleep inertia in physiological and pathological conditions, as well as objectively evaluating wake-promoting treatments or non-pharmacological countermeasures to reduce this phenomenon.

Infraclinical detection of voluntary attention in coma and post-coma patients using electrophysiology.

OBJECTIVE: Early functional evaluation and prognosis of patients with disorders of consciousness is a major challenge that clinical assessments alone cannot solve. Objective measures of brain activity could help resolve this uncertainty. We used electroencephalogram at bedside to detect voluntary attention with a paradigm previously validated in healthy subjects. METHODS: Using auditory-oddball sequences, our approach rests on detecting known attentional modulations of Event Related Potentials that reflect compliance with verbal instructions. Sixty-eight unresponsive patients were tested in their first year after coma onset (37 coma and 31 first year post-coma patients). Their evolution 6 months after the test was considered. RESULTS: Fourteen of the 68 patients, showed a positive response. Nine were in a coma and 5 in a minimally conscious state (MCS). Except for one who died early, all responders evolved to exit-MCS within 6 months (93%), while 35 (65%) among non-responders only. CONCLUSIONS: Among those patients for whom the outcome is highly uncertain, 21% responded positively to this simple but cognitively demanding test. Strikingly, some coma patients were among responders. SIGNIFICANCE: The proposed paradigm revealed cognitive-motor dissociation in some coma patients. This ability to sustain attention on demand predicted awakening within 6 months and represents an immediately useful information for relatives and caregivers.

High Dream Recall Frequency is Associated with Increased Creativity and Default Mode Network Connectivity.

INTRODUCTION: Several results suggest that the frequency of dream recall is positively correlated with personality traits such as creativity and openness to experience. In addition, neuroimaging results have evidenced different neurophysiological profiles in high dream recallers (HR) and low dream recallers (LR) during both sleep and wakefulness, specifically within regions of the default mode network (DMN). These findings are consistent with the emerging view that dreaming and mind wandering pertain to the same family of spontaneous mental processes, subserved by the DMN. METHODS: To further test this hypothesis, we measured the DMN functional connectivity during resting wakefulness, together with personality and cognitive abilities (including creativity) in 28 HR and 27 LR. RESULTS: As expected, HR demonstrated a greater DMN connectivity than LR, higher scores of creativity, and no significant difference in memory abilities. However, there was no significant correlation between creativity scores and DMN connectivity. DISCUSSION: These results further demonstrate that there are trait neurophysiological and psychological differences between individuals who frequently recall their dreams and those who do not. They support the forebrain and the DMN hypotheses of dreaming and leave open the possibility that increased activity in the DMN promotes creative-thinking during both wakefulness and sleep. Further work is needed to test whether activity in the DMN is causally associated with creative-thinking.

Dream recall frequency is associated with attention rather than with working memory abilities.

Several factors influencing dream recall frequency (DRF) have been identified, but some remain poorly understood. One way to study DRF is to compare cognitive processes in low and high dream recallers (LR and HR). According to the arousal-retrieval model, long-term memory encoding of a dream requires wakefulness while its multisensory short-term memory is still alive. Previous studies showed contradictory results concerning short-term memory differences between LR and HR. It has also been found that extreme DRFs are associated with different electrophysiological traits related to attentional processes. However, to date, there is no evidence for attentional differences between LR and HR at the behavioural level. To further investigate attention and working memory in HR and LR, we used a newly-developed challenging paradigm called "MEMAT" (for MEMory and ATtention), which allows the study of selective attention and working memory interaction during memory encoding of non-verbal auditory stimuli. We manipulated the difficulties of the distractor to ignore and of the memory task. The performance of the two groups were not differentially impacted by working memory load. However, HR were slower and less accurate in the presence of a hard rather than easy to-ignore distractor, while LR were much less impacted by the distractor difficulty. Therefore, we show behavioural evidence towards less resistance to hard-to-ignore distractors in HR. Using a challenging task, we show for the first time, attentional differences between HR and LR at the behavioural level. The impact of auditory attention and working memory on dream recall is discussed.

Nightmare content during the COVID-19 pandemic: Influence of COVID-related stress and sleep disruption in the United States.

