| | Temporal coupling of rapid eye movements and cerebral activities during REM sleepAccepted 11 October 2008. Abstract 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. 1. Introduction  During rapid eye movement (REM) sleep, the experience of dreaming is more frequent, more vivid, and clearer than in non-REM sleep (Dement and Kleitman, 1957). Recently, it has been suggested that brain functioning during REM sleep may related to the characteristic form of dreaming that occurs during REM sleep (Hobson and Stickgold, 1994). The relationship between dreaming and rapid eye movements has interested researchers since the initial discovery that such movements occur during sleep (Aserinsky and Kleitman, 1953, Dement and Kleitman, 1957, Hobson et al., 2000, Hobson and McCarley, 1977, Hobson and Stickgold, 1994, Okuma, 1992). In the present study, we investigated the brain activities that occur during REM sleep by examining rapid eye movements. Saccades (during wakefulness) are rapid ocular movements between visual fixations. With averaged EEGs time-locked to saccades, a positive cerebral potential called the lambda response was observed at occipital sites (Scott and Bickford, 1967, Scott et al., 1967, Scott, 1967, Kurtzberg and Vaughan, 1977, Yagi, 1979). The lambda response is not observed when participants are in a dark room or when they close their eyes (Scott and Bickford, 1967, Scott et al., 1967, Scott, 1967, Kurtzberg and Vaughan, 1977); therefore, it has been proposed that this response is indicative of the cortical visual information processing that results from the input of the visual image across the retina (Barlow and Cignek, 1969, Ebersole and Galambos, 1973). Previous studies have shown that the rapid eye movements that occur during REM sleep also elicit similar brain potentials over the occipital regions, again dubbed the lambda-like response (Miyauchi et al., 1987, Miyauchi et al., 1990, Niiyama et al., 1988, Ogawa et al., 2005, Ogawa et al., 2006). This finding suggests that a kind of visual information processing may occur during REM sleep, similar to that which occurs during wakefulness. The lambda response during wakefulness is associated with the offset of the saccades (Yagi, 1979). However, the lambda-like response during REM sleep has been reported associated with both the onset (Miyauchi et al., 1987, Miyauchi et al., 1990, Niiyama et al., 1988) and the offset (Ogawa et al., 2005, Ogawa et al., 2006) of rapid eye movements. If the function of the lambda-like response during REM sleep is the same as that of the lambda response during wakefulness, the response should start at the offset of rapid eye movements. Therefore, even if the sizes of eye movements were to differ, the duration of lambda-like responses time-locked to the offset of the rapid eye movements should be constant. In this study, we examined the temporal relationship between latencies of the lambda-like response and four sizes of rapid eye movements. The eye movement’s size refers to how far the participant’s eyes move across the visual field. 2. Method 2.1. Participants Nine healthy university students (5 men and 4 women, mean age=22.9 years old) participated in the study. They had normal or corrected-to-normal vision. They did not consume caffeine or alcohol on the days of the experiment. They all gave written informed consent to participate in the study. 2.2. Procedure After an adaptation night, participants spent two or three non-consecutive nights (mean=2.1 nights) in the sleep laboratory, until enough trials were obtained from each participant to average electroencephalogram (EEG) tracings during REM sleep. On each experimental day, participants came to the laboratory 4h before their sleep session. Before lying on a bed, the participants sat in a comfortable chair in a non-illuminated room, with their heads fixed in a chinrest. A black stimulus board was placed 60cm in front of each participants’ eyes. In the center of the board, a fixation LED was always placed between two stimulus LEDs. The stimulus LEDs were randomly presented horizontally, at either the right or left side of the fixation LED at a random pace (2–3s). The two stimuli LEDs were placed 5°, 10°, 15° or 20° away from the fixation LED. The size of all LEDs was 1°. The participants were instructed to shift their gaze as quickly as possible from the fixation to the stimulus, whenever it was presented. Each trial consisted of 40 saccades and took 1min. Each participant completed three trials for each size of display, in a randomized order. After the waking session, participants were asked to lie on the bed and fall asleep. The polysomnogram was recorded during nocturnal sleep. 