Cognitive and emotional processes during dreaming: a neuroimaging view

Dream is a state of consciousness characterized by internally-generated sensory, cognitive and emotional experiences occurring during sleep. Dream reports tend to be particularly abundant, with complex, emotional, and perceptually vivid experiences after awakenings from rapid eye movement (REM) sleep. This is why our current knowledge of the cerebral correlates of dreaming, mainly derives from studies of REM sleep. Neuroimaging results show that REM sleep is characterized by a specific pattern of regional brain activity. We demonstrate that this heterogeneous distribution of brain activity during sleep explains many typical features in dreams. Reciprocally, specific dream characteristics suggest the activation of selective brain regions during sleep. Such an integration of neuroimaging data of human sleep, mental imagery, and the content of dreams is critical for current models of dreaming; it also provides neurobiological support for an implication of sleep and dreaming in some important functions such as emotional regulation.     

Dreaming and the brain: toward a cognitive neuroscience of conscious states

Sleep researchers in different disciplines disagree about how fully dreaming can be explained in terms of brain physiology. Debate has focused on whether REM sleep dreaming is qualitatively different from nonREM (NREM) sleep and waking. A review of psychophysiological studies shows clear quantitative differences between REM and NREM mentation and between REM and waking mentation. Recent neuroimaging and neurophysiological studies also differentiate REM, NREM, and waking in features with phenomenological implications. Both evidence and theory suggest that there are isomorphisms between the phenomenology and the physiology of dreams. We present a three-dimensional model with specific examples from normally and abnormally changing conscious states.     

The case against memory consolidation in REM sleep

We present evidence disputing the hypothesis that memories are processed or consolidated in REM sleep. A review of REM deprivation (REMD) studies in animals shows these reports to be about equally divided in showing that REMD does, or does not, disrupt learning/memory. The studies supporting a relationship between REM sleep and memory have been strongly criticized for the confounding effects of very stressful REM deprivation techniques. The three major classes of antidepressant drugs, monoamine oxidase inhibitors (MAOIs), tricyclic antidepressants (TCAs), and selective serotonin reuptake inhibitors (SSRIs), profoundly suppress REM sleep. The MAOIs virtually abolish REM sleep, and the TCAs and SSRIs have been shown to produce immediate (40-85%) and sustained (30-50%) reductions in REM sleep. Despite marked suppression of REM sleep, these classes of antidepressants on the whole do not disrupt learning/memory. There have been a few reports of patients who have survived bilateral lesions of the pons with few lingering complications. Although these lesions essentially abolished REM sleep, the patients reportedly led normal lives. Recent functional imaging studies in humans have revealed patterns of brain activity in REM sleep that are consistent with dream processes but not with memory consolidation. We propose that the primary function of REM sleep is to provide periodic endogenous stimulation to the brain which serves to maintain requisite levels of central nervous system (CNS) activity throughout sleep. REM is the mechanism used by the brain to promote recovery from sleep. We believe that the cumulative evidence indicates that REM sleep serves no role in the processing or consolidation of memory.     

Testing the involvement of the prefrontal cortex in lucid dreaming: A tDCS study

Recent studies suggest that lucid dreaming (awareness of dreaming while dreaming) might be associated with increased brain activity over frontal regions during rapid eye movement (REM) sleep. By applying transcranial direct current stimulation (tDCS), we aimed to manipulate the activation of the dorsolateral prefrontal cortex (DLPFC) during REM sleep to increase dream lucidity. Nineteen participants spent three consecutive nights in a sleep laboratory. On the second and third nights they randomly received either 1 mA tDCS for 10 min or sham stimulation during each REM period starting with the second one. According to the participants’ self-ratings, tDCS over the DLPFC during REM sleep increased lucidity in dreams. The effects, however, were not strong and found only in frequent lucid dreamers. While this indicates some preliminary support for the involvement of the DLPFC in lucid dreaming, further research, controlling for indirect effects of stimulation and including other brain regions, is needed.     

