Nocturnal Sleep in Isolation-Reared Monkeys: Evidence for Environmental Independence MARTIN REITE ROBERT SHORT De velopm en tal Psycho biology Research Group Department of Psychiatry University of Colorado Medical Center Denver. Colorado Thirteen all-night sleep recordings were obtained from 3 infant pigtailed (MUCQCU nemestrina) monkeys raised on a cloth surrogate mother under conditions of social isolation. Totally implantable biotelemetry systems were used to record the sleep physioIogy from the unrestrained animals. Sleep stages and night-to-night variability were virtually identical to values previously found in 8 mother-reared group-Iiving infants. Sustained alterations in the early rearing environment, even though considerably modifying the organism’s development, did not appear to result in differences in sieep organization.
Previous studies of nocturnal sleep in several primate species have demonstrated both considerable variability in sleep patterns among closely related species (Bert, Pegram, & Balzano, 1972) and prominent night-to-night variability in members of the same species (Clausen, Sersen, & Lidsky, 1974; Reite Stynes, Vaughn, Pauley, & Short, 1976). Bert and Pegram (1972) have suggested that 3 factors influence the organization of sleep: (1) a genetic factor; (2) a learning factor; and (3) an environmental factor. Our laboratory has been studying the influence of altered early environments on behavioral and physiological development in pigtailed macaque (Macaca nemestrina) monkeys, including the effects of partial social isolation. Social isolation rearing may produce significant deficits in later individual and social competence in monkeys, as well as varying degrees of individual behavioral peculiarities (Harlow, 1964; Mason, 1968; Sackett, Holm, & Ruppenthan, 1976). Relatively little is known of the physiological development of such infants, however. In the present study, nocturnal sleep patterns were recorded from 3 pigtailed infants raised in partial social isolation on cloth surrogate mothers, and were compared t o similar data previously obtained from 8 mother-reared social-group-living pigtail infants. Of special note is the fact that these data were obtained utilizing totally implantable multichannel biotelemetry systems. With few exceptions, most previous studies on sleep in man and other species have entaded variations on hard-wire Reprint requests should be sent to Martin Reite, M.D., Department of Psychiatry, Box C 2 6 8 , University of Colorado Medical Center, 4200 East Ninth Avenue, Denver, Colorado, U.S.A. Received for publication 1 November 1976 Revised for publication 14 December I976
Developmental Psychobiology, lO(6): 555-561 (1977)
@ 1911 by John Wiley & Sons, Inc.
555
556
REITE AND SHORT
recording systems which, unavoidably, induce some degree of environmental change merely to collect the sleep data. Implantable telemetry technology bypasses this requirement. No changes at all need to be introduced into the environment in order to collect the sleep data, and the data should be considerably more reliable.
Methods The 3 experimental infants were born of feral-born mothers who had been living in the Department of Psychiatry Primate Laboratory for several years. The infants were removed from their mothers within approximately 24 hr of birth and were housed initially in cardboard boxes lined with towels. Supplemental heat was provided by an electric heating pad in the bottom of the box. l l i e infdnts were fed by hand from standard nursing bottles. During the 1st 24 hr they were @en 1OCh glucose and water; during the 2nd 24 hr, a 50-SO mixture of 1% glucose and Similac' ; and after 48 hr, undiluted Similac. Initially, feedings were essentially on demand. As soon as the infants were able to support themselves adequately, a nursing bottle on a ring stand was added to the box and they were allowed to feed as often as they desired. They were provided with a brown cloth surrogate within the 1st several weeks of life and evidenced attachment to this surrogate quite early. Between the ages of 3 and S weeks, they were moved to a 50 x SO x 50-cm epoxy-coated, wooden cage that was kept in a well-ventilated room where the ambient temperature was maintained at a nominal 25°C. Their cages contained only the surrogates and plastic chains suspended from the tops of the cages. No supplemental heating was provided after the move to the surrogate cage. Timercontrolled lights were off between 2000 and 0700 hours. The infants were raised with a mininzum of human contact except that necessary for cage cleaning and maintenance. They had n o visual contact with other animals and limited visual and auditory contact with ongoing activity in