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Chimpanzee sleep stages
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
CHIMPANZEE
485
SLEEP STAGES I
FRANK R. FREEMON, JAMES J. M C N E W AND W. R o s s ADEY Marquette School of Medicine, Milwaukee, Wisc. 53226, and Brain Research Institute, UCLA Center for the Health Sciences, Los Angeles, Calif. 90024 (U.S.A.) (Accepted for publication: April 6, 1971)
Chimpanzee sleep can be divided into electroencephalographic stages analogous to the stages of sleep in man (Adey et al. 1963). The purpose of the present study was to measure the amounts of each of these stages during normal sleep in unrestrained chimpanzees. At the time this project was begun, the only study dividing chimpanzee sleep into stages similar to the human sleep stages was the technical report of Rickles (1965), who studied the abnormal sleep of chimpanzees restrained in a chair. Since the completion of the present study, a report by Bert et al. (1970) has appeared which gives sleep stage percentages in unrestrained chimpanzee. Our results show some differences from theirs, and comparison of the sleep of chimpanzee in two different laboratories may allow refinement of our knowledge of the sleep of this important species. MATERIALSAND METHODS This study of 7 consecutive nights of sleep each from one male chimpanzee, named Corky, and one female, named Kelly, was performed at the Space Biology Laboratory, UCLA. The animals were 4 years old and weighed 18 kg. Details of animal care, electrode implantation and telemetry methods have been published previously (Freemon et al. 1969). Cortical EEG was recorded between pairs of stainless-steel screws overlying frontal, parietal and occipital cortices. The electro-oculogram (EOG) was recorded between stainless-steel wire leads 1The investigation was supported by National Aeronautics and Space Administration under contract NSR 05-007-158 and by the National Institute of Neurological Diseases and Stroke, National Institutes of Health, U.S.
Public Health Service under Grant NB 02501.
placed in the ventral lateral orbital ridge and medial dorsal orbital ridge of the right eye. The electromyogram (EMG) was recorded from an electrode in the posterior neck muscles. Each animal was monitored from at least 30 min before lights out at 19.00 to at least 30 min after lights on at 07.00 by closed television and by telemetered EEG, EOG and EMG for 7 consecutive nights. The animal was adapted to the television camera, the telemetry aerial beneath his cage and the telemetry pack for at least one week before the recording. Kelly had participated in a previous 7 consecutive night study; Corky had not. The records were scored by a slight modificat:on of the Rechtschaffen and Kales (1968) modification of the Dement and Kleitman scoring rules for human sleep stages. The EMG showed a decrease in amplitude during transition from wakefulness to sleep but was not helpful in differentiating REM (rapid eye movement) from nonREM sleep. All scoring was done on the basis of the cortical EEG channels and the EOG without reference to the electrical activity of subcortical structures. When each 20 sec epoch was scored strictly according to the rules, changes between waking (W) and 1 and among stages 2, 3 and 4 were too frequent to make a graph of these changes intelligible. We therefore "smoothed" the graph by transforming 9 successive groups of 20 sec epochs into one 3 min epoch by extracting that sleep stage which occupied a majority or plurality of the 9 epochs. RESULTS
As summarized in Table I, one of our animals showed less REM, less stage 4, and more W on Electroenceph. olin. Neurophysiol., 1971, 31:485489
486
F . R . FREEMON e t a l .
KELLY
TABLE I 20 0O
A comparison of the first experimental night to the average of nights 2-7 for each animal. Time in minutes. Corky
' N
!
r~w 2N
Kelly
Sleep stage
First night
Nights 27
First night
Nights 2-7
W 1 2 3 4 REM
89.0 58.7 274.3 91.0 58.7 148.7
61.4 42.7 274.1 97.3 84.1 160.1
104.7 58.7 242.0 87.3 61.7 148.0
63.0 57.7 302.1 94.1 52.1 141.0
22 00
i
2400
~
~
0200
. ~
.
. -
~
04 00
.
. ~
. j
~ j ~ _
w
aN ~ R i ~ I ~ d ~ f ~ ~
~
0600
.
