Temporal coupling of rapid eye movements and cerebral activities during REM sleep

ObjectivesWe investigated event-related potentials time locked to the onset and offset of rapid eye movements during rapid eye movement (REM) sleep.MethodNine healthy university students participated in this study. Data were collected in a sleep laboratory. Rapid eye movements during REM sleep were recorded during natural nocturnal sleep. Saccades during wakefulness were recorded during a visually triggered task. Event-related potentials were averaged, time-locked to the onset and offset of eye movements.ResultsDuring REM sleep, a lambda-like response occurred over the occipital region, time-locked to the offset of rapid eye movements (similar to what occurs during wakefulness). Moreover, we found that a positive potential (P200r) occurred at about 200 ms, with the maximal amplitude over the central region and time-locked to the onset of rapid eye movements during REM sleep; this potential was not observed during wakefulness.ConclusionsDuring REM sleep, the P200r occurs with the start of rapid eye movements, and then the lambda-like response occurs after termination of the movements.SignificanceWe demonstrated temporal coupling of rapid eye movements and cerebral activities during REM sleep. These activities might provide a useful basis for future investigations of brain functions during REM sleep.     

fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep

We studied the neural correlates of rapid eye movement during sleep (REM) by timing REMs from video recording and using rapid event-related functional MRI. Consistent with the hypothesis that REMs share the brain systems and mechanisms with waking eye movements and are visually-targeted saccades, we found REM-locked activation in the primary visual cortex, thalamic reticular nucleus (TRN), 'visual claustrum', retrosplenial cortex (RSC, only on the right hemisphere), fusiform gyrus, anterior cingulate cortex, and the oculomotor circuit that controls awake saccadic eye movements (and subserves awake visuospatial attention). Unexpectedly, robust activation also occurred in non-visual sensory cortices, motor cortex, language areas, and the ascending reticular activating system, including basal forebrain, the major source of cholinergic input to the entire cortex. REM-associated activation of these areas, especially non-visual primary sensory cortices, TRN and claustrum, parallels findings from waking studies on the interactions between multiple sensory data, and their 'binding' into a unified percept, suggesting that these mechanisms are also shared in waking and dreaming and that the sharing goes beyond the expected visual scanning mechanisms. Surprisingly, REMs were associated with a decrease in signal in specific periventricular subregions, matching the distribution of the serotonergic supraependymal plexus. REMs might serve as a useful task-free probe into major brain systems for functional brain imaging.     

Lack of presaccadic positivity before rapid eye movements in human REM sleep

Differences between oculomotor control of rapid eye movements (REMs) in REM sleep and that of saccades in wakefulness were examined electrophysiologically in human adults. Fourteen healthy young volunteers participated in the study. Brain potentials were recorded from the scalp and time-locked to the onsets of saccades and REMs during a visually triggered saccade task and natural nocturnal sleep. In wakefulness, presaccadic positivity (PSP) appeared at centro-parietal sites starting about 150 ms before saccades. In REM sleep, no PSP was found but a slow negative potential (pre-REM negativity: PRN) appeared at the prefrontal sites. The findings suggest that the generation of REMs does not involve the cortical process reflected in the PSP but is associated with a different neural process reflected in the PRN.     

Brain potentials associated with the onset and offset of rapid eye movement (REM) during REM sleep

The relationship between dreaming and rapid eye movements (REM) during REM sleep is still controversial. This study records the brain potentials time-locked to the onset and offset of REM in 11 healthy young volunteers. Before the onset of REM, no presaccadic readiness potential was found. Conversely, two positive potentials (P1 and P2) appeared following the offset of REM. The latter potentials were dominant in the parieto-occipital area. These findings suggest that REM is initiated without preparation but elicits some information-processing activities that were speculated to occur in the cortical visual area. The data support the activation-synthesis or association hypothesis of dreaming rather than the scanning hypothesis.     

Characteristics of rapid eye movement production during REM sleep in man: organization and rhythmicity

The purpose of this study was to verify statistically the existence of certain characteristics of rapid eye movement (REM) production during REM sleep: organization and rhythmicity. REM data were collected intermittently, over a period of 20 consecutive nights, from 6 normal adult subjects of both sexes. Results concerning the organization of REM production revealed the presence of 3 evolving slow trends: quadratic, linear and quasi-sinusoidal. The occurrence of a given trend type was not related to subject, night, time of night or length of REM sleep phase being analysed. Results of the analysis showed that it is possible for a series of REMs to contain one, two or more statistically significant rhythmic periods, or no significant rhythmic period. The rhythmic periods that were detected ranged from 1 to 21 min, and no predominant periods were present. As in the case of the slow trends, the occurrence of a given rhythmic period was not dependent on subject, night, time of night or length of the REM sleep phase.     

Human cerebral potentials associated with REM sleep rapid eye movements: links to PGO waves and waking potentials

Eye movement triggered averaging and topographic display techniques indicate the presence of parieto-occipital potentials that precede the rapid eye movements of human REM sleep. Since these potentials have strong similarities with PGO waves in animals, including lateralization according to eye movement (EM) direction, and with waking EM-antecedent potentials in man, this suggests that PGO-like activity both exists in man, and may be functionally related to EM-antecedent potentials in waking. The ability to detect such central potentials opens the possibility of studying REM sleep central physiological structure in a variety of normal and pathological conditions in humans.     