2.3. Polysomnogram recordings The EEG was recorded at 26 scalp sites (Fp1, Fp2, F3, F4, P3, P4, O1, O2, F7, F8, T3, T4, T5, T6, F9, F10, P9, P10, Fpz, Fz, Cz, Pz, POz, Oz, A1 and A2 according to the international 10% system; American Encephalographic Society, 1991), referenced to an average of C3–C4 with a time constant of 5s. Horizontal and vertical electrooculograms (EOGs) were recorded from the outer canthi of both eyes, and from above and below the left eye with a time constant of 5s. The horizontal EOG was also recorded with a time constant of 0.03s for picking the onsets of saccades and rapid eye movements. The electromyogram (EMG) was recorded from the mentalis muscles with a time constant of 0.03s. Electrode impedance was below 5kΩ. The entire recording was made via Ag/AgCl electrodes affixed to the scalp with collodion or surgical tape. A high-cut filter of 100Hz was used. The sampling rate was 1000Hz. The EEG was re-referenced to linked earlobes offline. 2.4. Data reduction Only the data recorded during the epochs scored as ‘Stage REM’ according to the standard sleep stage criteria were analyzed (Rechtschaffen and Kales, 1968, Sleep Computing Committee of The Japanese Society of Sleep Research Society (JSSR), 2001). Rapid eye movements during REM sleep were classified into four sizes (⩾5°, 6–10°, 11–15°, and 16–20°), individually based on the horizontal EOG amplitudes for the four saccade sizes measured during wakefulness. To detect the onset and offset of eye movements, the following procedure was used. For rapid eye movements during REM sleep, we identified a recording epoch in which the amplitude of the horizontal EOG with a time constant of 0.03s that exceeded a predetermined level. This level was determined (for each participant) as being 20% of the mean EOG amplitude from the saccades during wakefulness. Second, rapid eye movements were classified into four sizes. After that, the onset and offset of both saccades and rapid eye movements were determined by visual inspection on a computer monitor. For the lambda and lambda-like responses, the EEGs from 400ms before to 400ms after the onset and offset of eye movements were averaged separately for onset and offset, for the four eye movement sizes. The baseline was aligned with the mean amplitude of the first 300ms period. Identical numbers of EEG epochs for towards the right and towards the left eye movements were averaged. The lambda and lambda-like components were identified as the positive peaks about 80ms after the onset and offset of eye movements. Epochs containing more than two eye movements or large vertical EOG artifacts (over 80μV in wakefulness; over 120μV in sleep) during 1s after the offset of eye movements were removed from the analyses. 2.5. Statistical analysis We conducted separate nonparametric statistical analysis (Friedman test) on the data of the three oculomotor variables (the duration, velocity and acceleration) for both saccades and rapid eye movements (total of 6 tests). We also conducted Wilcoxon signed rank test to compare oculomotor measures between saccades and rapid eye movements. To examine the temporal relationship between eye movement size and latencies of the lambda and lambda-like response, latencies were compared using nonparametric statistics (Friedman test) for four eye movement sizes during wakefulness and REM sleep, separately. The significance level was set at p<0.05 for all comparisons. Post hoc tests were also performed by Wilcoxon signed rank test. The significance level was adjusted using the Bonferroni procedure. 