.
~.~
~J~F
4 NR~32r ~EI
r~h,l-tl~hn~ 5 NR32 ~,~E
~,- ~j
n,,, iMn~ ~ ~lk~l~p,n,~ ~;~LF u--~-~L_/~-~-q_j--rLl UUl/- I I U
TABLE II Time (in minutes)spent by each animal in each sleep stage is an average of experimental nights 2-7. The results are broken down by 3 h periods from 1900 to 0700. In most instances, the sleep stages do not add exactly to 180 min for any fourth of the night, because a few epochs were obliterated by telemetry
7 dRi'i~ ~ RE~- .
artifact.
~
Sleep stage
Fourth of the night 3
Total 4
Percentage of sleep
12.8 63.0 16.1 57.7 8 5 . 7 302.1 8.1 94.1 0.6 52.1 4 9 . 3 141.0
-9 47 14 8 22
1
2
32.8 20.9 51.3 34.0 28.0 11.4
6.0 1 1 . 4 7.7 1 3 . 0 72.7 92.4 2 9 . 3 22.7 20.2 3.3 44.1 36.2
W 1 2 3
16.4 11.7 54.4 29.8
13.3 11.8 19.9 61.4 8.4 9.8 118 42.7 7 4 . 3 6 7 . 7 7 7 . 7 274.1 2 8 . 6 2 4 . 9 14.0 97.3
4 REM
41.5 26.9
2 7 . 0 14.6 1.0 84.1 2 7 . 8 5 1 . 2 5 4 . 2 160.1
.
~ .
~
[ - - ~ F_a__~ U , ~ u~
.
CORKY ~o
~
~o
3
rI
z N,tRE~32
2~o0
02oo
i
W
~
o4oo
o~0o __
~
3 NR32 tRE~ a
Kelly
W 1 2 3 4 REM
[-~ .
Corky
N~3] 4
R~
~w NR132 5 t E~ ~ 1w
-
-
6 42 15 13 24
the first experimental night than on the average of nights 2-7. Further analysis is restricted to nights 2-7 in order to be sure that a "first night effect" does not muddy our description of sleep patterns in normal juvenile chimpanzee. The animals were out of their cages and awake during the day, except after lunch from about 12.00 and 13.30 when they sometimes napped. Although these naps were not analyzed in detail, REM periods were seen. Behavioral
6LR~M4~
~'h~L~
~LI
"~LJ
"I~''lJU
L]''U
7 ~.~I.,'~' Fig. 1. Cyclic activity during 7 consecutive nights (1 7) of sleep in two chimpanzees. W=waking, NR 1-4=nonREM sleep stages, REM =REM sleep.
observations and 24 h recordings demonstrated that with this exception, the animals were awake throughout the day. Between lights out at 1900 and lights on at 0700, the two animals spent an average of 652.4 min asleep and 62.2 rain awake. An average of 5.4 rain per night was obscured by artifact. Of the time asleep, 8 ~ was nonREM stage 1, 4 4 ~ stage 2, 15 ~ stage 3, 10 ~ stage 4 and 23 % stage REM. Table II breaks down these averages by E/ectroenc~Th. c/in. N e u r o p h y s i o l . ,
1971, 31 : 485 489
CHIMPANZEE SLEEP STAGES
487
TABLE III
wakefulness than did our animals. Bert et al. u s e d phencyclidine to sedate their animals for battery changes, whereas our animals, who could recorded in the present study, be handled for battery changes, had received no CNS depressants since electrode implantation Bert et al. (1970) Present over a year before recording. Sedatives decrease study the percentage of sleep spent in the REM stage, Total time of study 14 h 12 h and the chronic use of hypnotic medication can Time awake 260rain 62 min produce long-term effects on sleep; however, Time asleep 580 rain 652 min Bert et al. restricted analysis to those nights when Sleep stage(~o) the animals had not received phencyclidine for 1 14 8 2 32 44 at least the preceding 48 h, and it seems unlikely 3 29 15 that the animals received sedation so often as to 4 10 l0 demonstrate the chronic effects of the drug on REM 15 23 sleep. Differences in scoring methods might explain the differences between stages 1, 2 and 3, animal and by fourths of the night. The majority but the scoring of the REM type of sleep is of stage 2 and much of stage REM occurred straightforward; the combination of eye moveduring the latter portions of the sleeping period, ments and low voltage mixed frequency EEG is whereas almost all of stage 4 took place before quite distinct. A R E M period usually begins in 0100. chimpanzee with the change in EEG preceding the Fig. 1 gives the smoothed graphed data from first eye movement by up to a minute. Often a each animal for each night. One can see that burst of saw-tooth shaped waves in the EEG 7-9 complete REM periods occurred