Nightmares are often associated with psychiatric disorders and acute stress. This study explores how the COVID-19 pandemic may have influenced the content of nightmares. A sample of N = 419 US adults completed online surveys about sleep and COVID-19 experiences. Participants were asked about the degree to which they agreed with statements linking greater general stress, worse overall sleep and more middle-of-the-night insomnia with the COVID-19 pandemic. They were also asked if, during the pandemic, they experienced nightmares related to various themes. Logistic regression analyses examined each nightmare content as outcome and increased stress, worse sleep and more middle-of-the-night insomnia as predictors, adjusted for age, sex and race/ethnicity. Those who reported greater general COVID-related stress were more likely to have nightmares about confinement, failure, helplessness, anxiety, war, separation, totalitarianism, sickness, death, COVID and an apocalypse. Those who reported worsened sleep were more likely to have nightmares about confinement, oppression, failure, helplessness, disaster, anxiety, evil forces, war, domestic abuse, separation, totalitarianism, sickness, death, COVID and an apocalypse. Those who reported worsened middle-of-the-night insomnia were more likely to have nightmares about confinement, oppression, failure, helplessness, disaster, anxiety, war, domestic abuse, separation, totalitarianism, sickness, death, COVID and an apocalypse. These results suggest that increased pandemic-related stress may induce negatively-toned dreams of specific themes. Future investigation might determine whether (and when) this symptom indicates an emotion regulation mechanism at play, or the failure of such a mechanism.

High dream recall frequency is associated with an increase of both bottom-up and top-down attentional processes.

Event-related potentials (ERPs) associated with the involuntary orientation of (bottom-up) attention toward an unexpected sound are of larger amplitude in high dream recallers (HR) than in low dream recallers (LR) during passive listening, suggesting different attentional functioning. We measured bottom-up and top-down attentional performance and their cerebral correlates in 18 HR (11 women, age = 22.7 years, dream recall frequency = 5.3 days with a dream recall per week) and 19 LR (10 women, age = 22.3, DRF = 0.2) using EEG and the Competitive Attention Task. Between-group differences were found in ERPs but not in behavior. The results show that HR present larger ERPs to distracting sounds than LR even during active listening, arguing for enhanced bottom-up processing of irrelevant sounds. HR also presented larger contingent negative variation during target expectancy and P3b to target sounds than LR, speaking for an enhanced recruitment of top-down attention. The attentional balance seems preserved in HR since their performances are not altered, but possibly at a higher resource cost. In HR, increased bottom-up processes would favor dream recall through awakening facilitation during sleep and enhanced top-down processes may foster dream recall through increased awareness and/or short-term memory stability of dream content.

Relationship Between Epilepsy and Dreaming: Current Knowledge, Hypotheses, and Perspectives.

The interactions between epilepsy and sleep are numerous and the impact of epilepsy on cognition is well documented. Epilepsy is therefore likely to influence dreaming as one sleep-related cognitive activity. The frequency of dream recall is indeed decreased in patients with epilepsy, especially in those with primary generalized seizures. The content of dreams is also disturbed in epilepsy patients, being more negative and with more familiar settings. While several confounding factors (anti-seizure medications, depression and anxiety disorders, cognitive impairment) may partly account for these changes, some observations suggest an effect of seizures themselves on dreams. Indeed, the incorporation of seizure symptoms in dream content has been described, concomitant or not with a focal epileptic discharge during sleep, suggesting that epilepsy might directly or indirectly interfere with dreaming. These observations, together with current knowledge on dream neurophysiology and the links between epilepsy and sleep, suggest that epilepsy may impact not only wake- but also sleep-related cognition.

Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study.