Rapid eye movement sleep dreaming is characterized by uncoupled EEG activity between frontal and perceptual cortical regions

EEG coherent activity is involved in the binding of spatially separated but temporally correlated stimuli into whole events. Cognitive features of rapid eye movement sleep (REM) dreaming resemble frontal lobe dysfunction. Therefore, temporal coupling of EEG activity between frontal and perceptual regions was analyzed from 10 min prior to dream reports (8 adults) from stage-2 and REM sleep. EEG correlation between frontal and perceptual regions decreased and, among perceptual regions increased during REM. The temporal dissociation of EEG activity between executive and perceptual regions supplies an inadequate mechanism for the binding and interpretation of ongoing perceptual activity resulting in dream bizarreness.     

Dreaming and REM sleep are controlled by different brain mechanisms

The paradigmatic assumption that REM sleep is the physiological equivalent of dreaming is in need of fundamental revision. A mounting body of evidence suggests that dreaming and REM sleep are dissociable states, and that dreaming is controlled by forebrain mechanisms. Recent neuropsychological, radiological, and pharmacological findings suggest that the cholinergic brain stem mechanisms that control the REM state can only generate the psychological phenomena of dreaming through the mediation of a second, probably dopaminergic, forebrain mechanism. The latter mechanism (and thus dreaming itself) can also be activated by a variety of nonREM triggers. Dreaming can be manipulated by dopamine agonists and antagonists with no concomitant change in REM frequency, duration, and density. Dreaming can also be induced by focal forebrain stimulation and by complex partial (forebrain) seizures during nonREM sleep, when the involvement of brainstem REM mechanisms is precluded. Likewise, dreaming is obliterated by focal lesions along a specific (probably dopaminergic) forebrain pathway, and these lesions do not have any appreciable effects on REM frequency, duration, and density. These findings suggest that the forebrain mechanism in question is the final common path to dreaming and that the brainstem oscillator that controls the REM state is just one of the many arousal triggers that can activate this forebrain mechanism. The "REM-on" mechanism (like its various NREM equivalents) therefore stands outside the dream process itself, which is mediated by an independent, forebrain "dream-on" mechanism.     

Sleep disturbances in the aftermath of trauma and posttraumatic stress disorder

Sleep disturbances, including nightmares and insomnia, are prominent following trauma and with posttraumatic stress disorder (PTSD) and likely contribute to the pathogenesis of the disorder. Findings from laboratory studies of PTSD have been inconsistent in terms of documenting objective impaired sleep maintenance but have been somewhat more consistent in indicating alterations of rapid eye movement (REM) sleep. Studies of the early aftermath of trauma can reduce the complexity associated with chronicity and comorbidity, and may have implications for early diagnosis and prevention. Multiple studies indicate that dream content is affected by recent threatening experiences. The development of PTSD is associated with a more replicative type of nightmare content. Sleep is reported to be generally disrupted following trauma especially among those developing PTSD. The limited number of studies that provide objective recorded indices during the early aftermath of trauma also provide a mixed picture regarding overall sleep maintenance. Recent data suggest that a more specific disruption of REM sleep may be associated with the development of PTSD and that this disruption is associated with an increased signal of sympathetic nervous system activation during REM sleep. Disrupted REM sleep and increased sympathetic/noradrenergic activity may have implications for understanding recent promising interventions for PTSD sleep disturbance that can be applied to early intervention.     

A "Jekyll and Hyde" within: aggressive versus friendly interactions in REM and non-REM dreams

We hypothesized that representations of social interactions in REM and non-REM (NREM) dreams would reflect differing regional brain activation patterns associated with the two sleep states, and that levels of aggressive interactions would be higher in REM than in NREM dreams. One hundred REM, 100 NREM, and 100 wake reports were collected in the home from 8 men and 7 women using the Nightcap sleep-wake mentation-monitoring system and scored for number and variety of social interactions. We found that (a) social interactions were more likely to be depicted in dream than in wake reports, (b) aggressive social interactions were more characteristic of REM than NREM or wake reports, and (c) dreamer-initiated friendliness was more characteristic of NREM than REM reports. We conclude that processing of, or simulations about, selected social interactions is preferentially performed while "off-line" during the dream state, with the REM state specializing in simulation of aggressive interactions and the NREM state specializing in simulation of friendly interactions.     