each night, heralds the onset of the REM period. We scored From the graphs, one can calculate the sleep the beginning of the REM period as the time of cycle length, defined as the length of time from the EEG change. If Bert et al. restricted the bethebeginningofoneREMperiodtothebeginning ginning of a REM period to the first eye moveof the next REM period. For nights 2-7, the ment, this could possibly explain a small portion ,sleep cycle averaged 86.1 min (range 42-171) in of the difference between their and our REM Kelly and 85.2 rain (range 36-144) in Corky. percentages. We suspect that the major difference in DISCUSSION results, however, is a function of the age of the animals. Our animals were approximately 4 Table III contrasts the results of the present years old, were sexually immature, and weighed study with the previous results of Bert et al. approximately 18 kg. Bert et al. studied sexually (1970). The animals in the previous study were mature chimpanzees weighing 39 52 kg. In awake longer and had less stage R E M than our several species, including man, the younger animals. In addition, there were differences individual has a higher REM percentage and a among nonREM stages, particularly stages 2 longer total sleep time than older members of and 3. The percentage of sleep spent in stage 4 the same species (Roffwarg et al. 1966). Age is the was identical in the two studies. Since these are major distinguishing characteristic between our the only two quantitative studies of unrestrained chimpanzees and those of Bert et al., and our chimpanzee in which sleep stages were defined in results, taken together, are most easily intera manner analogous to Dement and Kleitman's preted as indicating that in chimpanzee, as in sleep stages for man, we will try to explain the man, the adolescent has a greater REM percendifferences in results, tage and a longer sleeping time than has the Bert et al. studied 14 h of sleep, from 1700 to adult. 0700, whereas we studied 12 h only. Even if the Bert et al. attribute a portion of the difference 2 h of difference were spent in wakefulness, the between the sleep of their chimpanzees and the animals of Bert et al. had greater amounts of sleep of man to environmental differences. They Comparison of the sleep of mature chimpanzee as studied by Bert et al. with the sleep of juvenile chimpanzee as
Electroenceph. clin. Neurophysiol., 1971, 3l: 485 489
488 suggest that the frequent awakenings in their study are related to the fact that their animals, although unrestrained in the sense that they are not tied to a chair, are restrained as compared to chimpanzees living in the wild, sleeping in trees. They point out that attempts to measure natural sleep will never be entirely successful since the very act of recording changes the nature of sleep, a sort of a Heisenberg principle of sleep research. It is possible that differences in environment at the Aeromedical Research Laboratory, Holloman Air Force Base, where Bert's experiments were performed, and at Space Biology Laboratory, UCLA, might account for some of the differences in the results of these two studies. The Aeromedical Research Laboratory, for instance, has part of its cage out-ofdoors, where seasonal variations in lighting could conceivably affect sleep patterns, whereas at the Space Biology Laboratory the chimpanzees spend their lives in a large but windowless room. Another important environmental difference is that our animals have undergone extensive domestication procedures producing dependence upon human trainers who handle and play with the chimps daily, whereas the Holloman animals are not tamed, and handling involves drugs and forced restraint. The two groups would naturally acquire different responses toward an experimental situation involving the presence of man. Studies of the effect of environment on sleep have lagged behind