Blackwell Publishing AsiaMelbourne, AustraliaSBRSleep and Biological Rhythms1446-92352005 Japanese Society of Sleep ResearchFebruary 200641105110Original ArticleREM sleep EEG patternM Takahara et al.
Sleep and Biological Rhythms 2006; 4: 105–110
doi:10.1111/j.1479-8425.2006.00201.x
ORIGINAL ARTICLE
REM sleep EEG pattern: Examination by a new EEG scoring system for REM sleep period Madoka TAKAHARA,1,2 Sakon KANAYAMA,1 Hiroshi NITTONO1 and Tadao HORI1 1
Department of Behavioral Sciences, Faculty of Integrated Arts and Sciences, Hiroshima University, HigashiHiroshima and 2Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo, Japan
Abstract The pattern of rapid eye movement (REM) sleep was examined using a new scoring system for electroencephalogram (EEG) stages. An all-night polysomnogram (PSG) was recorded from 12 young healthy volunteers. First, all the data were scored according to the standard criteria of Rechtschaffen and Kales’ A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects (1968), and epochs of typical REM sleep were collected. The extracted data were then re-scored for each 5 s using the criteria of seven EEG stages of REM sleep: (1) alpha wave, train; (2) alpha wave, intermittent A; (3) alpha wave, intermittent B; (4) EEG flattening; (5) theta wave; (6) sawtooth wave; and (7) movement time. The results showed that the EEG flattening (4) and theta wave stages (5) occupied 92.7% of the epochs of REM sleep. The most frequent transition pattern was also between these two stages (71.1%), and these stages rarely transitioned to other stages. The number of stage continuations within 2 epochs (10 s) was largest in EEG stage 4, and those in stage 5 followed it (64.5% and 54.2%, respectively). EEG stages 4 and 5 sometimes lasted for more than 13 epochs (over 1 min). The number of stages containing sawtooth waves was less than expected, and was more frequent at the beginning than at the end of REM sleep. The distinguishing feature of the REM sleep EEG pattern was the stability of the stages of EEG flattening and theta wave, compared with the sleep onset period EEG pattern.
Key words: REM sleep period, EEG stage, theta wave, EEG flattening, sawtooth wave, alpha wave.
INTRODUCTION Rapid eye movement (REM) sleep is defined by the concomitant occurrence of relatively low voltage, mixed frequency electroencephalogram (EEG) activity and episodic rapid eye movements.1 The EEG pattern resembles sleep stage 1, except that vertex sharp waves are not prominent in the REM stage. The EEG activities specific
Correspondence: Dr Tadao Hori, Department of Behavioral Sciences, Faculty of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima 7398521, Japan. Email:
[email protected] Accepted for publication 8 November 2005.
© 2006 The Authors Journal compilation © 2006 Japanese Society of Sleep Research
to REM sleep are the theta wave, the sawtooth wave,2–6 and the alpha wave.7–10 The theta wave is characterized by a frequency between 4 and 7 Hz and is dominant in central sites. The sawtooth wave, the EEG activity specific to REM sleep, is also dominant in the central area, and resembles the theta wave. However, the definition of the sawtooth wave varies across studies. Sato et al.5 defined it as a frequency between 2 and 5 Hz, amplitudes of 20–100 µV, and more than three waves. Bursts of alpha wave activity (frequency between 8 and 13 Hz and dominant in the occipital site) are also observed in REM sleep, and the frequency is generally slower than during wakefulness. Little is known about the pattern of occurrence or transition of these characteristic EEG activities during
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Procedure After an adaptation night, an all-night polysomnogram (PSG) was recorded. An EEG was obtained from 19 electrode sites (Fp1, Fp2, F7, F8, Fz, F3, F4, T3, T4, Cz, C3, C4, T5, T6, Pz, P3, P4, O1, O2) standardized to linked earlobes. Vertical and horizontal electrooculograms (EOG) and submental electromyogram (EMG) were also recorded. Time constants were 0.3 s for EEG and EOG and 0.003 s for EMG. The data were digitized at 1 kHz. The high cut filter was set at 30 Hz. All electrode impedances were set below 5 kΩ. Figure 1 Typical electroencephalogram (EEG) patterns during rapid eye movement (REM) sleep.