Sleep is punctuated by transient elevations of vigilance level called arousals or awakenings depending on their durations. Understanding the dynamics of brain activity modifications during these transitional phases could help to better understand the changes in cognitive functions according to vigilance states. In this study, we investigated the activity of memory-related areas (hippocampus and orbitofrontal cortex) during short (3 s to 2 min) arousing reactions detected from thalamic activity, using intracranial recordings in four drug-resistant epilepsy patients. The average power of the signal between 0.5 and 128 Hz was compared across four time windows: 10 s of preceding sleep, the first part and the end of the arousal/awakening, and 10 s of wakefulness. We observed that (a) in most frequency bands, the spectral power during hippocampal arousal/awakenings is intermediate between wakefulness and sleep whereas frontal cortex shows an early increase in low and fast activities during non-rapid-eye-movement (NREM) sleep arousals/awakenings; (b) this pattern depends on the preceding sleep stage with fewer modifications for REM than for non-REM sleep arousal/awakenings, potentially reflecting the EEG similarities between REM sleep and wakefulness; (c) a greater activation at the arousing reaction onset in the prefrontal cortex predicts longer arousals/awakenings. Our findings suggest that hippocampus and prefrontal arousals/awakenings are progressive phenomena modulated by sleep stage, and, in the neocortex, by the intensity of the early activation. This pattern of activity could underlie the link between sleep stage, arousal/awakening duration and restoration of memory abilities including dream recall.

Dreams, Sleep, and Psychotropic Drugs.

Over the past 60 years, the impact of psychotropic drugs on dream recall and content has been scarcely explored. A review of the few existing experimental results on the topic leads us to the following conclusions. For antidepressant drugs, in the great majority, they reduce dream recall frequency (DRF), and the improvement of depressive symptoms is associated with an increase of positive emotion in dream content. For sedative psychotropic drugs, their improvement of sleep quality is associated with a reduction of DRF, but the effect on dream content is less clear. Few occurrences of nightmare frequency increase have been reported, with intake of molecules disturbing sleep or with the withdrawal of some psychotropic drugs. Importantly, the impact of psychotropic drugs on rapid eye movement (REM) sleep does not explain DRF modulations. The reduction of intra-sleep awakenings seems to be the parameter explaining best the modulation of DRF by psychotropic drugs. Indeed, molecules that improve sleep continuity by reducing intra-sleep awakenings also reduce the frequency of dream recall, which is coherent with the "arousal-retrieval model" stating that nighttime awakenings enable dreams to be encoded into long-term memory and therefore facilitate dream recall. DRF is nonetheless influenced by several other factors (e.g., interest in dreams, the method of awakening, and personality traits), which may explain a large part of the variability of results observed and cited in this article.

Methodological Recommendations to Control for Factors Influencing Dream and Nightmare Recall in Clinical and Experimental Studies of Dreaming.

In order to ensure robust relationships between the dependent and independent variables in clinical dream/nightmare studies, the major factors which influence the frequency of reported dreams must be controlled. This article sets out methodological recommendations to both researchers seeking to ensure the equivalence of experimental groups of participants in group-matching designs, and to clinicians who wish to check that any change in frequency of reported nightmares over the course of a psychological or a pharmacological intervention is not caused by factors other than the experimental treatment itself. The main factors influencing the frequency of dream recall are presented: demographic variables, psychological characteristics, pathological dimensions, and substance consumption. A series of questionnaires is proposed for easily measuring these control variables.

Brain functional connectivity upon awakening from sleep predicts interindividual differences in dream recall frequency.

Why do some individuals recall dreams every day while others hardly ever recall one? We hypothesized that sleep inertia-the transient period following awakening associated with brain and cognitive alterations-could be a key mechanism to explain interindividual differences in dream recall at awakening. To test this hypothesis, we measured the brain functional connectivity (combined electroencephalography-functional magnetic resonance imaging) and cognition (memory and mental calculation) of high dream recallers (HR, n = 20) and low dream recallers (LR, n = 18) in the minutes following awakening from an early-afternoon nap. Resting-state scans were acquired just after or before a 2 min mental calculation task, before the nap, 5 min after awakening from the nap, and 25 min after awakening. A comic was presented to the participants before the nap with no explicit instructions to memorize it. Dream(s) and comic recall were collected after the first post-awakening scan. As expected, between-group contrasts of the functional connectivity at 5 min post-awakening revealed a pattern of enhanced connectivity in HR within the default mode network (DMN) and between regions of the DMN and regions involved in memory processes. At the behavioral level, a between-group difference was observed in dream recall, but not comic recall. Our results provide the first evidence that brain functional connectivity right after awakening is associated with interindividual trait differences in dream recall and suggest that the brain connectivity of HR at awakening facilitates the maintenance of the short-term memory of the dream during the sleep-wake transition.