studies describing species, age and drug-induced effects on sleep patterns, and we cannot know, at the present time, what effect environment has on chimpanzee sleep. Another way of comparing the results of the present study with the previous results of Bert et al. is to emphasize the areas of agreement. Two different laboratories studying two different age groups of chimpanzees in two different environments have produced somewhat similar results, For example, we can say with total confidence that chimpanzee sleep can be divided into stages analogous to Dement and Kleitman's sleep stages for man. We can say that approximately 10 ~ of chimpanzee sleep is nonREM stage 4, a characteristic type of sleep with large amounts of delta activity in the EEG. We can say that a significant proportion of chimpanzee sleep is
F.R. FREEMONet al. spent in the REM type of sleep. With individual differences, age differences, environmental differences, procedural differences, could we really have expected greater agreement? SUMMARY Using telemetry methods, we monitored the electroencephalogram and electro-oculogram of two unrestrained juvenile chimpanzees for 7 consecutive nights. The all-night records were scored by a slight modification of the rules developed by Dement and Kleitman for human sleep. The chimpanzees spent an average of 652 rain asleep and 62 rain awake. Of the sleeping time, 23 ~ was spent in the rapid eye movement or REM type of sleep, whereas 8, 44, 15 and 10~ were spent in nonREM stages 1 through 4 respectively. Seven to nine periods of REM sleep occurred per night. The average time from the beginning of one REM period to the beginning of the next was approximately 85 min. RESUME STADES DE SOMMEIL DU CHIMPANZE
A l'aide de m6thodes t616m6triques, nous avons enregistr6 l'61ectroenc6phalogramme et l'61ectro-oculogramme de deuxjeunes chimpanz6s lihres de leurs mouvements pendant 7 nuits cons6cutives. Les enregistrements de route la nuit ont ~t6 quantifi6s en modifiant 16g~rement les r6gles mises au point par Dement et Kleitman pour le sommeil humain. Les chimpanz6s ont pass4 en moyenne 652 min fi dorrnir et 62 min 6veill6s. Dans ce temps de sommeil, 23~ consistent en activit6s de mouvements oculaires rapides ou phases de mouvements oculaires (PMO) de sommeil, alors que 8, 44, 15 et 10~ respectivement sont d6volus aux stades 1 ~t 4 du sommeil lent. Sept ~t neuf p6riodes de PMO par nuit ont 6t6 d6nombr6es. Le temps moyen du d6but d'une p6riode de mouvements oculaires rapides au commencement de la suivante est d'environ 85 min.
The authors wish to thank Dr. J. Bert for commenting on
an earlier draft of this paper. Electroenceph. clin. Neurophysiol., 1971, 31 : 485-489
CHIMPANZEE SLEEP STAGES
REFERENCES ADEY, W. R., KADO, R. T. and RHODES, J. M. Sleep: cortical and subcortical recordings in the chimpanzee. Science, 1963, 141: 932-933. BERT, J., KR1PKE, D. F. and RHODES, J. M. Electroencephalogram of the mature chimpanzee: 24 hour recordings. Electroenceph. clin. Neurophysiol., 1970, 28:368 373. FREEMON, F. R., MCNEw, J. J. and ADEY, W. R. Sleep of unrestrained chimpanzee: cortical and subcortical recordings. Exp. Neurol., 1969, 25: 129-137. RECHTSCHAFFEN, A. and KALES, A. (Eds.). A manual 0/"
489 standardized terminolo.qy, techniques, and scorinq system jbr sleep staqes o/ human suh/ects. NIH, Publication 204, U.S. Government Printing Office, Washington, D.C., 1968, 55 p. RtCKLES, W. R. A study of EEG and somato-veoetative physiolooy of the immature chimpanzee durin# sleep. Aeromedical Res. Lab. Technol. Rept. No. 64-19, Holloman Air Force Base, New Mexico, 1965, 55 p. ROFFWARG,H. P., MUZIO, J. N. and DEMENT, W. C. Ontogenetic development of the human sleep-dream cycle. Science, 1966, 152: 604--619.
ReJbrence: FREEMON, F. R., McNEw, J. J. and ADEY, W. R. Chimpanzee sleep stages. Electroenceph. clin. Neurophysiol., 1971, 31:485 489.