REM sleep. The standardized criteria1 calculate scores for each 20–30 s. However, the REM sleep EEG should be more finely scored to take into account the transience of EEG activity. So we developed a new scoring system of EEG stages for the REM sleep period (Fig. 1) based on Hori’s nine EEG stages of the sleep onset period,11 because the EEG features of REM sleep resemble those of the sleep onset period. The major modification was that EEG stages 6–9 of Hori’s nine sleep onset stages including vertex sharp waves and spindles were excluded since these stages were not appropriate for REM sleep. Instead, an EEG stage for sawtooth wave activity was added. The purpose of this study was to examine the EEG changes during REM sleep using the newly developed seven EEG stages.
METHOD Participants Twelve young healthy students (six women and six men) volunteered to participate in this study (mean age = 22.7 ± 1.87 years). All participants reported that they were good sleepers, right-handed, non-smokers, and free from medication. Participants were instructed to wake up at their usual time and abstain from alcohol, caffeine or other medicines, excessive exercise and taking naps on the experimental days. Prior to the experimental days, each participant was instructed about the purpose and the procedure of this study, then they signed a consent form. They were free to discontinue the EEG recording or their participation in the study at any time.
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Analysis Polysomnogram recordings were scored according to the international standard criteria1 and its supplements and amendments12 for each 30 s. Among the periods scored as REM sleep, those that lasted for more than 5 min were further analyzed. EEG stage scoring was done every 5 s for the Cz site, referring to the O2 recording in accordance with the sleep onset period scoring of Hori et al.11 The periods that transitioned to another sleep stage during a REM sleep period (and then back to REM sleep again) were excluded from this analysis. Then the typical REM sleep periods were extracted. The scoring definitions are given below. EEG stage 1 − Alpha wave, train: epoch composed of a train of alpha activity with a minimum amplitude of 20 µV. EEG stage 2 − Alpha wave, intermittent A: epoch composed of a train of at least 50% alpha activity with a minimum amplitude of 20 µV. EEG stage 3 − Alpha wave, intermittent B: epoch composed of a train of less than 50% alpha activity with a minimum amplitude of 20 µV. EEG stage 4 − EEG flattening: epoch composed of suppressed waves of <20 µV. EEG stage 5 − Theta wave: epoch composed of low-voltage theta waves (20 µV < θ < 50 µV). EEG stage 5-STW − Sawtooth waves: epoch contained waves that looked like a “sawtooth” pattern. Based on the definition of Sato et al. (1997),5 at least three consecutive waves had amplitudes ranging between 20 and 100 µV, and frequencies of 2–5 Hz. MT − Movement time: epoch composed of a train with at least a 50% immediate increase of amplitudes in the EEG and EOG tracings, indicating muscle tension and/or artifacts associated with movement of the participant. The frequency of each EEG stage was tested by a repeated measures analysis of variance (ANOVA). The
© 2006 The Authors Journal compilation © 2006 Japanese Society of Sleep Research
REM sleep EEG pattern
reported significant results were corrected using the Greenhouse-Geisser ε correction. All the posthoc comparisons were done according to Tukey’s honest significant difference (HSD) test. For the comparison of the frequency of each EEG stage in the first and the last 5 min of the REM period, a paired t-test was used. Statistical significance was based on the 0.05 level.
and 5 occupied the 92.7% of all REM epochs. EEG stage 5 occurred more often than EEG stage 4 (P < 0.01). The number of EEG stage 5 (theta wave), following stage 4 (EEG flattening), was larger than the other stages (all P < 0.001). The number of epochs with sawtooth waves and alpha waves was small (1.6%). Table 2 shows the pattern of EEG stage changes during REM sleep. Each upper and lower cell represents the
RESULTS The REM episodes were extracted from each participant’s data. The EEG data from one participant was excluded from a further analysis because it showed constant high-voltage alpha waves throughout the REM sleep period. Therefore usable data was collected from 11 participants. A total of 23 episodes of REM sleep were analyzed, lasting an average of 1561.3 ± 260.27 s. Table 1 shows the number of epochs and the occurrence ratio of the scored EEG stages. The ANOVA revealed a significant main effect of EEG stage (F = 29.03, d.f. = 6.60, ε = 0.24, P < 0.001). EEG stages 4
Table 1 Number of epochs and occurrence ratio for each electroencephalogram (EEG) stage EEG stage