Electrophysiological evidence for dreaming: human cerebral potentials associated with rapid eye movement during REM sleep

In order to examine the relationship between rapid eye movement (REM) during REM sleep and dreaming, scalp EEGs (Fz, Cz, Pz and Oz) of 4 normal human subjects, time-locked to REM onset, to saccade onset toward fixation targets and to saccade onset in total darkness, were averaged. The results include the following: Three positive potentials were associated with REM: a sharp potential in the parieto-occipital area just before REM onset; a large, slow potential in the vertex area 140-180 msec after REM onset; and a potential in the occipital area 210-280 msec after REM onset. Three positive potentials, one being the so-called EM-antecedent potential and the others being the lambda response, were associated with the waking saccades toward targets: a sharp potential in the parieto-occipital area just before the saccade onset and two potentials in the occipital area with latencies of 140-150 and 260-310 msec from the saccade onset. Only the EM-antecedent potential appearing just before saccade onset was found in association with saccades in total darkness. The similarities between the 3 positive potentials during REM sleep and the lambda response during wakefulness, and the relationship between those potentials and dreaming, are discussed in terms of the neural processes occurring during REM sleep.     

Tonic and phasic components of eye movements during REM sleep in the rat

Phasic oculomotor activity is one of the features identifying rapid eye movement (REM) sleep. Recently, it has been shown in cats that, despite bursts of complex two-component rapid eye movements, the eyes tend to maintain a nasal and downward rotation during REM sleep. Although the function of eye movements during sleep remains elusive, it is important to know whether the characteristics of eye movements during sleep are species-specific in mammals. In this work, quantitative characteristics of eye movements, recorded by the scleral search coil technique, were studied during wakefulness and sleep in rats. During wakefulness, rats performed conjugated saccades at a very low rate and some eye movements associated to blinking and gnawing. Throughout non-REM sleep, eye movements were slow, mostly unconjugated and the eyes maintained a divergence in the horizontal plane. The beginning of REM sleep was characterized by a convergence and downward rotation of the eyes, which tended to persist until the end of REM sleep. Rapid eye movements, isolated and monocular at the beginning, became complex and organized in high-frequency bursts. These results demonstrate that, despite the difference in extraocular anatomy and visuomotor strategies between frontal- and lateral-eyed species, eye movements during REM sleep in rats are very similar to those described in cats. This suggests that the mechanisms generating eye movements during REM sleep are largely conserved in mammals.     

Neural generators of brain potentials before rapid eye movements during human REM sleep: a study using sLORETA

OBJECTIVE: Brain activity preceding rapid eye movements (REM) during human REM sleep has remained poorly understood. Slow negative brain potential (pre-REM negativity) appears before REMs. Current sources of this potential were investigated to identify brain activity immediately preceding REMs. METHODS: In this study, 22 young healthy volunteers (20-25 years old) participated. Polysomnograms were recorded during normal nocturnal sleep. Brain potentials between 200ms before and 50ms after the onset of REMs and pseudo-triggers (3000ms before the onset of REMs) were averaged. Standardized low-resolution brain electromagnetic tomography (sLORETA) was used to estimate current sources of pre-REM negativity. RESULTS: Pre-REM negativity appeared with the maximal amplitude at right prefrontal sites immediately before REMs. However, this negativity did not appear before pseudo-triggers. Current sources of the pre-REM negativity were estimated in the ventromedial prefrontal cortex, uncus, insula, anterior cingulated cortex, basal forebrain, parahippocampal gyrus, premotor cortex and frontal eye field. CONCLUSIONS: The pre-REM negativity reflects brain activity coupled with the occurrence of REMs. Results of this study suggest that emotion, memory, and motor-related brain activity might occur before REMs. SIGNIFICANCE: Pre-REM negativity is expected to be a psychophysiological index for elucidating functions of REM sleep.     

Electrocorticography of waves associated with eye movements in man during wakefulness.

Waves associated with horizontal saccadic eye movements were recorded from cortical occipital areas through multilead intracerebral electrodes implanted for a few days in 6 drug-resistant epileptic patients in order to localize epileptogenic foci. The waves were studied statistically when the EEG activity was not disturbed by interictal discharges. Cortical occipital waves related to free eye movements while scanning complex material started at the end of the eye movement, later in fact than the corresponding scalp parieto-occipital phenomena. The amplitude of the cortical waves increased with the complexity of the external field (contrasts having no marked effect) and was reduced in an unpatterned field and in dim light. Waves persisted in darkness. Their amplitude was independent of the size of the eye movement. The latency of the waves, calculated from the onset of eye movement, increased with the size of the movement, the complexity of the external field and also in darkness. Imposed eye movements induced cortical waves of larger amplitude and shorter latency and anticipatory potential changes beginning before onset of the eye movement. Waves related to eye movements differed from blinks and from responses to several types of light stimulation more strikingly in cortical records than in those from the scalp. These findings are discussed in relation to lambda waves, activation waves and eye movement potentials, expectancy waves and premotor potentials, and to the phenomena of perceptual blanks preceding normal perception after fixation of gaze. The importance of the subject's attention is emphasized.     