Brain-mind states: reciprocal variation in thoughts and hallucinations

The exclusion of thinking from recent studies of sleep mentation has hindered a full appreciation of how cognitive activity differs across the states of waking and sleep. To overcome this limitation, this study investigated thoughts and hallucinations using experience sampling, home-based sleep-wake monitoring, and formal analyses of the psychological data. The prevalence of thoughts decreased gradually from waking through sleep onset and non-REM sleep, to reach its nadir in REM sleep, whereas hallucinations increased sharply across these states. Furthermore, multiple occurrences of hallucinations but not of thoughts increased significantly from sleep onset through non-REM sleep, to a peak in REM sleep. This reciprocity in thoughts and hallucinations might reflect a progressive shift from high to low aminergic-to-cholinergic neuromodulatory ratios across wake-sleep states, accompanied by an array of changes in the regional activation patterns of the brain.     

Dreaming without REM sleep

To test whether mental activities collected from non-REM sleep are influenced by REM sleep, we suppressed REM sleep using clomipramine 50mg (an antidepressant) or placebo in the evening, in a double blind cross-over design, in 11 healthy young men. Subjects were awakened every hour and asked about their mental activity. The marked (81%, range 39-98%) REM-sleep suppression induced by clomipramine did not substantially affect any aspects of dream recall (report length, complexity, bizarreness, pleasantness and self-perception of dream or thought-like mentation). Since long, complex and bizarre dreams persist even after suppressing REM sleep either partially or totally, it suggests that the generation of mental activity during sleep is independent of sleep stage.     

Search activity in the context of psychosomatic disturbances,of brain monoamines and REM sleep function

The author discusses a number of controversial aspects of the search activity concept. This concept, based on an analysis of data cited by other researchers and the results of the author’s own investigation, performed together with V. V. Arshavsky, postulates that search activity raises the body’s resistance to stress and experimentally induced pathology whereas renunciation of search forms a nonspecific predisposition to somatic disturbances (e.g., psychosomatic disease). REM sleep is regarded as a specific form of search activity aimed at compensating for the state of renunciation of search in walking. In this paper the author argues that 1) renunciation of search can be accompanied either by anxiety or by depression, 2) REM sleep deprivation on a “small platform” raises the requirement in REM sleep by producing renunciation of search, 3) during search activity brain catecholamine synthesis is stimulated by catabolism whereas a state of renunciation of search upsets this feedback system. The actuation of the brain mechanisms of search in REM sleep necessitates a certain brain catecholamine level. If the brain catecholamine level is very high during waking behavior due to intensive search activity, the REM sleep requirement is low, REM sleep becoming reduced. After a moderate drop in the brain catecholamine level at the initial stage of renunciation of search the requirement in REM sleep rises and this phase grows longer. But at the late stage of renunciation of search the brain catecholamine level drops extremely, REM sleep shrinking in spite of the great appropriate requirement, and 4) the functional insufficiency of REM sleep invites various forms of pathology.     

Dreaming and the default network: A review,synthesis, and counterintuitive research proposal

This article argues that the default network, augmented by secondary visual and sensorimotor cortices, is the likely neural correlate of dreaming. This hypothesis is based on a synthesis of work on dream content, the findings on the contents and neural correlates of mind-wandering, and the results from EEG and neuroimaging studies of REM sleep. Relying on studies in the 1970s that serendipitously discovered episodes of dreaming during waking mind-wandering, this article presents the seemingly counterintuitive hypothesis that the neural correlates for dreaming could be further specified in the process of carrying out EEG/fMRI studies of mind-wandering and default network activity. This hypothesis could be tested by asking participants for experiential reports during moments of differentially high levels of default network activation, as indicated by mixed EEG/fMRI criteria. Evidence from earlier EEG/fMRI studies of mind-wandering and from laboratory studies of dreaming during the sleep-onset process is used to support the argument.     

