A review of mentation in REM and NREM sleep: "covert" REM sleep as a possible reconciliation of two opposing models

Numerous studies have replicated the finding of mentation in both rapid eye movement (REM) and nonrapid eye movement (NREM) sleep. However, two different theoretical models have been proposed to account for this finding: (1) a one-generator model, in which mentation is generated by a single set of processes regardless of physiological differences between REM and NREM sleep; and (2) a two-generator model, in which qualitatively different generators produce cognitive activity in the two states. First, research is reviewed demonstrating conclusively that mentation can occur in NREM sleep; global estimates show an average mentation recall rate of about 50% from NREM sleep--a value that has increased substantially over the years. Second, nine different types of research on REM and NREM cognitive activity are examined for evidence supporting or refuting the two models. The evidence largely, but not completely, favors the two-generator model. Finally, in a preliminary attempt to reconcile the two models, an alternative model is proposed that assumes the existence of covert REM sleep processes during NREM sleep. Such covert activity may be responsible for much of the dreamlike cognitive activity occurring in NREM sleep.     

EEG asymmetry and sleep mentation during REM and NREM

The hypothesis that dreaming is mediated by the right hemisphere was evaluated by monitoring EEG power asymmetry during REM and NREM sleep, and obtaining mentation reports when short-term temporal shifts in the EEG indicated relative left- or right-hemispheric dominance. Content analyses provided no support for the right-hemisphere hypothesis; indeed, some scales showed higher content during relative left-hemispheric dominance. In contrast to earlier reports, no difference between REM and NREM in EEG asymmetry was observed.     

Effects of protein synthesis inhibitors on sleep and amygdala-kindled seizure thresholds in cats

This study examined the effects of protein synthesis inhibitors on sleep and seizure susceptibility in amygdala-kindled cats. Six cats with stable seizure thresholds were treated with 150 mg/kg of chloramphenicol or its cogener, thiamphenicol, at 12-h intervals over a 30-h period. State pattern variables were monitored continuously during the first 18 h. At 30 h, kindled seizure thresholds were measured in terms of minimum stimulus intensities (microA) required to elicit generalized tonic clonic convulsions. All cats were exposed to both drugs, with a 1-week intertrial interval and the order of drug treatment counterbalanced. Rapid eye movement (REM) sleep was significantly attenuated after chloramphenicol but was unaffected by thiamphenicol, as previously shown. Seizure thresholds were unaltered regardless of changes in sleep state physiology. The results extend previous work showing that protein synthesis inhibitors which suppress REM sleep increase seizure susceptibility only in animals that are either highly predisposed to seizures or that display REM sleep disruption as the sole sleep deficit associated with their seizure condition.     

Electroencephalographic and autonomic alterations in subjects with frequent nightmares during pre-and post-REM periods

Abnormal arousal processes, sympathetic influences, as well as wake-like alpha activity during sleep were reported as pathophysiological features of Nightmare Disorder. We hypothesized that in Nightmare Disorder, wake-like cortical activity and peripheral measures linked to arousals would be triggered by physiological processes related to the initiation of REM periods. Therefore, we examined electroencephalographic (EEG), motor and autonomous (cardiac) activity in a group of nightmare (NM) and healthy control (CTL) subjects during sleep-state-transitions while controlling for the confounding effects of trait anxiety. Based on the second-nights’ polysomnographic recordings of 19 Nightmare Disordered (NM) and 21 control (CTL) subjects, we examined the absolute power spectra focusing on the alpha range, measures of heart rate variability (HRV) and motor (muscle tone) activity during pre-REM and post-REM periods, separately. According to our results, the NM group exhibited increased alpha power during pre-REM, but not in post-REM, or stable, non-transitory periods. While CTL subjects showed increased HRV during pre-REM periods in contrast to post-REM ones, NM subjects did not exhibit such sleep state-specific differences in HRV, but showed more stable values across the examined sleep stages and less overall variability reflecting generally attenuated parasympathetic activity during sleep-state-transitions and during stable, non-transitory NREM states. These differences were not mediated by waking levels of trait anxiety. Moreover, in both groups, significant differences emerged regarding cortical and motor (muscle tone) activity between pre-REM and post-REM conditions, reflecting the heterogeneity of NREM sleep. Our findings indicate that NM subjects’ sleep is compromised during NREM–REM transitions, but relatively stabilized after REM periods. The coexistence of sleep-like and wake-like cortical activity in NM subjects seems to be triggered by REM/WAKE promoting neural activity. We propose that increased arousal-related phenomena in NREM–REM transitions might reflect altered emotional processing in NM subjects.     

