Co-occurrence of the sawtooth waves and rapid eye
movements during REM sleep
Madoka Takaharaa, Sakon Kanayamab, Tadao Horib,c
a
Research Center of Brain and Oral Science, Kanagawa Dental College, Kanagawa, Japan
Dept. of Behavioral Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima
University, Hiroshima, Japan
c
Sleep Research Institute, Fukuyama Transporting Shibuya Longevity Health Foundation, Hiroshima,
Japan
b
Correspondence: M. Takahara, Kanagawa Dental College, 82, Inaokacho, Yokosuka, Kanagawa, 238-8580, Japan. E-mail:
takaharam@kdcnet.ac.jp, phone +81 46 822 9403, fax+81 46 822 9522
Abstract. To investigate the relationship between the sawtooth waves and rapid eye movements during
REM sleep period using the EEG scoring system for every 5 seconds [Takahara et al., 2006]. Eleven
university and graduate school student volunteers participated in this study. The extracted REM sleep
periods data according to the standard criteria of Rechtschaffen & Kales (1968) by 30 seconds from
normal polysomnogram (PSG) recordings were re-scored by 5 seconds according to the EEG scoring
system for REM sleep. The occurrence rate of rapid eye movements during the 5-seconds epoch was
highest for the EEG stage 5-STW (44.8 %), in comparison to other EEG stages (20.5 % on average).
Moreover, the number of rapid eye movements within 2 minutes before and after the sawtooth waves’
epoch was the largest just in the same epoch of the sawtooth waves’ epoch. The relationship between
the sawtooth waves and rapid eye movements during REM sleep was not at random. During REM
sleep, rapid eye movements temporally had to do with the sawtooth waves. It was clarified that the
sawtooth waves not necessarily precede rapid eye movements, however, PGO processes may possibly
be related to the sawtooth waves occurrence.
Keywords: rapid eye movement (REM) sleep, sawtooth waves, EEG stages
1. Introduction
The sawtooth wave, the electroencephalogram (EEG) activity specific to rapid eye movement
(REM) sleep, indicates central dominant in the scalp area. The definition of the sawtooth wave varies
across studies. Sato et al. (1997) defined it as a frequency between 2 and 5 Hz, amplitudes of 20–100
µV, and more than three waves. 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 [Pearl et al., 2002; Hadjiyannakis et al., 1997]. This suggests that the sawtooth
waves were observed before REM sleep started, and were associated with the beginning or
stabilization of REM sleep. The EEG activities specific to REM sleep are the theta wave, the sawtooth
wave, and the alpha wave. The theta wave is also characterized by a frequency between 4 and 7 Hz and
is dominant in central sites.
Previously we revealed the pattern of occurrence or transition of these characteristic EEG activities
during REM sleep, using a new scoring system of EEG stages for the REM sleep period based on
Hori’s nine EEG stages of the sleep onset period [Takahara et al., 2006]. REM sleep was characterized
by EEG stage 4 (EEG flattening) and EEG stage 5 (theta wave). The purpose of this study was to
investigate the relationship between a new EEG stage score and REMs during REM sleep.
2. Material and Methods
2. 1. Participants
Eleven young healthy students (5 women and 6 men) volunteered to participate in this study (mean
age = 22.7 ± 1.87 years). All participants self-reported as good sleepers, right-handed, non-smokers
and free from any medication. On the experimental day, participants were instructed to wake up at
their usual time and abstain from alcohol, caffeine or other medication, exceeded exercises and taking
naps. Prior to the experimental day, each participant well-instructed about the purpose and the
procedure of this study, and then signed a consent form. They were aware that they were free to
discontinue the recording whenever they wished. The protocol was approved by the Human Ethics
Committee of the Faculty of Integrated Arts and Sciences of Hiroshima University.
2. 2. Recordings and Experimental Procedure
All night polysomnogram (PSG) was recorded after an adaptation night. Electroencephalogram
(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 reference to linked earlobes. Vertical and
horizontal electrooculograms (EOGs) and submental electromyogram (EMG) were also recorded.
Time constants were 0.3 seconds for EEG and EOG and 0.003 seconds for EMG. The data were
digitized at 1k Hz. High cut filter was set at 30 Hz. All electrode impedances were set below 5 kΩ. Part
of the present data were previously reported [Takahara et al., 2006].
2. 3. Analysis
PSG recordings were scored according to the international standard criteria [Rechtschaffen and
Kales, 1968] and its supplements and amendments [Sleep Computing Committee of the Japanese
Society of Sleep Research (JSSR), 2001] by each 30 seconds. Among the periods scored as REM
sleep, those lasted for more than 5 minutes were carried into a further analysis. EEG stage scoring has
done every 5 seconds for Cz site, referring to O2 recording. The parts transited 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 for REM sleep EEG stage were
according to the previous research [Takahara et al., 2006] as described 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 looked like “sawtooth” shape. Their
amplitudes range was between 20-100 µV, frequency 2-5 Hz, and at least consecutive 3 waves were
needed. This definition was according to Sato et al. (1997).
