Sleep, 2(3):299-307
© 1980 Raven Press, New York
The REM Cycle is a
Sleep-Dependent Rhythm
L. C. Johnson
Naval Health Research Center, San Diego, California
Summary: Two studies, using data from fragmented sleep studies from three
sleep laboratories, are reviewed. These studies indicate that the REM cycle is
primarily governed by a sleep-dependent oscillator. These data, however, do
not rule out the potential influence of endogenous or environmental variables
as factors influencing the REM cycle. Further, acceptance of the REM cycle as
a sleep-dependent rhythm does not lead to the denial of the basic rest-activity
cycle (BRA C) proposed by Kleitman. It is questioned, however, whether the
BRAC measured during waking is an extension of the REM cycle recorded
during sleep. Key Words: Sleep-REM cycle-Ultradian rhythms.
Some may wonder why the title of this paper does not read' 'the REM - NREM
cycle is a sleep-dependent rhythm." While REM - NREM is the cycle of sleep,
our goal was to see if the REM cycle continued during awake activity and thus in
the absence of intervening NREM sleep. The continuation of the 90-100 min
REM cycle throughout the 24 hr period, regardless of state, is what we refer to as
the sleep-independent model. Though we found little support for this sleepindependent model, the focus of our study was on the REM cycle and not on the
REM- NREM cycle.
For clarity of discussion, I have positively stated our position in the title of this
paper. This rhythm, however, is not imperturbable. Our own data clearly indicate
that fragmentation of sleep, which leads to shortened REM episodes, reduces the
length of the REM cycle (Moses et aI., 1978). Also, as indicated by the varying
positions taken by participants in this workshop and the numerous factors that
have been advanced as governors of REM sleep, it is highly unlikely that a single
explanation would account for all the variance.
Globus (1966), in a study of daytime nap sleep, found that REM onsets tended
to cluster around certain clock times, relatively independent of the time of sleep
onset, and concluded that the occurrence of REM sleep is a function of the time of
day. Schulz et al. (1975) reported a gradual forward shift in REM onset time from
Accepted for publication April 1980.
Address reprint requests to Dr. Johnson at Naval Health Research, Bldg. 36-4, Naval Regional
Medical Center, San Diego, California 92134.
299
300
L. C. JOHNSON
night to night, indicating that the occurrence of REM is not dependent on time of
day, but is rather a function of an ongoing basic rest-activity cycle (BRAC), with
a cycle length that is not a submultiple of 24 hr. Brezinovli (1974) found that the
duration of the REM cycle was sensitive to factors within sleep itself, such as the
amount of stages 3 and 4 within the cycle, suggesting that the timing of the REM
cycle is not a simple manifestation of an ongoing BRAC. In a study of acute shifts
in the sleep-wake cycle, Taub and Berger (1973) interpreted their finding of
shortened REM cycles when-sleep onset was delayed past 0200 hr as a reflection
of the circadian influence on the REM cycle.
Before summarizing our results and conclusions, I would like to clarify our
position vis a vis Kleitman's BRAC hypothesis (1963). In its simplest form, this
hypothesis states that there is an ultradian oscillation in certain neurophysiological functions that continues throughout waking and sleeping. We have never
stated that a BRAC is nonexistent. We maintain that there is more than one
oscillatory system governing the rhythms seen during waking and sleeping. It is
quite possible that certain neurophysiological functions exhibit ultradian rhythms,
regardless of the state of consciousness. But we have presented evidence (Moses
et aI., 1977, 1978) that at least one-REM sleep-is governed by a state-dependent
oscillator. Our data come from nap studies from three different sleep laboratories.
METHODS
The reader is referred to the original articles by Moses et al. (1977, 1978) for
details as to subjects and procedures. Briefly, the sleep of a total of 25 subjects
from three independent sleep laboratories was analyzed. In addition, following a
base-line night, 8 male Naval School of Health Sciences students, aged 18-22
years, underwent a 60 min sleep-160 min wake schedule for 40 hr at the Naval
Health Research Center (NHRC) , San Diego. The 40 hr period was followed by 8
hr of recovery sleep (Moses et aI., 1975a). Ten students, 6 men and 4 women, aged
17-21, were studied at the Stanford University School of Medicine. Following 2
base-line nights, the subjects were placed on a 30 min sleep-60 min wake schedule for 5 days. The altered schedule was followed by 2-4 recovery nights, on
which the subjects were allowed to sleep ad lib (Carskadon and Dement, 1975).