CHIMPANZEE
485
SLEEP STAGES I
FRANK R. FREEMON, JAMES J. M C N E W AND W. R o s s ADEY Marquette School of Medicine, Milwaukee, Wisc. 53226, and Brain Research Institute, UCLA Center for the Health Sciences, Los Angeles, Calif. 90024 (U.S.A.) (Accepted for publication: April 6, 1971)
Chimpanzee sleep can be divided into electroencephalographic stages analogous to the stages of sleep in man (Adey et al. 1963). The purpose of the present study was to measure the amounts of each of these stages during normal sleep in unrestrained chimpanzees. At the time this project was begun, the only study dividing chimpanzee sleep into stages similar to the human sleep stages was the technical report of Rickles (1965), who studied the abnormal sleep of chimpanzees restrained in a chair. Since the completion of the present study, a report by Bert et al. (1970) has appeared which gives sleep stage percentages in unrestrained chimpanzee. Our results show some differences from theirs, and comparison of the sleep of chimpanzee in two different laboratories may allow refinement of our knowledge of the sleep of this important species. MATERIALSAND METHODS This study of 7 consecutive nights of sleep each from one male chimpanzee, named Corky, and one female, named Kelly, was performed at the Space Biology Laboratory, UCLA. The animals were 4 years old and weighed 18 kg. Details of animal care, electrode implantation and telemetry methods have been published previously (Freemon et al. 1969). Cortical EEG was recorded between pairs of stainless-steel screws overlying frontal, parietal and occipital cortices. The electro-oculogram (EOG) was recorded between stainless-steel wire leads 1The investigation was supported by National Aeronautics and Space Administration under contract NSR 05-007-158 and by the National Institute of Neurological Diseases and Stroke, National Institutes of Health, U.S.
Public Health Service under Grant NB 02501.
placed in the ventral lateral orbital ridge and medial dorsal orbital ridge of the right eye. The electromyogram (EMG) was recorded from an electrode in the posterior neck muscles. Each animal was monitored from at least 30 min before lights out at 19.00 to at least 30 min after lights on at 07.00 by closed television and by telemetered EEG, EOG and EMG for 7 consecutive nights. The animal was adapted to the television camera, the telemetry aerial beneath his cage and the telemetry pack for at least one week before the recording. Kelly had participated in a previous 7 consecutive night study; Corky had not. The records were scored by a slight modificat:on of the Rechtschaffen and Kales (1968) modification of the Dement and Kleitman scoring rules for human sleep stages. The EMG showed a decrease in amplitude during transition from wakefulness to sleep but was not helpful in differentiating REM (rapid eye movement) from nonREM sleep. All scoring was done on the basis of the cortical EEG channels and the EOG without reference to the electrical activity of subcortical structures. When each 20 sec epoch was scored strictly according to the rules, changes between waking (W) and 1 and among stages 2, 3 and 4 were too frequent to make a graph of these changes intelligible. We therefore "smoothed" the graph by transforming 9 successive groups of 20 sec epochs into one 3 min epoch by extracting that sleep stage which occupied a majority or plurality of the 9 epochs. RESULTS
As summarized in Table I, one of our animals showed less REM, less stage 4, and more W on Electroenceph. olin. Neurophysiol., 1971, 31:485489
486
F . R . FREEMON e t a l .
KELLY
TABLE I 20 0O
A comparison of the first experimental night to the average of nights 2-7 for each animal. Time in minutes. Corky
' N
!
r~w 2N
Kelly
Sleep stage
First night
Nights 27
First night
Nights 2-7
W 1 2 3 4 REM
89.0 58.7 274.3 91.0 58.7 148.7
61.4 42.7 274.1 97.3 84.1 160.1
104.7 58.7 242.0 87.3 61.7 148.0
63.0 57.7 302.1 94.1 52.1 141.0
22 00
i
2400
~
~
0200
. ~
.
. -
~
04 00
.
. ~
. j
~ j ~ _
w
aN ~ R i ~ I ~ d ~ f ~ ~
~
0600
.
.
