International Journal of Bioelectromagnetism
Vol. 11, No. 3, pp.144-148, 2009
www.ijbem.org
Co-occurrence of Sawtooth Waves and Rapid Eye
Movements during REM Sleep
a
Madoka Takaharaa, Sakon Kanayamab, Tadao Horib,c
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. We investigated the relationship between sawtooth waves and rapid eye movements during
periods of REM sleep using a system that scored electroencephalograms (EEG) in 5-sec intervals
[Takahara et al., 2006]. Eleven university and graduate-school student volunteers participated in this
study. Initially we scored polysomnographic (PSG) recordings according to standard criteria for 30-sec
intervals, and we used standard criteria to identify REM epochs. These 30-sec REM epochs were
subdivided into 5-sec epochs, and they were re-scored according to Sato’s definition of sleep stages.
The fraction of 5-sec epochs that contained at least one REM was higher for the EEG stage 5-STW
epochs (44.8%) than for the corresponding fraction for other EEG stages (20.5% on average). REMs
occurred far more frequently in 5-sec epochs containing sawtooth waves than in any other epoch
within 2 minutes of an epoch containing sawtooth waves, suggesting that the relationship between
sawtooth waves and rapid eye movements during REM sleep is not random. During REM sleep, rapid
eye movements are temporally related to sawtooth waves. We showed that sawtooth waves do not
necessarily precede rapid eye movements. The present study suggested that PGO processes possibly
are related to the occurrence of sawtooth waves.
Keywords: rapid eye movement (REM) sleep, sawtooth waves, EEG stages
1. Introduction
The sawtooth wave is a distinctive pattern in electroencephalograms (EEG) that occurs only in
REM sleep and that is recorded mainly in the central scalp area. Different investigators have defined
sawtooth waves differently. Sato et al. (1997) defined a sawtooth wave as an EEG pattern with 3
characteristics: 1) EEG frequency between 2 and 5 Hz; 2) EEG amplitude in the range 20–100 μV, and
3) three or more waves. NREM sleep transitions to REM sleep 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 sawtooth waves stabilize REM sleep. The EEG
patterns specific to REM sleep are the theta wave, the sawtooth wave, and the alpha wave. The theta
wave is characterized by a frequency between 4 and 7 Hz and is dominant in central sites.
Previously we showed the pattern of occurrence and the transitions of these characteristic EEG
patterns during REM sleep using a new scoring system of EEG stages for REM sleep based on Hori’s
nine EEG stages of the sleep onset period [Takahara et al., 2006]. REM sleep consists of a mixture of
the characteristics of EEG stage 4 (EEG flattening) and EEG stage 5 (theta wave). The purpose of this
study was to investigate how a new system of scoring EEG stages affects some parameters of REM
sleep.
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2. Materials and Methods
2. 1. Participants
Eleven healthy young students (5 women and 6 men) volunteered to participate in this study (mean
age = 22.7 ± 1.9 years). All participants reported themselves to be good sleepers, right-handed, nonsmokers and free from any medication. On the experimental day, participants were instructed to wake
up at their usual time and to abstain from alcohol, caffeine, medication, excessive exercise, and naptaking. Prior to the experiment, participants received adequate instruction about the purpose and
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 Human Ethics Committee of the Faculty of
Integrated Arts and Sciences of Hiroshima University approved the protocol.
2. 2. Recordings and Experimental Procedure
On two consecutive nights we recorded all-night polysomnograms (PSG) that included EEGs 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 as a reference, vertical and horizontal electrooculograms (EOGs), and
submental electromyograms (EMG). The first night was an adaptation night; the second night provided
the data for this analysis. Time constants were 0.3 seconds for EEG and EOG and 0.003 seconds for
EMG. The data were digitized at 1 kHz. A high-pass filter was set at 30 Hz. All electrode impedances
were set below 5 kΩ. Part of the present data have been reported previously [Takahara et al., 2006].
2. 3. Analysis
PSG recordings were divided into 30-sec epochs and scored according to international standard
criteria [Rechtschaffen and Kales, 1968] and their supplements and amendments [Sleep Computing
Committee of the Japanese Society of Sleep Research (JSSR), 2001]. We further analyzed the periods
scored as REM sleep that lasted for more than 5 minutes. We divided the trace from the Cz site (with
respect to O2) into 5-sec epochs. We extracted typical REM sleep periods, although we excluded
intervals in which REM sleep transitioned to another sleep stage and then back to REM sleep. We used
the same scoring definitions for REM sleep EEG stage that we have used in previous research
[Takahara et al., 2006], as described in Table 1.
Table1 Scoring definitions for REM sleep EEG stage
EEG stage Description
1
Alpha wave, train: epoch composed of a train of alpha activity with a minimum amplitude of 20 μV.
2
Alpha wave, intermittent A: epoch composed of a train of at least 50% alpha activity with a minimum amplitude of 20
μV.
3
Alpha wave, intermittent B: epoch composed of a train of < 50% alpha activity with a minimum amplitude of 20 μV.