Seven subjects, 6 men and 1 woman, aged 23-40, participated in a study at the
Clinical Research Center of Montefiore Hospital. The subjects slept normally for
7 base-line nights and then underwent a 60 min sleep-120 min wake schedule for
10 days. Seven recovery nights followed the altered schedule (Weitzman et aI.,
1974). All sleep recordings were scored according to Rechtschaffen and Kales
(1968).
In the analysis concerned with severe sleep fragmentation, the data from two
additional groups of subjects from a previous study were used (Moses et aI.,
1975b). These subjects underwent 3 consecutive nights of either slow-wave deprivation (S group, n = 7) or REM deprivation (R group, n = 7).
RESULTS
Altered sleep-wake schedules, such as in napping or multiphase sleep, provide
an opportunity to test the sleep-dependent hypothesis. According to the BRAC
Sleep, Vol. 2, No.3. 1980
THE REM CYCLE
301
hypothesis, REM should occur at approximately equidistant times throughout the
altered schedule period. This, however, was not the case. The total time (wake plus
sleep time) between REM onsets was extremely variable, both within and between
subjects, ranging from 21 min to more than 24 hr. Although the amount of REM in
all these studies was greatest between 0200 and 1000 hr, REM onset had no consistent relationship to time of day. REM onset appeared to be related to the amount of
sleep since the last REM onset.
If the REM cycle clock is sleep-dependent, stage REM onset should occur only
after 90-110 min of sleep has accrued since the last REM onset, regardless of the
amount of wake time between or within the scheduled periods. Figure 1 illustrates
the sleep-dependent and sleep-independent models.
According to the sleep-dependent hypothesis, the REM cycle length (RCL) in
naps should not differ significantly from the base-line night RCL. All analyses
began with the first REM onset of the sleep episode. RCL was measured from the
beginning of one REM episode to the beginning of the next REM episode. A REM
episode was a series of consecutive sequences of REM sleep separated by less
than 15 min of NREM sleep, movement time, or waking. We computed the average difference between nap and base-line RCL for each subject, and the overall
average difference was tested for significant (0.05 level) deviation from zero with a
t-test. None of the mean differences differed significantly from zero (Table 1).
Since publication of the data in Table 1, we have collected data on 4 subjects
from a subsequent study of fragmented sleep. Following a full night of sleep, the
subjects maintained a continuous 44 hr testing schedule, followed by two 2 hr naps
taken 8 hr apart. They were then allowed a full night of recovery sleep. When the
sleep time obtained during base line, naps, and recovery was combined and
viewed as one continuous sleep period, the average REM-to-REM interval was
SLEE P - DEPENDENT
MINUTES,
20
10
60
60
30
30
60
20
10
60
20
10
SLEEP - INDEPENDENT
MINUTES,
20
10
60
20
10
60
20
10
I
<.'.~'
~
FIG. 1. Hypothetical examples of REM onsets occurring during a 30-min sleep/60-min wake schedule.
In the s'leep~dependent model, total sleep time between REM onsets is 90 min (total real time is 270
min). The "c1ock" governing the time interval between REM onsets runs only during sleep; it stops on
awakening and resumes at the next sleep onset. In the sleep-independent model, total real time
, between REM onsets is 90 min (total sleep time is 30 min). The "clock" runs during both sleep and
waking. Studies of nap sleep from three independent sleep laboratories support the sleep-dependent
model. (From Moses et al., 1977.)
Sleep, Vol. 2, No.3, 1980'
302
L. C. JOHNSON
TABLE 1. REM cycle length for nap and
base-line sleep conditions
REM cycle length
Sleep
condition
San Diego
(n
= 8)
Nap
%.6 ± 20
Base line
97.1 ± 12
Nap minus
base line" -0.50 ± 21
Stanford
(n = 10)
Montefiore
(n = 7)
79.1 ± 23
92.0 ± 12
119.2 ± 30
104.6 ± 12
-12.9 ± 24
14.6 ± 31
a None of the differences between nap and base-line RCL are
statistically significant.
Values are means ± SO.
110.8 ± 11 min, well within the range of REM intervals in normal nocturnal
monophasic sleep.