~.~
~J~F
4 NR~32r ~EI
r~h,l-tl~hn~ 5 NR32 ~,~E
~,- ~j
n,,, iMn~ ~ ~lk~l~p,n,~ ~;~LF u--~-~L_/~-~-q_j--rLl UUl/- I I U
TABLE II Time (in minutes)spent by each animal in each sleep stage is an average of experimental nights 2-7. The results are broken down by 3 h periods from 1900 to 0700. In most instances, the sleep stages do not add exactly to 180 min for any fourth of the night, because a few epochs were obliterated by telemetry
7 dRi'i~ ~ RE~- .
artifact.
~
Sleep stage
Fourth of the night 3
Total 4
Percentage of sleep
12.8 63.0 16.1 57.7 8 5 . 7 302.1 8.1 94.1 0.6 52.1 4 9 . 3 141.0
-9 47 14 8 22
1
2
32.8 20.9 51.3 34.0 28.0 11.4
6.0 1 1 . 4 7.7 1 3 . 0 72.7 92.4 2 9 . 3 22.7 20.2 3.3 44.1 36.2
W 1 2 3
16.4 11.7 54.4 29.8
13.3 11.8 19.9 61.4 8.4 9.8 118 42.7 7 4 . 3 6 7 . 7 7 7 . 7 274.1 2 8 . 6 2 4 . 9 14.0 97.3
4 REM
41.5 26.9
2 7 . 0 14.6 1.0 84.1 2 7 . 8 5 1 . 2 5 4 . 2 160.1
.
~ .
~
[ - - ~ F_a__~ U , ~ u~
.
CORKY ~o
~
~o
3
rI
z N,tRE~32
2~o0
02oo
i
W
~
o4oo
o~0o __
~
3 NR32 tRE~ a
Kelly
W 1 2 3 4 REM
[-~ .
Corky
N~3] 4
R~
~w NR132 5 t E~ ~ 1w
-
-
6 42 15 13 24
the first experimental night than on the average of nights 2-7. Further analysis is restricted to nights 2-7 in order to be sure that a "first night effect" does not muddy our description of sleep patterns in normal juvenile chimpanzee. The animals were out of their cages and awake during the day, except after lunch from about 12.00 and 13.30 when they sometimes napped. Although these naps were not analyzed in detail, REM periods were seen. Behavioral
6LR~M4~
~'h~L~
~LI
"~LJ
"I~''lJU
L]''U
7 ~.~I.,'~' Fig. 1. Cyclic activity during 7 consecutive nights (1 7) of sleep in two chimpanzees. W=waking, NR 1-4=nonREM sleep stages, REM =REM sleep.
observations and 24 h recordings demonstrated that with this exception, the animals were awake throughout the day. Between lights out at 1900 and lights on at 0700, the two animals spent an average of 652.4 min asleep and 62.2 rain awake. An average of 5.4 rain per night was obscured by artifact. Of the time asleep, 8 ~ was nonREM stage 1, 4 4 ~ stage 2, 15 ~ stage 3, 10 ~ stage 4 and 23 % stage REM. Table II breaks down these averages by E/ectroenc~Th. c/in. N e u r o p h y s i o l . ,
1971, 31 : 485 489
CHIMPANZEE SLEEP STAGES
487
TABLE III
wakefulness than did our animals. Bert et al. u s e d phencyclidine to sedate their animals for battery changes, whereas our animals, who could recorded in the present study, be handled for battery changes, had received no CNS depressants since electrode implantation Bert et al. (1970) Present over a year before recording. Sedatives decrease study the percentage of sleep spent in the REM stage, Total time of study 14 h 12 h and the chronic use of hypnotic medication can Time awake 260rain 62 min produce long-term effects on sleep; however, Time asleep 580 rain 652 min Bert et al. restricted analysis to those nights when Sleep stage(~o) the animals had not received phencyclidine for 1 14 8 2 32 44 at least the preceding 48 h, and it seems unlikely 3 29 15 that the animals received sedation so often as to 4 10 l0 demonstrate the chronic effects of the drug on REM 15 23 sleep. Differences in scoring methods might explain the differences between stages 1, 2 and 3, animal and by fourths of the night. The majority but the scoring of the REM type of sleep is of stage 2 and much of stage REM occurred straightforward; the combination of eye moveduring the latter portions of the sleeping period, ments and low voltage mixed frequency EEG is whereas almost all of stage 4 took place before quite distinct. A R E M period usually begins in 0100. chimpanzee with the change in EEG preceding the Fig. 1 gives the smoothed graphed data from first eye movement by up to a minute. Often a each animal for each night. One can see that burst of saw-tooth shaped waves in the EEG 7-9 complete REM periods occurred