Number of epochs
Occurrence ratio (%)
1 2 3 4 5 5-STW MT Total
5 38 139 2052 3398 96 153 5881
0.1 0.6 2.4 34.9 57.8 1.6 2.6 100.0
Table 2 Number of stage changes Precedent EEG stages (This stage precedes…)
Subsequent EEG stages (…is followed by this stage)
1 (%) 1 (%) (%) 2 (%) (%) 3 (%) (%) 4 (%) (%) 5 (%) (%) 5-STW (%) (%) MT (%) Total
2.9 1 25.0 1.1 1 25.0 0.1 1 25.0 0.0 0 0.0 0.0 0 0.0 1.1 1 25.0 0.2 4 100.0
2
3
4
5
5-STW
MT
Total
20.0 1 2.9
40.0 2 2.2 34.3 12 13.0
0.0 0 0.0 31.4 11 1.4 33.7 31 4.0
20.0 1 0.1 25.7 9 1.1 47.8 44 5.2 86.8 692 82.5
0.0 0 0.0 0.0 0 0.0 1.1 1 1.2 2.0 16 19.5 7.9 64 78.0
20.0 1 1.2 5.7 2 2.5 6.5 6 7.4 6.1 49 60.5 2.8 23 28.4 0.0 0 0.0
100.0 5 0.3 100.0 35 1.8 100.0 92 4.8 100.0 797 41.7 100.0 814 42.6 100.0 80 4.2 100.0 90 4.7 100.0 1913 100.0
9.8 9 25.7 1.8 14 40.0 1.2 10 28.6 0.0 0 0.0 1.1 1 2.9 1.8 35 100.0
3.1 25 27.2 5.9 48 52.2 2.5 2 2.2 3.3 3 3.3 4.8 92 100.0
© 2006 The Authors Journal compilation © 2006 Japanese Society of Sleep Research
82.2 669 85.8 28.8 23 2.9 51.1 46 5.9 40.8 780 100.0
68.8 55 6.6 42.2 38 4.5 43.9 839 100.0
1.1 1 1.2 4.3 82 100.0
4.2 81 100.0
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5-STW occurred more frequently in the first 5 min than the last 5 min of REM sleep periods (P < 0.05, t = 2.89, d.f. = 9).
DISCUSSION REM sleep was characterized by EEG stage 4 (EEG flattening) and EEG stage 5 (theta wave). EEG stage changes were mostly observed between these two stages. Transitions infrequently occurred from these two stages to the other stages of alpha waves or sawtooth waves. The number of continuous epochs was largest for EEG stages 4 and 5, which lasted more than 13 epochs (over 1 min). The other stages occurred with short durations and then transitioned to stages 4 or 5. Body movements also occurred in EEG stages 4 and 5, and were often followed by stage 4. Many similarities in EEG activity between the sleep onset period and REM sleep have been reported for the low-voltage pattern and the transition changes. Some reports classified the EEG activities during the sleep onset period into EEG stages, and discussed the pattern of occurrence, durations, transitions, and association with hypnagogic imagery.2,13–15 Tanaka et al.14 60
50
Number of epochs in 5 min
frequency for the preceding EEG stages and for the subsequent EEG stages, respectively. EEG stage 4 was preceded by EEG stage 5 82.5% of the time, and was followed by EEG stage 5 82.2% of the time. EEG stage 5 was preceded by EEG stage 4 85.8% of the time, and was followed by EEG stage 4 86.8% of the time. Thus, changes between EEG stages 4 and 5 were the most frequent patterns in REM sleep. EEG stage 5-STW was preceded by EEG stage 5 68.8% of the time, and followed by EEG stage 4 28.8% of the time. EEG stage 5-STW was followed by EEG stage 5 78.0%, of the time and followed EEG stage 4 19.5% of the time. EEG stages 1 and 2 were preceded and followed by all the EEG stages except stage 5-STW. EEG stage 3 was preceded and followed by EEG stage 5 with frequencies of 47.8% and 52.2%, respectively. The stage of movement time was preceded by EEG stage 4 51.1% of the time, and followed by EEG stage 5 42.2% of the time. MT was followed by EEG stage 4 60.5% of the time. Table 3 shows the number of continuous epochs for each EEG stage. The most frequent stage duration for one occurrence was about 10 s of EEG stage 4, followed by EEG stage 5. These stages had more continuous epochs than other stages. Only stages 4 and 5 had EEG stages lasting seven or more epochs in time (35 s). EEG stages 1, 2 and 5-STW were sustained for no more than 10 s. EEG stage 3 had some continuous epochs lasting more than 10 s. Figure 2 shows the mean number of epochs for the seven EEG stages in the first and the last 5 min of each REM sleep period. Data from one participant was excluded from this analysis because of an insufficient number of epochs in the first 5 min of the REM period. EEG stage 4 tended to occur more in the last 5 min than the first 5 min (P < 0.10, t = 2.06, d.f. = 9). EEG stage
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† 30
20
Table 3 Number of continuous epochs for each EEG stage 10
Number of continuous epochs EEG stages 1 2 3 4 5 5-STW MT Total
108
1–2
*
3–4 5–6 7–8 9–10 11–12 ≥13
5 – – 34 – – 90 8 2 557 157 77 411 156 78 64 – – 80 11 – 1241 332 157
– – – 38 35 – – 73
– – – 18 21 – – 39
– – – 5 20 – – 25
– – – 11 37 – – 48
0
1
2
3
4
5
5-STW MT
EEG stages
Figure 2 Mean number of epochs of each electrencephalogram (EEG) stage within () the first 5 min and () the last 5 min of all rapid eye movement (REM) sleep periods (N = 10). *,†Statistically significant difference between the first and the last 5 min of REM sleep periods at P < 0.05 and P < 0.1, respectively. STW, sawtooth; MT, movement time.