3. Results 3.1. Oculomotor measures during wakefulness and REM seep During wakefulness, 480 saccades were recorded for each participant. The mean number of rapid eye movements during REM sleep was 225.3 (SD=19.4) per night for each participant. Table 1 shows the mean duration, velocity and acceleration of saccades during wakefulness, as well as these values for rapid eye movements during REM sleep. The Friedman test with a factor of the eye movement size revealed a significant main effect for the saccade duration (X2=25.13, df=3, p<0.01). The Friedman test for the rapid eye movements duration also indicated a main effect of the eye movement size (X2=25.93, df=3, p<0.01). Durations of saccades and rapid eye movements were significantly longer as the size of the eye movements increased. | | |  | Size (°) | Saccade | REM | |
|---|
| Duration | Velocity | Acceleration | Duration | Velocity | Acceleration | |
|---|
| 5 | 38.3 (2.0) | 133.2 (6.0) | 3607.0 (303.8) | 60.9 (2.6) | 64.2 (4.1) | 1084.9 (100.6) | | | 10 | 48.7 (1.5) | 206.7 (6.1) | 4303.7 (246.0) | 74.1 (1.3) | 106.3 (3.4) | 1442.6 (66.2) | | | 15 | 61.7 (2.3) | 246.1 (9.7) | 4087.3 (333.5) | 101.5 (3.6) | 120.1 (5.1) | 1210.0 (98.5) | | | 20 | 70.6 (2.4) | 286.0 (9.1) | 4121.9 (252.1) | 129.0 (5.9) | 131.0 (7.7) | 1045.2 (96.9) | | | X2 | 25.13∗∗ | 25.93∗∗ | 8.60∗ | 25.93∗∗ | 23.13∗∗ | 15.53∗∗ | | | | |
The Friedman test with a factor of the eye movement size indicated significant main effect for the saccade velocity (X2=25.93, df=3, p<0.01) and the rapid eye movement velocity (X2=23.13, df=3, p<0.01). Velocities of saccades and rapid eye movements were significantly faster as the size of the eye movements increased. The Friedman test for the acceleration showed significant main effects of the eye movement size for saccades (X2=8.60, df=3, p<0.05) and rapid eye movements (X2=15.53, df=3, p<0.05). Result of post hoc comparison indicated that acceleration of rapid eye movements for the 6–10° size was significantly greater than that for ⩾5° and 16–20° (the significance level was α=0.0083). In the result of Wilcoxon signed rank test between oculomotor variables of saccades and rapid eye movements, the mean duration of rapid eye movements (91.4±2.2(SE)ms) was significantly longer than that of saccades (54.8±1.8ms), p<0.01. The mean velocity of rapid eye movements (105.4±3.8°/s) was significantly slower than that of saccades (218.0±6.5°/s), p<0.01. The mean acceleration of rapid eye movements (1195.7±64.5°/s2) was significantly smaller than that of saccades (4030.0±238.0°/s2), p<0.01. 3.2. Brain potentials time-locked to the onset of eye movements Previous studies (Ogawa et al., 2005, Ogawa et al., 2006) have indicated that the lambda response during wakefulness occurs at occipital site (Oz) and has its electrical current source in the cuneus and the ligual gyrus. In comparison to wakefulness, it has also been demonstrated that the lambda-like response during REM sleep occurs at the parietal-occipital site (POz) and has its electrical source in the precuneus of the parietal association cortex, a more parietal location, compared to the cuneus and the ligual gyrus. Therefore, in this study also, we analyzed the potentials in these areas. Fig. 1 shows the grand mean waveforms for the 9 participants, time-locked to the onset of eye movements during wakefulness (N=2668 EEG tracings) and REM sleep (N=2164 EEG tracings). The superimposed waveforms for the four eye movement sizes at Oz during wakefulness and at Cz/POz during REM sleep are also shown. The lambda response (P1: 3.0±0.6μV at Oz) and lambda-like response (P1r: 3.3±0.7μV at POz) were observed in the waveforms over the occipital regions. Table 2 shows the mean latency of the P1 and P1r. The Friedman test with a factor of eye movement size showed a significant main effect for the latency of P1 (X2=24.07, df=3, p<0.01). The latency of P1r also indicated a significant main effect of eye movement size (X2=11.00, df=3, p<0.05). | | | | Size (°) | Onset-locked | |
|---|
| Wakefulness | REM sleep | |
|---|
| P1 | P1r | |
|---|
| 5 | 152.2 (4.6) | 219.4 (8.3) | | | 10 | 155.8 (5.9) | 240.9 (7.8) | | | 15 | 174.6 (6.4) | 237.0 (3.2) | | | 20 | 212.6 (8.3) | 250.4 (7.9) | | | X2 | 24.07∗∗ | 11.00∗ | | | | |