each night, heralds the onset of the REM period. We scored From the graphs, one can calculate the sleep the beginning of the REM period as the time of cycle length, defined as the length of time from the EEG change. If Bert et al. restricted the bethebeginningofoneREMperiodtothebeginning ginning of a REM period to the first eye moveof the next REM period. For nights 2-7, the ment, this could possibly explain a small portion ,sleep cycle averaged 86.1 min (range 42-171) in of the difference between their and our REM Kelly and 85.2 rain (range 36-144) in Corky. percentages. We suspect that the major difference in DISCUSSION results, however, is a function of the age of the animals. Our animals were approximately 4 Table III contrasts the results of the present years old, were sexually immature, and weighed study with the previous results of Bert et al. approximately 18 kg. Bert et al. studied sexually (1970). The animals in the previous study were mature chimpanzees weighing 39 52 kg. In awake longer and had less stage R E M than our several species, including man, the younger animals. In addition, there were differences individual has a higher REM percentage and a among nonREM stages, particularly stages 2 longer total sleep time than older members of and 3. The percentage of sleep spent in stage 4 the same species (Roffwarg et al. 1966). Age is the was identical in the two studies. Since these are major distinguishing characteristic between our the only two quantitative studies of unrestrained chimpanzees and those of Bert et al., and our chimpanzee in which sleep stages were defined in results, taken together, are most easily intera manner analogous to Dement and Kleitman's preted as indicating that in chimpanzee, as in sleep stages for man, we will try to explain the man, the adolescent has a greater REM percendifferences in results, tage and a longer sleeping time than has the Bert et al. studied 14 h of sleep, from 1700 to adult. 0700, whereas we studied 12 h only. Even if the Bert et al. attribute a portion of the difference 2 h of difference were spent in wakefulness, the between the sleep of their chimpanzees and the animals of Bert et al. had greater amounts of sleep of man to environmental differences. They Comparison of the sleep of mature chimpanzee as studied by Bert et al. with the sleep of juvenile chimpanzee as
Electroenceph. clin. Neurophysiol., 1971, 3l: 485 489
488 suggest that the frequent awakenings in their study are related to the fact that their animals, although unrestrained in the sense that they are not tied to a chair, are restrained as compared to chimpanzees living in the wild, sleeping in trees. They point out that attempts to measure natural sleep will never be entirely successful since the very act of recording changes the nature of sleep, a sort of a Heisenberg principle of sleep research. It is possible that differences in environment at the Aeromedical Research Laboratory, Holloman Air Force Base, where Bert's experiments were performed, and at Space Biology Laboratory, UCLA, might account for some of the differences in the results of these two studies. The Aeromedical Research Laboratory, for instance, has part of its cage out-ofdoors, where seasonal variations in lighting could conceivably affect sleep patterns, whereas at the Space Biology Laboratory the chimpanzees spend their lives in a large but windowless room. Another important environmental difference is that our animals have undergone extensive domestication procedures producing dependence upon human trainers who handle and play with the chimps daily, whereas the Holloman animals are not tamed, and handling involves drugs and forced restraint. The two groups would naturally acquire different responses toward an experimental situation involving the presence of man. Studies of the effect of environment on sleep have lagged behind