While an examination of REM intervals gives an indication of cyclicity, it does
not address the question of rhythmicity per se. To determine rhythmicity, an
autocorrelation analysis developed by Naitoh et aI. (1973) was applied to the base
line, compressed nap sleep, and recovery sleep of the three groups of nap subjects. This method estimates the period of the REM cycle and yields r2, the
variance in REM cycle periodicity accounted for by a cosine wave and, thus, a
measure of the strength of that periodicity. For the details of this analysis, see
Moses et aI. (1978).
The average base line, nap, recovery sleep (min), and r2 values are presented in
Table 2. The r2 values were compared with t-tests for correlated means.
Except for the Stanford group, the length of the nap REM cycle did not change
significantly from base line during the compressed nap sleep. The overall decrease
in the strength of rhythmicity during nap sleep (Table 2) reflects the increased
variability in REM cycle length during the altered schedules. These nap r2 values,
however, were significantly larger than those obtained from a random distribution
of sleep stages. When the stages were randomized, all the r2 values fell to near
zero.
There were no consistent trends across nap segments in the Stanford and Montefiore groups; the RCL and r2 values remained relatively stable throughout the
schedule. There were too few REM cycles in the NHRC data for trend analysis.
An illustration of the REM cycle rhythmicity in one subject for the base line,
compressed nap, and recovery night is illustrated in Fig. 2.
Since the Stanford group's sleep was relatively more fragmented than the other
two groups (twice as many sleep periods per 24 hr), we explored the possibility
that RCL was influenced by the degree of sleep fragmentation.
In this analysis, we used two groups of subjects from our previous study on
sleep stage deprivation (Moses et aI., 1975b) to compare to the nap groups. We
chose these subjects for comparison because their sleep was highly fragmented:
an average of 55 awakenings per night for the 7 subjects of the R group and 44
awakenings for the 7 subjects of the S group (this between-group difference was
not significant).
Sleep, Vol. 2, No.3, 1980
TABLE 2. REM cycle length and r2 in base-line, nap, and recovery sleep
Groups
San Diego
(n = 6'1'
Stanford
(n = 10)
Montefiore
(n = 7)
Sleep/wake
cycle
(min)
60/160
Duration of
altered
schedule
40 hr
Mean r2
Mean REM cycle lengths (min)
Base line
Nap
Recovery
Base line
Nap
.
Recovery
~
tl'j
100.3 ± 16
105.6 ± 22
100.3 ± 22
0.622 ± 0.28
0.456 ± 0.15
0.691 ± 0.23
::r.:,
30/60
5 days
105.0 ± 15
60.0 ± 9°
98.3 ± 14
0.767 ± 0.15
0.423 ± 0.12°
0.779 ± 0.11
60/120
10 days
115.1 ± 18
100.8 ± II
102.1 ± II
0.752 ± 0.09
0.456 ± 0.06°
0.774 ± 0.09
tl'j
~
()
~
t'-<
tl'j
° Significant difference from base line, p < 0.05.
Two NHRC subjects had only one REM cycle during the naps and thus were excluded in this analysis.
Values are means ± SO.
b
~
""
~
..::
~
~
~
.w
~
c
v",
~
304
L. C. JOHNSON
BASE-LINE NIGHT
PERIOD: 9B MIN
,2
=.903
-1.0_
1.0
Z
0
~
:::
COMPRESSED NAPS
SEGMENT
PERIOD: 92 MIN
0
0
,2
.
u
= .785
;
C
-1.0_
1.0
Z
Q
~
.
RECOVERY NIGHT
PERIOD: 86 MIN
,2 = .898
0
~:0
C
-10_
I
20
I
60
,
100
I
140
I
180
I
220
LAG IN MINUTES
FIG. 2. Example of REM cycle period (length) rhythmicity in one subject under three experimental
conditions (Montefiore group). Top: Total elapsed time, 301 min; total sleep time, 300 min; time of day
range, 2354-0455; local time of REM onsets: 2354,0138,0310,0440; average sleep time between REM
onsets, 95 ± 8 min. Middle: Total elapsed time, 1,423 min (23 hr, 43 min); total sleep time, 300 min
obtained in seven I-hr naps at 0000,0300,0600,0900, 1200, 1500, 1800; time of day range, 0055-0038;
local time of REM onsets, 0055, 0628,1233,1853; average sleep time between REM onsets, 87 ± 12
min. Bottom: Total elapsed time, 301 min; total sleep time: 300 min; time of day range, 0006-0507;
local time of REM onsets, 0006, 0113, 0239, 0401; average sleep time between REM onsets, 80 ± 9
min. (From Moses et aI., 1978.)