During REM sleep, a positive potential was also observed in the waveform over the central region this potential was not observed during wakefulness. The mean peak-to-peak amplitudes of this positive potential (the positive potential minus the prior negative potential) were compared among the three sites (Fz, Cz, and Pz). The Friedman test with a factor of site showed a significant main effect for the amplitude (X2=9.56, df=2, p<0.01). Post hoc comparison showed that the amplitude was significantly larger at Cz (5.9±1.0μV) than at Fz (3.9±0.9μV) (α=0.017). Table 3 (left side) shows the mean latency of this positive potential at Cz, which time-locked to the onset of rapid eye movements. The Friedman test for the latency showed a non-significant main effect of eye movement size (X2=0.95, df=3, n.s.). The mean latency of this positive potential was 200.6±7.1ms. Fig. 2 shows the topographical maps (Current Source Density: CSD maps) of this potential. The CSD maps were drawn from the grand average waveforms using EEGFOCUS 2.1 (MEGIS Software; Munich, Germany) with the spherical spline interpolation method. This potential had its focus of CSD at the Cz. The mean amplitudes for four sizes were 2.2±1.0μV (5°), 4.1±0.9μV (10°), 8.2±2.2μV (15°) and 8.2±2.0μV (20°). The Friedman test for the amplitude showed a significant main effect of eye movement size (X2=9.61, df=3, p<0.05). The amplitudes were significantly larger as size of rapid eye movements increased (see Fig. 3). 3.3. Brain potentials time-locked to the offset of eye movements Fig. 4 shows the grand mean waveforms for the 9 participants, time-locked to the offset of eye movements during wakefulness (N=2544 EEG tracings) and REM sleep (N=2186 EEG tracings). The superimposed waveforms for the four eye movement sizes at Oz during wakefulness and at Cz/POz during REM sleep are also shown. The lambda response (P1: 2.7±0.6μV at Oz) and lambda-like response (P1r: 2.4±0.8μV and P2r: 3.0±1.0μV at POz) were observed in the waveforms over the occipital region. Table 4 shows the mean latency of the P1 and P1r/P2r. The Friedman test with a factor of eye movement size indicated a non-significant main effect for latencies of P1 (X2=0.10, df=3, n.s.), and P1r/P2r (P1r: X2=2.42, df=3, n.s., P2r: X2=2.43, df=3, n.s.). | | | | Size (°) | Offset-locked | |
|---|
| Wakefulness | REM sleep | |
|---|
| P1 | P1r | P2r | |
|---|
| 5 | 116.8 (5.3) | 62.4 (5.6) | 164.3 (4.7) | | | 10 | 115.9 (6.1) | 74.7 (6.1) | 157.7 (4.4) | | | 15 | 118.2 (8.7) | 75.9 (8.3) | 155.7 (9.8) | | | 20 | 119.6 (4.7) | 72.1 (6.1) | 165.2 (4.6) | | | X2 | 0.10 | 2.42 | 2.43 | | | | |
During REM sleep, a positive potential was also observed in the waveforms over the central region. The mean peak-to-peak amplitudes of the positive potential (the positive potential minus the prior negative potential) were compared among the three sites (Fz, Cz, and Pz). The Friedman test with a factor of site showed a significant main effect for the amplitude of the positive potential (X2=12.67, df=2, p<0.01). Post hoc comparison showed that the amplitude of the positive potential time-locked to the offset was significantly larger at Cz (4.6±0.5μV) and Pz (4.1±0.4μV) than at Fz (3.1±0.5μV) (α=0.017). Table 3 (right side) shows the mean latency of this positive potential at Cz, which time-locked to the offset of raid eye movements. The Friedman test showed a significant main effect of eye movement size for the latency of the positive potential related to the offset (X2=8.35, df=3, p<0.05). 4. Discussion 4.1. Rapid eye movements during REM sleep During REM sleep, the duration and velocity of rapid eye movements became significantly longer and faster with the increase in the size of eye movements. The relationship between the size of eye movements and velocity during REM sleep was similar to that observed during wakefulness, a finding that is consistent with previous studies (Herman et al., 1983). The durations and velocities of rapid eye movements were longer and slower than comparable values for saccades, which is also consistent with previous studies (Aserinsky et al., 1985, Fukuda et al., 1981, Ornitz et al., 1973). We also demonstrated that the acceleration of rapid eye movements became significantly faster with the increase in eye movement size, and smaller than that of saccades. Zhou and King (1997) have demonstrated that rapid eye movements during REM sleep and spontaneous saccades in darkness have similar velocity-size relationships and suggested that similar neuronal circuits might generate both types of eye movements. In this study, we used a visual stimulus for saccades during wakefulness. This stimulus could have been the reason for the faster saccades observed in this study, in comparison to rapid eye movements during REM sleep. 