Sensorimotor EEG operant conditioning: Experimental and clinical effects

Neurophysiological studies in cats have established a functional relationship between waking 12–15 Hz sensorimotor cortex rhythmic EEG activity (the sensorimotor rhythm or SMR) and a similar pattern during sleep, the sleep spindle. Both result from oscillatory thalamocortical discharge involving ventrobasal thalamus and sensorimotor cortex, and both are associated with a state of suppressed motor excitability. Enhancement of the SMR with operant conditioning methods in the cat clearly led to reduced seizure susceptibility. The experimental application of this approach to seizure control in epileptics has resulted in (A) evidence that EEG patterns can be manipulated significantly in man with operant conditioning, (B) suggestive observations concerning a potential component of pathology in epilepsy, and (C) strong preliminary evidence that SMR operant conditioning in epileptics is specifically therapeutic. Current research has focused upon the EEG during sleep in epileptics with primary motor symptomatology. This measure often reveals several hard signs of pathology. These include the presence of abnormal activity in the 4–7 Hz frequency band and the absence or disturbance of activity in the 11–15 Hz frequency band. Power spectral analysis is being utilized to quantify these sleep EEG components in five groups of epileptic patients, studied with different frequency patterns rewarded in an A-B-A design which provides for counterbalancing of order effects. Initial laboratory training is followed by 9–12 months of training at home with portable feedback equipment. Reward contingencies are reversed within each group at approximately three month intervals. Clinical EEG data, blood anticonvulsant measures and patient seizure logs supplement sleep EEG data obtained before training and after each phase of the design. Early results have again indicated specific therapeutic benefits following training of high frequency rhythmic central cortical activity.     

Hemispheric lateralization of the EEG during wakefulness and REM sleep in young healthy adults

EEG recordings confirm hemispheric lateralization of brain activity during cognitive tasks. The aim of the present study was to investigate spontaneous EEG lateralization under two conditions, waking and REM sleep. Bilateral monopolar EEG was recorded in eight participants using a 12-electrode montage, before the night (5 min eyes closed) and during REM sleep. Spectral analysis (0.75-19.75 Hz) revealed left prefrontal lateralization on total spectrum amplitude power and right occipital lateralization in Delta activity during waking. In contrast, during REM sleep, right frontal lateralization in Theta and Beta activities and right lateralization in occipital Delta activity was observed. These results suggest that spontaneous EEG activities generated during waking and REM sleep are supported in part by a common thalamo-cortical neural network (right occipital Delta dominance) while additional, possibly neuro-cognitive factors modulate waking left prefrontal dominance and REM sleep right frontal dominance.     

Sleep EEG changes during adolescence: An index of a fundamental brain reorganization