Poor recall of eye-movement signals from Stage 2 compared to REM sleep: implications for models of dreaming

An ongoing assumption made by sleep researchers is that since dreams are more often recalled on awakening from rapid eye movement (REM) sleep, dreams must occur more often during this stage of sleep. An alternative hypothesis is that cognition occurs throughout sleep, but the recall of this mentation differs on awakening. When a dream is not reported on awakening, there is no method of establishing whether it did not happen or was forgotten. The aim of the present study was to investigate this issue using an eye movement (EM) signal verification technique. Participants were instructed to produce an EM signal whenever they heard a tone. Tones were presented at increasing volume during Stage 2 and REM sleep until EM signal verification was observed. Ninety seconds after signal verification, participants were awakened and asked if they remembered hearing the tone or responding with the EM signal. Such recollection of signal verified tone (SVT) presentations was significantly less after Stage 2 sleep (65%) compared to REM sleep (100%) presentations. Furthermore, SVT recall was significantly correlated with reported dream recall frequency, suggesting the same processes involved in recalling SVTs might also underlie dream recall.     

Continuity between waking activities and dream activities

Empirical studies largely support the continuity hypothesis of dreaming. Despite of previous research efforts, the exact formulation of the continuity hypothesis remains vague. The present paper focuses on two aspects: (1) the differential incorporation rate of different waking-life activities and (2) the magnitude of which interindividual differences in waking-life activities are reflected in corresponding differences in dream content. Using a correlational design, a positive, non-zero correlation coefficient will support the continuity hypothesis. Although many researchers stress the importance of emotional involvement on the incorporation rate of waking-life experiences into dreams, formulated the hypothesis that highly focused cognitive processes such as reading, writing, etc. are rarely found in dreams due to the cholinergic activation of the brain during dreaming. The present findings based on dream diaries and the exact measurement of waking activities replicated two recent questionnaire studies. These findings indicate that it will be necessary to specify the continuity hypothesis more fully and include factors (e.g., type of waking-life experience, emotional involvement) which modulate the incorporation rate of waking-life experiences into dreams. Whether the cholinergic state of the brain during REM sleep or other alterations of brain physiology (e.g., down-regulation of the dorsolateral prefrontal cortex) are the underlying factors of the rare occurrence of highly focused cognitive processes in dreaming remains an open question. Although continuity between waking life and dreaming has been demonstrated, i.e., interindividual differences in the amount of time spent with specific waking-life activities are reflected in dream content, methodological issues (averaging over a two-week period, small number of dreams) have limited the capacity for detecting substantial relationships in all areas. Nevertheless, it might be concluded that the continuity hypothesis in its present general form is not valid and should be elaborated and tested in a more specific way.     

Motivation and affect in REM sleep and the mentation reporting process

Although the emotional and motivational characteristics of dreaming have figured prominently in folk and psychoanalytic conceptions of dream production, emotions have rarely been systematically studied, and motivation, never. Because emotions during sleep lack the somatic components of waking emotions, and they change as the sleeper awakens, their properties are difficult to assess. Recent evidence of limbic system activation during REM sleep suggests a basis in brain architecture for the interaction of motivational and cognitive properties in dreaming. Motivational and emotional content in REM and NREM laboratory mentation reports from 25 participants were compared. Motivational and emotional content was significantly greater in REM than NREM sleep, even after controlling for the greater word count of REM reports.     