Visbrain: A Multi-Purpose GPU-Accelerated Open-Source Suite for Multimodal Brain Data Visualization.

We present Visbrain, a Python open-source package that offers a comprehensive visualization suite for neuroimaging and electrophysiological brain data. Visbrain consists of two levels of abstraction: (1) objects which represent highly configurable neuro-oriented visual primitives (3D brain, sources connectivity, etc.) and (2) graphical user interfaces for higher level interactions. The object level offers flexible and modular tools to produce and automate the production of figures using an approach similar to that of Matplotlib with subplots. The second level visually connects these objects by controlling properties and interactions through graphical interfaces. The current release of Visbrain (version 0.4.2) contains 14 different objects and three responsive graphical user interfaces, built with PyQt: Signal, for the inspection of time-series and spectral properties, Brain for any type of visualization involving a 3D brain and Sleep for polysomnographic data visualization and sleep analysis. Each module has been developed in tight collaboration with end-users, i.e., primarily neuroscientists and domain experts, who bring their experience to make Visbrain as transparent as possible to the recording modalities (e.g., intracranial EEG, scalp-EEG, MEG, anatomical and functional MRI). Visbrain is developed on top of VisPy, a Python package providing high-performance 2D and 3D visualization by leveraging the computational power of the graphics card. Visbrain is available on Github and comes with a documentation, examples, and datasets (http://visbrain.org).

Hard to wake up? The cerebral correlates of sleep inertia assessed using combined behavioral, EEG and fMRI measures.

The first minutes following awakening from sleep are typically marked by reduced vigilance, increased sleepiness and impaired performance, a state referred to as sleep inertia. Although the behavioral aspects of sleep inertia are well documented, its cerebral correlates remain poorly understood. The present study aimed at filling this gap by measuring in 34 participants the changes in behavioral performance (descending subtraction task, DST), EEG spectral power, and resting-state fMRI functional connectivity across three time points: before an early-afternoon 45-min nap, 5 min after awakening from the nap and 25 min after awakening. Our results showed impaired performance at the DST at awakening and an intrusion of sleep-specific features (spectral power and functional connectivity) into wakefulness brain activity, the intensity of which was dependent on the prior sleep duration and depth for the functional connectivity (14 participants awakened from N2 sleep, 20 from N3 sleep). Awakening in N3 (deep) sleep induced the most robust changes and was characterized by a global loss of brain functional segregation between task-positive (dorsal attention, salience, sensorimotor) and task-negative (default mode) networks. Significant correlations were observed notably between the EEG delta power and the functional connectivity between the default and dorsal attention networks, as well as between the percentage of mistake at the DST and the default network functional connectivity. These results highlight (1) significant correlations between EEG and fMRI functional connectivity measures, (2) significant correlations between the behavioral aspect of sleep inertia and measures of the cerebral functioning at awakening (both EEG and fMRI), and (3) the important difference in the cerebral underpinnings of sleep inertia at awakening from N2 and N3 sleep.

Dream Recall Frequency Is Associated With Medial Prefrontal Cortex White-Matter Density.

Recent findings indicate that dream recall frequency (DRF) is associated with neurophysiological traits, and notably the regional cerebral blood flow at rest within the medial prefrontal cortex (MPFC) and the temporo-parietal junction (TPJ). To test whether, such physiological traits are rooted in anatomical specificities, we used voxel-based morphometry to compare the white matter and gray matter density in regions related to dream recall (either at the experimental or theoretical level, MPFC, TPJ, hippocampus and amygdala) between 46 high dream recallers (HR, DRF = 5.98 ± 1.25 days per week with a dream report) and 46 low dream recallers (LR, DRF = 0.34 ± 0.29). We found an increased medial prefrontal cortex white-matter density in HR compared to LR but no other significant difference between the two groups. These results are consistent with previous studies showing that lesions within the white matter of medial prefrontal cortex are associated with a partial or total cessation of dream reporting and suggest an implication of this region in dream recall or, more likely, in dream production.