studies describing species, age and drug-induced effects on sleep patterns, and we cannot know, at the present time, what effect environment has on chimpanzee sleep. Another way of comparing the results of the present study with the previous results of Bert et al. is to emphasize the areas of agreement. Two different laboratories studying two different age groups of chimpanzees in two different environments have produced somewhat similar results, For example, we can say with total confidence that chimpanzee sleep can be divided into stages analogous to Dement and Kleitman's sleep stages for man. We can say that approximately 10 ~ of chimpanzee sleep is nonREM stage 4, a characteristic type of sleep with large amounts of delta activity in the EEG. We can say that a significant proportion of chimpanzee sleep is
F.R. FREEMONet al. spent in the REM type of sleep. With individual differences, age differences, environmental differences, procedural differences, could we really have expected greater agreement? SUMMARY Using telemetry methods, we monitored the electroencephalogram and electro-oculogram of two unrestrained juvenile chimpanzees for 7 consecutive nights. The all-night records were scored by a slight modification of the rules developed by Dement and Kleitman for human sleep. The chimpanzees spent an average of 652 rain asleep and 62 rain awake. Of the sleeping time, 23 ~ was spent in the rapid eye movement or REM type of sleep, whereas 8, 44, 15 and 10~ were spent in nonREM stages 1 through 4 respectively. Seven to nine periods of REM sleep occurred per night. The average time from the beginning of one REM period to the beginning of the next was approximately 85 min. RESUME STADES DE SOMMEIL DU CHIMPANZE
A l'aide de m6thodes t616m6triques, nous avons enregistr6 l'61ectroenc6phalogramme et l'61ectro-oculogramme de deuxjeunes chimpanz6s lihres de leurs mouvements pendant 7 nuits cons6cutives. Les enregistrements de route la nuit ont ~t6 quantifi6s en modifiant 16g~rement les r6gles mises au point par Dement et Kleitman pour le sommeil humain. Les chimpanz6s ont pass4 en moyenne 652 min fi dorrnir et 62 min 6veill6s. Dans ce temps de sommeil, 23~ consistent en activit6s de mouvements oculaires rapides ou phases de mouvements oculaires (PMO) de sommeil, alors que 8, 44, 15 et 10~ respectivement sont d6volus aux stades 1 ~t 4 du sommeil lent. Sept ~t neuf p6riodes de PMO par nuit ont 6t6 d6nombr6es. Le temps moyen du d6but d'une p6riode de mouvements oculaires rapides au commencement de la suivante est d'environ 85 min.
The authors wish to thank Dr. J. Bert for commenting on
an earlier draft of this paper. Electroenceph. clin. Neurophysiol., 1971, 31 : 485-489
CHIMPANZEE SLEEP STAGES
REFERENCES ADEY, W. R., KADO, R. T. and RHODES, J. M. Sleep: cortical and subcortical recordings in the chimpanzee. Science, 1963, 141: 932-933. BERT, J., KR1PKE, D. F. and RHODES, J. M. Electroencephalogram of the mature chimpanzee: 24 hour recordings. Electroenceph. clin. Neurophysiol., 1970, 28:368 373. FREEMON, F. R., MCNEw, J. J. and ADEY, W. R. Sleep of unrestrained chimpanzee: cortical and subcortical recordings. Exp. Neurol., 1969, 25: 129-137. RECHTSCHAFFEN, A. and KALES, A. (Eds.). A manual 0/"
489 standardized terminolo.qy, techniques, and scorinq system jbr sleep staqes o/ human suh/ects. NIH, Publication 204, U.S. Government Printing Office, Washington, D.C., 1968, 55 p. RtCKLES, W. R. A study of EEG and somato-veoetative physiolooy of the immature chimpanzee durin# sleep. Aeromedical Res. Lab. Technol. Rept. No. 64-19, Holloman Air Force Base, New Mexico, 1965, 55 p. ROFFWARG,H. P., MUZIO, J. N. and DEMENT, W. C. Ontogenetic development of the human sleep-dream cycle. Science, 1966, 152: 604--619.
ReJbrence: FREEMON, F. R., McNEw, J. J. and ADEY, W. R. Chimpanzee sleep stages. Electroenceph. clin. Neurophysiol., 1971, 31:485 489.