© 2006 The Authors Journal compilation © 2006 Japanese Society of Sleep Research
REM sleep EEG pattern
investigated the EEG stages during the sleep onset period and found that there was a sequential order of occurrence of nine EEG stages. A similar ordered pattern was also observed in a previous study, which investigated auditory stimulation.13 However, we observed no particular order of EEG stages during REM sleep. The EEG pattern for stable episodes of REM sleep was anchored by the relatively highvoltage theta waves (EEG stage 5) or the low-voltage “flattening” waves (EEG stage 4), and transitioned back and forth between these two stages. The EEG pattern in REM sleep showed no specific pattern of progression, which is different from the progression found for the sleep onset period. The relation between theta oscillation and REM sleep has been reported before.16 However, the EEG flattening stage is less well documented and understood. In the sleep onset period, EEG stage 4 was infrequent and was a transient phenomenon.14 How to interpret this stage is unclear. Another question is whether there is any difference in meaning or in function between the EEG flattening stage in REM sleep and the sleep onset period. Spectrum analysis or topographic analysis may shed additional light on the meaning or function of EEG stage 4 in REM sleep. The present study also investigated the differences in EEG patterns between the first and the last 5 min of REM sleep episodes. A significant difference was obtained for EEG stage 5-STW (sawtooth wave), which occurred much more often in the first 5 min compared with the last 5 min of REM sleep (1.9 vs. 1.0). EEG stage 4 (EEG flattening) was slightly more frequent in the last 5 min compared with the first 5 min of REM sleep (17.7 vs. 15.3). The transition from NREM sleep to REM sleep occurs in the following order: diminution of muscle tension, occurrence of the sawtooth wave, and occurrence of rapid eye movements.6,17 This suggests that the sawtooth waves were observed before REM sleep started, and were associated with the beginning or stabilization of REM sleep. Thus, EEG stage 5-STW was more frequently observed in the first 5 min of REM sleep. Studies that used a spectrum analysis across NREM and REM sleep transitions18,19 showed that the power of delta- and sigma-bands diminished and the power of beta- and gamma-bands increased immediately at the beginning of REM sleep. In contrast, there was a gradual increase in the delta- and sigma-bands’ power and a gradual decrease in the beta- and gamma-bands’ power at the end of the REM sleep period. Thus, there was no immediate change in power related to the end of REM sleep. This suggests that REM sleep terminates with a relatively moderate transition to the other sleep stage.
© 2006 The Authors Journal compilation © 2006 Japanese Society of Sleep Research
The tendency for the more frequent occurrence of EEG stage 4 in the last 5 min of REM sleep was due to the low-voltage EEG pattern that preceded the spindles or K-complexes of sleep stage 2. The present study investigated the stable state of REM sleep to determine the typical EEG pattern. However, it is known that REM sleep sometimes breaks into another sleep stage. Further investigation is needed examining the unstable state of REM sleep using the EEG stage scoring used in this study to increase knowledge about the features of all types of REM sleep periods. Also, REM sleep has been suggested to be sensitive to some life events. How the first night effect20 or the learning process21 influences the EEG structure and stability of REM sleep are other interesting issues for future research. In summary, the new EEG stage scoring system for the REM sleep period, partly using Hori’s nine EEG stages for the sleep onset period, revealed features of the all-REM sleep EEG pattern. The results are basically consistent with the framework of the EEG pattern of sleep stage 1 suggested by Rechtshaffen and Kales in 19681. We found differences in the transition pattern of the time course between stage 1 and stage 1-REM periods.
ACKNOWLEDGMENTS This study was supported by a Grant-in-Aid of Japan Society for the Promotion of Science (JSPS) (No. 17005268), and a Grant-in-Aid for Scientific Research (C) (No. 17605008).
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