Correction: Characteristics of the memory sources of dreams: A new version of the content-matching paradigm to take mundane and remote memories into account.

[This corrects the article DOI: 10.1371/journal.pone.0185262.].

Sleep and dream habits in a sample of French college students who report no sleep disorders.

There is a lack of up-to-date data on sleep and dream habits of college students. To fill in this gap, we used an online questionnaire sent to the student mailing lists of two major universities of Lyon (Lyon 1 and Lyon 2) for the recruitment of an functional magnetic resonance imaging study with sleep disorders as exclusion criteria. In the sample (1,137 French college students, 411 males, mean age = 22.2 ± 2.4 years, body mass index = 22.0 ± 3.2 kg m-2 ), on average, the participants reported spending about 8 hr in bed during weekdays, 9 hr during the weekends, and 90.9% of them reported no difficulty falling asleep. Less than 0.4% of students reported to have sleep-walking episodes regularly, but nearly 7% reported regular sleep-talking episodes. The average dream recall frequency was about 3 mornings per week with a dream in mind. Dream recall frequency was positively correlated with the clarity of dream content and the frequency of lucid dreaming, and was negatively correlated with age. Fourteen percent of the students reported frequent lucid dreams, and 6% reported frequent recurrent dreams. We found a gender effect for several sleep and dream parameters, including dream recall frequency and time in bed, both of which were higher in women than in men. We have also observed differences between academic disciplines, namely humanities students (Lyon 2) reported spending more time in bed than sciences students (Lyon 1). These results confirm a gender difference for several sleep and dream parameters, and suggest a link between academic disciplines and sleep duration.

Daydreams incorporate recent waking life concerns but do not show delayed ('dream-lag') incorporations.

This study investigates the time course of incorporation of waking life experiences into daydreams. Thirty-one participants kept a diary for 10 days, reporting major daily activities (MDAs), personally significant events (PSEs) and major concerns (MCs). They were then cued for daydream, Rapid Eye Movement (REM) and N2 dream reports in the sleep laboratory. There was a higher incorporation into daydreams of MCs from the previous two days (day-residue effect), but no day-residue effect for MDAs or PSEs, supporting a function for daydreams of processing current concerns. A day-residue effect for PSEs and the delayed incorporation of PSEs from 5 to 7 days before the dream (the dream-lag effect) have previously been found for REM dreams. Delayed incorporation was not found in this study for daydreams. Daydreams might thus differ in function from REM sleep dreams. However, the REM dream-lag effect was not replicated here, possibly due to design differences from previous studies.

Characteristics of the memory sources of dreams: A new version of the content-matching paradigm to take mundane and remote memories into account.

Several studies have demonstrated that dream content is related to the waking life of the dreamer. However, the characteristics of the memory sources incorporated into dreams are still unclear. We designed a new protocol to investigate remote memories and memories of trivial experiences, both relatively unexplored in dream content until now. Upon awakening, for 7 days, participants identified the waking life elements (WLEs) related to their dream content and characterized them and their dream content on several scales to assess notably emotional valence. Thanks to this procedure, they could report WLEs from the whole lifespan, and mundane ones before they had been forgotten. Participants (N = 40, 14 males, age = 25.2 ± 7.6) reported 6.2 ± 2.0 dreams on average. For each participant, 83.4% ± 17.8 of the dream reports were related to one or more WLEs. Among all the WLEs incorporated into dreams dated by the participants (79.3 ± 19%), 40.2 ± 30% happened the day before the dream, 26.1 ± 26% the month before (the day before excluded), 15.8 ± 21% the year before the dream (the month before excluded), and 17.9 ± 24% happened more than one year before the dream. As could be expected from previous studies, the majority of the WLEs incorporated into dreams were scored as important by the dreamers. However, this was not true for incorporated WLEs dating from the day before the dream. In agreement with Freud's observations, the majority of the day residues were scored as mundane. Finally, for both positive and negative WLEs incorporated into dreams, the dreamt version of the WLE was rated as emotionally less intense than the original WLE. This result, showing that dreams tend to attenuate the emotional tone of waking-life memories towards a more neutral one, argues in favor of the emotional regulation hypothesis of dreaming.