The autocorrelation analysis was applied to the Rand S groups to determine the
length of the REM cycle and the strength of rhythmicity during base line, sleep
stage deprivation, and recovery. REM cycle analysis was possible for the R group
because the deprivation procedure, while severely shortening each REM episode,
did not completely eliminate REM sleep. As with the three nap groups, all wake
time within sleep sessions was subtracted. REM deprivation significantly reduced
the RCL from a base-line average of98 min to an average of73 min, and the r2 was
reduced from 0.77 base line to 0.34 during REM deprivation. Furthermore, the r2
during REM deprivation was significantly lower than the average r2 in the three
nap groups. Despite the frequent awakenings, slow wave sleep deprivation had no
effect either on REM cycle length or r2.
Sleep, Vol. 2, No.3, 1980
THE REM CYCLE
305
Recovery Sleep
Inspection of Table 2 shows that despite the severe alteration of the normal
sleep-wake pattern during the nap schedules, RCL and rhythmicity on recovery
were unchanged from base-line levels. This is of particular interest in the Stanford
group, whose REM cycles were shortened during the naps and who were allowed
to sleep ad lib during the recovery; the average total sleep time of the Stanford
subjects on the first recovery night was 838 min.
DISCUSSION
A clear REM cycle was seen in all three studies, and with the exception of the
Stanford group, the length of the REM cycle in compressed nap sleep did not
change.
The reduced nap r2 value, however, raises the question of what r2 value can be
considered as indicative of significant rhythmicity. While the significant reduction
in nap r2 for two of the three groups reflects increased validity in the nap RCL, we
presently lack an adequate method of testing these r2 values for significance. Our
analyses using randomized sleep stages, however, yielded near-zero r2 values,
demonstrating that the nap data were nonrandom.
No biological rhythm is impervious to external factors, and we have never
implied, nor meant to imply, that the REM cycle is an exception. But for a
biological event to be considered cyclic, it must repeat itself in time in some sort of
regular fashion. If the BRAC concept is to be useful, it has to be capable of
predicting the approximate timing of certain events. One interpretation of the
BRAC is that REM should occur at approximately equidistant time intervals
throughout the altered sleep-wake schedule. Our data clearly do not support this
interpretation.
Finally, there is some inconsistency in the interpretation of waking rhythms and
REM sleep as manifestations of a BRAC. Stage REM during normal sleep appears
to be a state of heightened physiological arousal, relative to NREM sleep, as
shown by electroencephalographic changes, rapid eye movements, increased and
more variable heart rate, increased body motility, and lowered arousal threshold.
Some studies of waking rhythms have shown cyclic occurrences of periods of
heightened arousal such as increased oral activity and rapid eye movements that
are perhaps consistent with REM-like processes. Other studies have reported
cyclic periods during waking of lowered arousal, expressed as increased test
errors, ocular quiescence, and increased fantasy and daydreaming. It is not yet
clear whether the periods of heightened arousal or lowered arousal are supposed
to be the waking counterparts of REM and NREM episodes during sleep.
Furthermore, to assume a continuation of the REM - NREM cycle throughout
the 24 hr period would assume that the REM cycle during the awake state would
have a functional significance similar to that during sleep. Many would question
such an assumption, and the diversity in the physiology and behavioral states in
the awake ultradian rhythms that have been identified would support skepticism
Sleep, Vol. 2, No.3, 1980
306
L. C. JOHNSON
as to the similarity of sleep and awake REM cycles. In a very thorough review of
the issue of BRAC and ultradian rhythms, Kripke (1974) raised the question as to
whether a BRAC concept is appropriate for human adults and pointed out the
need for the kind of evidence we have tried to provide: "More evidence is needed
to establish that the phenomena [ultradian rhythms in sleep and wakefulness]
result from a common oscillatory system, an inference based presently only on the
resemblance of the cycles described."