ACTH activates rapid eye movement-related phasic inhibition during REM sleep in patients with infantile spasms

OBJECTIVES: Phasic inhibition index (PII) is the rate of the simultaneous occurrence of phasic chin muscle activity (PCMA) and rapid eye movement bursts during rapid-eye-movement sleep (REMS). In naive patients with infantile spasms (IS), the PII value was found to reflect their prognosis. We studied the effects of adrenocorticotropic hormone (ACTH) on REMS components including PII in IS. METHODS: REMS parameters were examined in 18 IS patients before and after ACTH treatment. The effects of corticosteroids (CSs) were examined in 3 patients with congenital adrenal hyperplasia (CAH) and 3 with nephrotic syndrome (NS). RESULTS: ACTH decreased PII and PCMA in IS patients. In CAH patients, physiological doses of CSs corrected the increased intrinsic ACTH level and increased PII. In NS patients, therapeutic doses of CSs suppressed PCMA without affecting PII. CONCLUSION: ACTH suppressed PCMA through CSs, and reduced PII directly. ACTH was hypothesized to eliminate IS through these dual modes of action.     

Functional neuroanatomical correlates of eye movements during rapid eye movement sleep in depressed patients

In depressed patients, REM density, or the number of rapid eye movements (REMs) per minute of REM sleep, is a correlate of depression severity and clinical outcomes. We investigated the functional neuroanatomical correlates of average REM counts (RC), an automated analog of REM density, in depression. Thirteen medication-free depressed patients underwent all night polysomnography and positron emission tomography (PET) scans using [(18)F]fluoro-2-deoxy-d-glucose ([(18)F] FDG) during REM sleep. Regression analyses were conducted with Statistical Parametric Mapping (SPM-99). Average RC significantly and positively correlated with relative regional cerebral metabolic rate of glucose (rCMRglc) bilaterally in the striate cortex, the posterior parietal cortices, and in the medial and ventrolateral prefrontal cortices. Average RC were negatively correlated with rCMRglc in areas corresponding bilaterally to the lateral occipital cortex, cuneus, temporal cortices, and parahippocampal gyri. The areas where average RC was positively correlated with rCMRglc appear to constitute a diffuse cortical system involved in the regulation of emotion-induced arousal. The observed pattern of correlations suggests that average RC may be a marker of hypofrontality during REM sleep in depressed patients.     

Functional neuroanatomical correlates of eye movements during rapid eye movement sleep in depressed patients

In depressed patients, REM density, or the number of rapid eye movements (REMs) per minute of REM sleep, is a correlate of depression severity and clinical outcomes. We investigated the functional neuroanatomical correlates of average REM counts (RC), an automated analog of REM density, in depression. Thirteen medication-free depressed patients underwent all night polysomnography and positron emission tomography (PET) scans using [¹⁸F]fluoro-2-deoxy- -glucose ([¹⁸F] FDG) during REM sleep. Regression analyses were conducted with Statistical Parametric Mapping (SPM-99). Average RC significantly and positively correlated with relative regional cerebral metabolic rate of glucose (rCMRglc) bilaterally in the striate cortex, the posterior parietal cortices, and in the medial and ventrolateral prefrontal cortices. Average RC were negatively correlated with rCMRglc in areas corresponding bilaterally to the lateral occipital cortex, cuneus, temporal cortices, and parahippocampal gyri. The areas where average RC was positively correlated with rCMRglc appear to constitute a diffuse cortical system involved in the regulation of emotion-induced arousal. The observed pattern of correlations suggests that average RC may be a marker of hypofrontality during REM sleep in depressed patients.     

Density of rapid eye movements during active sleep in preterm newborn infants

Rapid eye movement (REM) density has been helpful as a reliable index of phasic eye movements activity during REM (active) sleep in adults. We evaluated this index in 28 newborns, at 34 to 39 weeks of conceptional age (CA). The 5 hours polysomnographic recording during sleep included electroencephalogram, electrooculogram, electrocardiogram, pneumogram, nasal thermistor for detecting airflow, and continuous oxygen saturation (tcPO2) monitoring. REM density was measured by two distinct criteria: REM density as the duration of phasic eye movements in relation to REM periods (REMP). Such index varied from 10.6 to 14.1% and was higher in the 36-37 weeks CA group. REM density was calculated as a percentage of 10-second epochs of REM sleep in which phasic eye movements occurred. This criterion confirmed the narrow range of such index in this age bracket (39.9-44.6%), was higher in the first REMP and in the 36-37 weeks CA group. Our data suggest that REM density is a consistent phasic REM sleep feature in preterm newborns with levels close to the adult population, in spite of the gradual decrease of REM sleep duration with age. Higher indices were also found in the first REMP and in the 36-37 weeks CA group by both methods.