Delta (1–4 Hz) EEG power in non-rapid eye movement (NREM) sleep declines massively during adolescence. This observation stimulated the hypothesis that during adolescence the human brain undergoes an extensive reorganization driven by synaptic elimination. The parallel declines in synaptic density, delta wave amplitude and cortical metabolic rate during adolescence further support this model. These late brain changes probably represent the final ontogenetic manifestation of nature’s strategy for constructing nervous systems: an initial overproduction of neural elements followed by elimination. Errors in adolescent brain reorganization may cause mental illness; this could explain the typical age of onset of schizophrenia. Longitudinal studies of sleep EEG are enhancing our knowledge of adolescent brain maturation. Our longitudinal study of sleep EEG changes in adolescence showed that delta power, which may reflect frontal cortex maturation, begins its decline between ages 11 and 12 years and falls by 65% by age 17 years. In contrast, NREM theta power begins its decline much earlier. Delta and theta EEG frequencies are important to sleep theory because they behave homeostatically. Surprisingly, these brain changes are unrelated to pubertal maturation but are strongly linked to age. In addition to these (and other) maturational EEG changes, sleep schedules in adolescence change in response to a complex interaction of circadian, social and other influences. Our data demonstrate that the daytime sleepiness that emerges in adolescence is related to the decline in NREM delta as well as to altered sleep schedules. These longitudinal sleep data provide guideposts for studying cognitive and behavioral correlates of adolescent brain reorganization.     

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.     

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.     

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.     

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.     

Frontal electroencephalogram alpha asymmetry during sleep: stability and its relation to affective style

Electroencephalogram (EEG) alpha (8-12 Hz) asymmetries were collected from the mid-frontal and central regions during presleep wakefulness and Stage 1, Stage 2, and rapid eye movement (REM) sleep in 11 healthy right-handed participants who were free of psychiatric, neurological, and sleep problems. The authors found significant correlations between presleep wakefulness and different stages of sleep in the frontal, but not central, EEG alpha asymmetry measure. The strongest correlation was between presleep waking and REM sleep, replicating and extending relation earlier work to a normal population. The high degree of association between presleep waking and REM sleep may be a result of high cortical activation common to these states and may reflect a predisposition to different styles of emotional reactivity.     

Changes in processing of masked stimuli across early- and late-night sleep: a study on behavior and brain potentials

Sleep has proven to support the memory consolidation in many tasks including learning of perceptual skills. Explicit, conscious types of memory have been demonstrated to benefit particularly from slow-wave sleep (SWS), implicit, non-conscious types particularly from rapid eye movement (REM) sleep. By comparing the effects of early-night sleep, rich in SWS, and late-night sleep, rich in REM sleep, we aimed to separate the contribution of these two sleep stages in a metacontrast masking paradigm in which explicit and implicit aspects in perceptual learning could be assessed separately by stimulus identification and priming, respectively. We assumed that early sleep intervening between two sessions of task performance would specifically support stimulus identification, while late sleep would specifically support priming. Apart from overt behavior, event-related EEG potentials (ERPs) were measured to record the cortical mechanisms associated with behavioral changes across sleep. In contrast to our hypothesis, late-night sleep appeared to be more important for changes of behavior, both for stimulus identification, which tended to improve across late-night sleep, and for priming, with the increase of errors induced by masked stimuli correlating with the duration of REM sleep. ERP components proved sensitive to presence of target shapes in the masked stimuli and to their priming effects. Of these components, the N2 component, indicating processing of conflict, became larger across early-night sleep and was related to the duration of S4 sleep, the deepest substage of SWS containing particularly high portions of EEG slow waves. These findings suggest that sleep promotes perceptual learning primarily by its REM sleep portion, but indirectly also by way of improved action monitoring supported by deep slow-wave sleep.     

Brain Gene Expression During REM Sleep Depends on Prior Waking Experience

In most mammalian species studied, two distinct and successive phases of sleep, slow wave (SW), and rapid eye movement (REM), can be recognized on the basis of their EEG profiles and associated behaviors. Both phases have been implicated in the offline sensorimotor processing of daytime events, but the molecular mechanisms remain elusive. We studied brain expression of the plasticity-associated immediate-early gene (IEG) zif-268 during SW and REM sleep in rats exposed to rich sensorimotor experience in the preceding waking period. Whereas nonexposed controls show generalized zif-268 down-regulation during SW and REM sleep, zif-268 is upregulated during REM sleep in the cerebral cortex and the hippocampus of exposed animals. We suggest that this phenomenon represents a window of increased neuronal plasticity during REM sleep that follows enriched waking experience.     