As we have always maintained, we do not feel that our sleep-dependent model
is adequate for the complete understanding and prediction of REM cycling. It is
obvious that a more comprehensive model is needed to account for the rhythms
during waking and to clarify the relationship, if any, of such rhythms to the REM
cycle during sleep. Our results do not preclude a relationship between awake and
the sleep ultradian rhythms, but our data strongly suggest that REM processes are
processes of sleep.
ACKNOWLEDGMENT
This research was supported by the Naval Medical Research and Development
Command, Department of the Navy, under Work Unit MF58.524.004-9026. The
views presented in this paper are those of the author. No endorsement by the
Department of the Navy has been given or should be inferred.
REFERENCES
Bfezinova V. Sleep cycle content and sleep cycle duration. Electroencephalogr Clin Neurophysiol
36:275-282, 1974.
Carskadon MA and Dement WC. Sleep studies on a 90-minute day. Electroencephalogr Clin
Neurophysiol 39: 145-155, 1975.
Globus GG. Rapid eye movement cycle in real time. Arch Gen Psychiatry 15:654-659, 1966.
Kleitman N. Sleep and Wakefulness. University of Chicago Press, Chicago, 1963.
Kripke DF. Ultradian rhythms in sleep and wakefulness. In: ED Weitzman (Ed), Advances in Sleep
Research, Vol 1, Spectrum, New York, 1974, pp 305-325.
Moses JM, Hord DJ, Lubin A, Johnson LC, and Naitoh P. Dynamics of nap sleep during a 40 hour
period. Electroencephalogr Clin Neurophysiol 39:627-633, 1975a.
Moses JM, Johnson LC, Naitoh P, and Lubin A. Sleep stage deprivation and total sleep loss: Effects
on sleep behavior. Psychophysiology 12: 141-146, 1975b.
Moses J, Lubin A, Johnson LC, and Naitoh P. Rapid eye movement cycle is a sleep-dependent
rhythm. Nature 265:360-361, 1977.
Moses J, Naitoh P, and Johnson LC. The REM cycle in altered sleep/wake schedules. Psychophysiology 15:569- 575, 1978.
Naitoh P, Johnson LC, Lubin A, and Nute C. Computer extraction of an ultradian cycle in sleep from
manually scored sleep stages. Int J Chronobiol 1:223-234, 1973.
Rechtschaffen A and Kales A (Eds). A Manual of Standardized Terminology, Techniques and Scoring
System for Sleep Stages of Human Subjects. UCLA Brain Information ServicelBrain Research
Institute, Los Angeles, 1968.
Schulz H, Dirlich G, and Zulley J. Phase shift in the REM sleep rhythm. Pj/uegers Arch 358:203-212,
1975.
Taub JM and Berger RJ. Sleep stage patterns associated with acute shifts in the sleep-wakefulness
cycle. Electroencephalogr Clin Neurophysiol 35:613-619, 1973.
Weitzman ED, Nogeire C, Perlow M, Fukushima D, Sassin J, McGregor P, Gallagher TF, and
Hellman L. Effects of a prolonged 3-hour sleep-wake cycle on sleep stages, plasma cortisol, growth
hormone and body temperature in man. J Clin Endocrinol 38: 1018-1030, 1974.
Sleep, Vol. 2, No.3, 1980
THE REM CYCLE
307
DISCUSSION
The conclusion that "'REM processes are processes of sleep" was questioned, as the
data related only to the REM - NREM cycle and did not address the circadian rhythm of
REM sleep. Dr. Johnson agreed that his work was related to the ultradian REM cycle and
that when the data were analyzed in terms of the time of day, there was more REM
sleep in the morning than in the afternoon. However, the REM cycle period length
remained the same. He hypothesized that the phenomenon of sleep onset REM episodes,
raised by Dr. Weitzman, probably occurred only when a sufficient amount of sleep time
had elapsed since the onset of the previous REM episode. He felt this explained the
very short REM sleep latencies observed in some naps and longer latencies in others.
Dr. Roffwarg emphasized the similarity of results in the REM deprivation experiments
and questioned whether the increased frequency of the REM - NREM cycle observed was
related to REM deprivation.
Dr. Spielman mentioned that he REM sleep deprived several patients with the
narcolepsy-cataplexy syndrome. The awakenings required for REM deprivation continued
to cluster throughout the night, at the time of expected REM episodes. He suggested this
might be a good model to study the daytime period length of the Basic Rest- Activity Cycle
(BRAC).
Sleep, Vol. 2, No.3, 1980