NonREM sleep mentation in chronically-treated persons with schizophrenia

This study examined the laboratory dream content reported by 14 patients with schizophrenia and 15 controls, with a focus on reports obtained from NonREM sleep. Both the controls' and patients' frequency of dream recall following awakenings from NonREM and REM sleep were similar to values reported for healthy participants. Patients' NonREM sleep narratives were shorter than those from controls. When compared to their reports from REM sleep, both groups' NonREM sleep reports included significantly fewer words and reportable items. The controls were more likely to report a subjective feeling of bizarreness for their REM sleep reports as compared to their NonREM sleep reports. This difference was not observed in patients with schizophrenia. Taken together, these findings suggest few differences between the NonREM sleep mentation of patients with schizophrenia and of controls and that sleep stage cognitive style is comparable in both groups, with NonREM sleep reports being more thought-like, less elaborate and bizarre than REM sleep reports.     

The ability to self-tickle following Rapid Eye Movement sleep dreaming

Self-produced tactile stimulation usually feels less tickly--is perceptually attenuated--relative to the same stimulation produced externally. This is not true, however, for individuals with schizophrenia. Here, we investigate whether the lack of attenuation to self-produced stimuli seen in schizophrenia also occurs for normal participants following REM dreams. Fourteen participants were stimulated on their left palm with a tactile stimulation device which allowed the same stimulus to be generated by the participant or by the experimenter. The level of self-tickling attenuation did not differ between REM and non-REM sleep awakening conditions, where presence or absence of an accompanying dream was not controlled for. However, for the female participants, when awakening occurred from an REM sleep dream, self-stimulation ratings were higher than for external stimulation, whereas ratings after NREM sleep unaccompanied by a dream were lower for self-stimulation than for external stimulation. These results indicate deficits in self-monitoring and a confusion between self- and externally generated stimulation accompany REM dream formation.     

Cognitive asymmetry and dreaming: lack of relationship

The present study investigated the relationship between cognitive laterality and dream recall, dream characteristics, and eye movement density in rapid eye movement (REM) sleep. Fifty-two right-handed males, age 20-30 years, were tested on a six-test battery of which three tests measure right hemisphere function and three tests measure left hemisphere function. Based on their performance, 14 subjects were selected for a sleep laboratory study. Each spent 3 experimental nights in the laboratory during which they were awakened from REM sleep for dream reports. Dream reports were scored for bizarreness, emotions, visual elements, and overall "dreamlike" versus "thoughtlike" character. Subjects were awakened from 123 REM periods, of which 96 yielded positive dream reports (78.04%). Neither the rate of recall nor the four evaluation scores were correlated with the laterality scores that were constructed from the six-test battery. Eye movement density during REM sleep was significantly positively correlated with the total performance of the two hemispheres. These results do not support the alleged lateralization of dreaming. In agreement with recent reports in the literature, it is concluded that dreaming cannot be seen as a "right hemisphere" function.     

Dream recall, dream length, and sleep duration: state or trait factor

Longer sleep duration should be related to dream recall (longer REM sleep), but previous findings regarding the relationship between habitual sleep duration and dream recall frequency have been conflicting, whereas experimental manipulation of sleep duration yielded a significant effect. The analysis of diaries kept by the 444 participants over 14 days indicated that intra-individual fluctuations and interindividual differences in sleep duration affect dream recall.     

REM motivation induced by brief REM deprivation: the influence of cognition, gender, and personality.

Prominence of the brain's right-hemisphere information processing and intensity of dream experience are two theoretically related constructs that have been proposed as important psychological aspects of REM sleep. Either view is consistent with the prediction that the effect of REM deprivation will depend in part on the nature of cognitive activity that is initiated at the onset of each REM period and that "substitutes" for the interrupted REM process. In the present study, the effect of REM deprivation was more striking for female subjects given a digits task than for female subjects given a fantasy-reporting task during awakening used to induce REM deprivation for the first 6 hours of the night. High neuroticism appeared to exaggerate the effect. No corresponding pattern was observed for the male subjects. These preliminary finding may be exaggerated by cognitive activity that is functionally incongruent with those processes. The results also raise interesting questions about individual differences.