4.2. The lambda-like response during REM sleep During REM sleep, the mean peak latencies of the lambda-like response time-locked to the offset of rapid eye movements were constant regardless of eye movement size. This result shows that the lambda-like response is associated with the offset of rapid eye movements, as is the case during wakefulness. Our findings suggest that although there is no input of visual imagery during REM sleep, the occipital area is nevertheless activated after the termination of rapid eye movements. 4.3. The central activity during REM sleep We also found a positive potential at the central region during REM sleep. When EEGs are time-locked to the onset of rapid eye movements, this potential shows a constant latency (200ms) regardless of rapid eye movement size. This result shows that this positive potential, named “P200r”, is related to the onset of rapid eye movements. This P200r (or a similar positive potential) did not occur during wakefulness. A positive potential was also observed in previous studies of brain potentials related to rapid eye movements (Miyauchi et al., 1987, Niiyama et al., 1988). However, the exact interpretation of this potential differs across researchers. Miyauchi et al. (1987) suggested that this potential may be the primary component of the k-complex, which is typically elicited by rapid eye movements as an internal stimulus. Niiyama et al. (1988) suggested that this potential may be a P300-like potential that occurs during REM sleep in the form of a response to the visual imagery of dreaming. Previous brain imaging studies have documented high activation in the central area, which include the cingulate, amygdale and the thalamus, during REM sleep (Hong et al., 1995, Maquet et al., 1996, Nofzinger et al., 1997, Braun et al., 1998, Buchsbaum et al., 2001, Peigneux et al., 2001). A positron emission tomography (PET) study of REM sleep has reported that the number of rapid eye movements was positively correlated with the activities of the cingulated cortex (Hong et al., 1995). Wehrle et al. (2007), using functional magnetic resonance imaging (fMRI), have demonstrated that synchronized thalamocortical activity increases selectively during the phasic rapid eye movements period of REM sleep. P200r activity found in this study may be comparable to these brain activities; suggesting that these central activities occur simultaneously with the beginning of rapid eye movements during REM sleep. 5. Conclusion The main finding of our study is that during REM sleep, the P200r occurred over the central regions with the start of rapid eye movements, and the lambda-like response occurred over the occipital region after the rapid eye movements. These potentials show that there is a temporal coupling of eye movements and cerebral activities during REM sleep. This temporal coupling is a characteristic aspect of REM sleep, which suggests that the function of rapid eye movements during REM sleep is different from saccades during wakefulness. 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a Faculty of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa, Saitama, 359-1192, Japan b Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo, Japan c Japan Somnology Center, Neuropsychiatric Research Institute, Tokyo, Japan d Department of Behavioral Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, Higashi-Hiroshima, Japan e Sleep Research Institute of Fukuyama Transporting Shibuya Longevity Health Foundation, 2-5-22, Myojincho, Fukuyama, Hiroshima, 721-0961, Japan  Corresponding author. Tel./fax: +81 4 2947 6832.
PII: S1388-2457(08)01012-2 doi:10.1016/j.clinph.2008.10.006 © 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Inc. All rights reserved. | |
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