4
EEG flattening: epoch composed of suppressed waves of < 20 μV.
5
Theta wave: epoch composed of low-voltage theta waves (20 μV < θ < 50 μV).
Sawtooth waves: epoch contains waves that have the sawtooth shape. Their amplitude range is 20-100 μV, frequency 2-5
5-STW Hz,
and at least 3 consecutive waves are needed [Sato et al., 1997].
MT
Movement time: epoch composed of a train of at least 50% immediate increase of amplitude in the EEG and EOG
tracings
caused by muscle tension and/or by the movement of the participant.
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A topogram was captured based on the spectral power of a fast Fourier transform, using the
average value of each of the 19 scalp sites. Frequency bands were set as follows: 2 Hz ≤ theta1 < 4 Hz，
4 Hz ≤ theta2 < 8 Hz.
Statistical analysis was carried out by a repeated measure of analysis of variance (ANOVA). All
the post hoc comparisons were done with Tukey's honest significant difference (HSD) test.
3. Results
Percentage of epochs contain REMs
Consistent with our previous report, EEG stages 4 (EEG flattening) and 5 (theta wave) occupied
92.7% of the REM epochs, and EEG stage 5 occurred more often than EEG stage 4 (p 0.01).
There were far fewer epochs of EEG stage 5-STW (sawtooth waves) than EEG stage 5 (96 vs.
3398 epochs). For the EEG stages 4, 5, and 5-STW, ANOVA (Fig. 1) showed that the percentages of
epochs containing REMs for both EEG stage 5 and EEG stage 5-STW were significantly higher than
the corresponding percentage for EEG stage 4 (F(5,60) = 29.41, p < .001).
***
(%)
50
40
30
20
10
0
4
5
5-STW
EEG stages
Figure 1. Percentage of epochs that contain rapid eye movements for 3 EEG stages. *** represents a
statistically significant difference at p < .001.
To characterize and quantify the chronologic positions of REMs relative to sawtooth waves in
periods of REM sleep, we analyzed 4-min intervals of the EEG recordings (REM sleep only) that each
contained sawtooth waves in the 5-sec epoch at its center (Fig. 2). We “registered” these intervals by
designating the epoch with sawtooth waves as the Zero epoch, and we formed a cumulative count of
the total REMs for all subjects in the Zero epochs. For each of the 25 epochs in the 2 minutes
following the Zero epoch, we counted total REMs for all subjects. Similarly, we formed cumulative
counts for the 25 epochs before the Zero epoch. Zero minute or STW on the horizontal axis represents
the epoch that contains sawtooth waves. There were main effects of elapsed time before and after the
epoch containing sawtooth waves (F(24,240) = 8.85, p < .01; F(24,240) = 10.30, p < .01, respectively).
Post-hoc tests showed that the number of REMs occurring in the epoch containing sawtooth waves was
much larger than that for any epoch within 2 minutes of the epoch containing sawtooth waves.
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Number of Rapid Eye Movements
(N)
50
**
**
40
30
20
10
0
-2
-1
0
1
STW
2
Time (min)
Figure 2. Number of rapid eye movements in each 5-sec epoch within 2 minutes of the occurrence of
sawtooth waves. Counts are cumulative for all subjects and all REM sleep periods. The 5sec epoch at zero on the horizontal axis contains sawtooth waves. ** represents a
statistically significant difference at p < .01.
Amplitude distribution maps of theta ranges in EEG stages 5 and 5-STW show that amplitude is
centrally distributed and that all topograms strongly resemble each other (Fig. 3). Moreover, there was
no clear difference in distribution, whether the epoch contained REMs (phasic period of REM sleep) or
not (tonic period of REM sleep).
Theta 1
Log μV
2
Theta 2
Figure 3. Amplitude distribution maps of theta ranges in EEG stages 5 and 5-STW
4. Discussion
In the present study we investigated the stable state of REM sleep to detect and to quantify
relationships between EEG patterns and REMs. Our results show that rapid eye movements usually
occur within 5 seconds of the occurrence of sawtooth waves.
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A relationship between theta oscillation and REM sleep has been reported [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 sawtooth waves by means of a new scoring system
for REM sleep. There was no significant difference in percentage between EEG stages 5 and 5-STW.
The topograms of these two stages resembled each other. The sawtooth wave is indeed a characteristic
EEG pattern observed before and during REM sleep period, but its rate of occurrence is low.
EEG stage 4 was associated with REMs in 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 shows that the relationship between sawtooth waves and REMs
during REM sleep is not random. Sawtooth waves do not necessarily precede rapid eye movements.
During REM sleep, REMs are temporally associated with sawtooth waves. Ponto-geniculo-occipital
(PGO) spikes originate in the pons and appear after a few milliseconds in the lateral geniculate nucleus.
These spikes, which can be observed with further delay in the occipital cortex in cats, are known as a
generator of REMs in REM sleep. When REMs occur, PGO bursts also occur with high probability
[Siegel, 2005]. PGOs are possibly related to sawtooth waves.
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