MT. Movement time: epoch composed of a train of at least 50 % immediate increase of amplitudes
in the EEG and EOG tracings by muscle tension and/or artifacts associated with movement of the
participant.
Topogram was captured based on the spectrum power of fast Fourier transform, using averaged
value of each 19 scalp site. Frequency bands were set as following: 2 Hz ≤ theta 1 < 4 Hz，4 Hz ≤
theta 2 < 8 Hz.
Statistical analysis was carried out by a repeated measure of analysis of variance (ANOVA). All
the posthoc comparisons were according to Tukey's honest significant difference (HSD) test.
3. Results
As was previously reported, EEG stages 4 (EEG flattening) and 5 (theta wave) occupied the
92.7% of all REM epochs, and EEG stage 5 occurred more often than EEG stage 4 (p < 0.01).
Most of REM sleep period were occupied with EEG stage 4 and 5. Thus, EEG stage 5-STW
(sawtooth waves) was observed very little number compared to EEG stage 5 (96 vs. 3398 epochs).
Figure 1 shows the percentage of epochs contain rapid eye movements for each EEG stage 4, 5, and
5-STW. ANOVA revealed the significant difference in percentage of epochs which contained REMs
(F(5,60) = 29.41, p < .001). EEG stage 5 and 5-STW were more often associated with REMs than EEG
stage 4.
Percentage of epochs contain REMs
***
(%)
50
40
30
20
10
0
4
5
5-STW
EEG stages
Figure 1. Percentage of epochs contain rapid eye movements for each EEG stage. *** represents
statistically significant difference at p < .001.
Figure 2 shows the number of REMs in 2 minutes (25 epochs) before and after the occurrence of
sawtooth waves. Zero minute or STW on the horizontal axis represents the epoch contains sawtooth
waves. There were main effects of elapsed time for before and after the sawtooth waves epoch
(F(24,240) = 8.85, p < .01; F(24,240) = 10.30, p < .01, respectively). Post-hoc tests revealed that the
number of REMs within 2 minutes before and after the sawtooth waves’ epoch indicated the largest
just in the same epoch of the sawtooth waves’ epoch.
Number of Rapid Eye Movements
(N)
50
**
**
40
30
20
10
0
-2
-1
0
1
2
STW
Time (min)
Figure 2. Number of rapid eye movements in 2 minutes before and after the occurrence of sawtooth
waves. Zero minute or STW on the horizontal axis represents the epoch contains sawtooth
waves. ** represents statistically significant difference at p < .01.
Amplitude distribution maps of theta ranges in EEG stage 5 and 5-STW are shown in Figure 3. All
the theta range topograms had a central distribution, and strongly resembled each other. Moreover,
there was also clear difference whether the epoch contained REMs (phasic period of REM sleep) or
not (tonic period of REM sleep).
Theta 1
Theta 2
Figure 3. Amplitude distribution maps of theta ranges in EEG stages 5 and 5-STW
4. Discussion
The present study investigated the stable state of REM sleep to determine the typical EEG pattern
and its relation with REMs. The present results were summarized as follows. The occurrence rate of
rapid eye movements during the 5-seconds epoch was highest for the EEG stage 5-STW (44.8 %), in
comparison to other EEG stages (20.5 % on average). Moreover, the number of rapid eye movements
within 2 minutes before and after the sawtooth waves’ epoch was the largest just in the same epoch of
the sawtooth waves’ epoch.
The relation between theta oscillation and REM sleep has been reported before [Nishida et al.,
2004; Takahara et al., 2006]. The present study demonstrated in human EEG recordings the strong
relationship between REMs and theta waves and the sawtooth waves by means of new scoring system
for REM sleep. There was no significant difference in percentage between EEG stages 5 and 5-STW.
They also resembled in spectrum topogram. Sawtooth wave is indeed a characteristic EEG pattern
observed before and during REM sleep period, however, its rate of occurrence was very low.
Nevertheless the highest percentage of EEG epochs with the sawtooth waves was a remarkable result.
EEG stage 4 also considerably associated with REMs by 20.7 % of the epochs. The EEG flattening
stage has been less well documented and understood. In the sleep onset period, EEG stage 4 was
infrequent and was a transient phenomenon [Tanaka et al., 1996]. How to interpret this stage is still
unclear.
In summary, the present study revealed that the relationship between the sawtooth waves and
REMs during REM sleep was not at random. The sawtooth waves not necessarily precede rapid eye
movements. During REM sleep, REMs temporally had to do with sawtooth waves. Ponto-geniculooccipital (PGO) spikes, which originate in the pons, appear after a few milliseconds in the lateral
geniculate nucleus, and can be observed with further delay in the occipital cortex in cats, are known as
a generator of REMs in REM sleep. When REMs occurs, PGO bursts also occurred with high
probability [Siegel, 2005]. It was possible that PGO processes might be related to the sawtooth waves
occurrence.
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