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.     

Sleep-dependent hippocampal slow activity correlates with waking memory performance in humans

The positive effect of postlearning sleep on memory consolidation as well as the relationship between sleep-related memory processes and the hippocampal formation are increasingly clarified topics in neurobiology. However, the possibility of a stable relationship between waking mnemonic performance and sleep-dependent hippocampal electric activity is unexplored. Here we report a correlative analysis between sleep-dependent parahippocampal-hippocampal (pHip-Hip) electric activity recorded by foramen ovale (FO) electrodes and different types of memory performances in epileptic patients. Psychological testing was performed days or weeks before electrophysiological recordings. The relative spectral power of the slow activity (below 1.25 Hz) during deep non-REM (NREM) sleep at the right pHip-Hip region correlated positively with the visual memory performance according to Rey-Osterrieth Complex Figure Test (ROCFT). Along the posterior-anterior direction of the hippocampal formation a linear increasing of correlations was observed. The relative power of the activity below 1.25 Hz at the left pHip-Hip during phasic REM sleep correlated positively with verbal learning performance and mnemonic retention values according to ROCFT. It is concluded that the pHip-Hip structures' capacity of producing high amplitude and synchronized slow (< 1 Hz) oscillation during deep NREM sleep is related to the functional power of these structures. We hypothesize that the asymmetric (side-specific) propagation of ponto-geniculo-occipital (PGO) activity to the pHip-Hip region is related to the memory correlates of phasic REM sleep.     

Associative relationships between pre-sleep sentence stimuli and reports of mental sleep experience

The aim of this experiment was to study some linguistic relationships between pre-sleep verbal stimuli and contents of reports of mental experience during sleep. In 4 weekly sessions 16 subjects listened before sleep to a sentence stimulus, which was either semantically acceptable (SEM+) or not (SEM-), and were told to retain it for a recall test after awakening; they were awakened once each night during NREM or REM sleep and asked to report their mental experience during sleep. The relationships between the stimulus and the contents of the reports were classified using Clark's (1970) associative rules. Both pre-sleep sentence stimuli were frequently incorporated into contents of NREM and REM reports, without significant differences between the two types of sleep. The SEM+ sentence led prevalently to incorporations through paradigmatic associative relationships, while the SEM- sentence led to incorporations through both paradigmatic and syntagmatic relationships. It appears that all the features of the lexical constituents of the stimulus may be involved in the processing leading to incorporation.     

Behavioral,subjective, and electroencephalographic indices of sleep onset latency and sleep duration

Electrographic (EEG, EOG, EMG) indices have been used for some decades in the definition of the stages of sleep and more recently in the diagnosis of sleep-related disorders, e.g., insomnia, despite the lack of detailed information concerning the precise relationship between such electrographic indices and behavioral and subjective criteria of sleep. Evaluation of the relationship between EEG, behavioral, and self-report measures of sleep onset latency and sleep duration was conducted using 17 young normal sleepers. The behavioral measure was provided by an apparatus which records subjects' button-press responses to an auditory stimulus presented at various interstimulus intervals (2, 5, and random 1, 2, 5, 7, and 10 min). The behavioral and stage 2 EEG estimates of sleep onset latency (SOL) and sleep duration (SD) were almost identical. The stage 1 EEG provided the shortest estimate of SOL; the self-report measure, the longest. The SD measures were in reverse order. There were no significant differences among the three interstimulus interval conditions (2, 5, and random min). Average response rates to the 50-dB chime were 100% during wakefulness, 81% during EEG stage 1, and 8% during EEG stage 2. Almost all stage 2 responding occurred during the first 5 min of each stage 2 period. The validity of electrographic indices as sleep criteria and the implications of the findings for the formulation of an adequate definition of sleep and its clinical measurement are discussed.