the laboratory. Thus, their social isolation (from other monkeys) was total; other sensory input was only slightly attenuated. By 3 months of age they were being fed twice daily at 0900 and 1600 hours; their diet consisted primarily of Purina monkey biscuits. The infants were surgically implanted with a multichannel biotelemetry system at the ages of 19, 24, or 28 weeks (mean: 23.7 weeks). Th: telemetry systems have been described previously (Pauley, Reite, & Walker, 11974). The infants were returned to their surrogate cages following recovery from surgical anesthesia; sutures were removed 10 days following surgery. Physiological and behavioral data collection began shortly thereafter. Details of our data collection system have been previously described (Reite, Pauley, Walker, Kaufman, & Stynes, 1974b). Briefly, the telemetered signal was received on a modified commercial FM receiver, demodulated, and recorded timelocked on a polygraph and a 7-channel FM instrumentation tape recorder. Physiological data relevant to sleep recordings included EOG. EMG, and 3 channels of extradural EEG. The infants were continuously monitored during the day with an infrared-sensitive closed-circuit video system, and were episodically rnonitored during the night with infrared illumination,
SLEEP IN ISOLATION-REARED MONKEYS
557
The data described in this report were obtained during 4-5 normal (baseline) 24-hr periods recorded from each infant that preceded other experimental manipulations. All baseline recordings were conducted on weekdays (i.e., Monday through Friday). Nocturnal sleep (2000 to 0700 hours) was recorded from the paper record. Sleip scoring criteria were based on previous work in adult M. nernestrina monkeys (Reite, Rhodes, Kavan, & Adey, 1965) with modifications appropriate to the younger animals (Reite, Pauley, Kaufman, Stynes, & Marker, 1974a). Sleep stages included Drowsy, Stage 2, Stage 3 4 (combined), and REM. Other sleep variables measured for each infant each night included sleep latency, time spent awake, total sleep time (TST), REM latency, number of REM periods (NREMP’s), and the inter-REM interval (IRI). Scoring procedures were identical to those used in a recent publication describing normal sleep patterns in group-living pigtailed infants (Reite et aZ., 19762).
Results AS has been reported in other studies in which monkey infants were raised under varying conditions of social isolation, these infants exhibited self-clasping, self-mouthing, and rocking behaviors. They avoided human contact and would retreat to their surrogate, rocking and screaming, when approached. A total of 13 all-night sleep recordings were obtained from the 3 surrogatereared infants. A summary of sleep data is presented in Table 1. As inspection of Table 1 indicates time spent awake, time spent in Stage 2 sleep, Stage 3-4 sleep, and REM sleep were virtually identical in the socially-isolated and the groupliving infants. The number of REM periods, inter-REM interval, and total sleep time were very similar in the 2 groups, which were not separable by statistical tests. The surrogate-reared infants did exhibit a greater amount of Stage Drowsy during the night than did the group-living infants (t = 5.02, df = 9, p < .Ol) and a significantly shorter sleep latency ( t = 2.91, df = 9 , p < .05).3 Sleep latency in group-living infants has been shown to be related to maternal dominance (Reite et al., 1976), with infants of low dominance mothers tending to have longer sleep latencies, possibly because low dominance animals require a longer period of time to settle securely into a sleeping location. Thus, this appears to be a mother- or social-group-related variable and, thus, we were not surprised that our surrogate-reared infants, without these influences, had shorter sleep latencies. We have no explanation at this point as to why the surrogate-reared infants exhibited a greater amount of Stage Drowsy than did the group-reared infants. This difference may have accounted for the slight differences in TST between the 2 groups, however, as when TST minus Drowsy was compared for the 2 groups they were, too, nearly identical.
Discussion Although we believe our results should not, because of the relatively small N , be considered definitive, they strongly suggest that nocturnal sleep is remarkably
5
13
31
F
208
180 r 30
15.4
Group means
Normal valuesb 180 + 25
5 0 + 32
S O + 23
67 + 2 3
44i9
3 4 1 12a
Awake ( j i SD)
t = 5.02‘ p < .01
16-r 7
39-r 13
28+ 7
52t13
41 2 4
Drowsy (b+SD)
_
_
302i: 31
151 t 27
1 6 8 t 22 1 5 1 + 21
301 + 39
130+9
149t 5
(bt SD)
St. 3 + 4
2 6 6 + 27
321i.35
3 2 3 + 22
St. 2 (2-rSD)
~ ~
9 0 2 20
8 9 t 16
8 4 + 14
97+21
8 6 t 11
REM ( g +SD)
~~~~~
t
14
t = 2.91 p < .05
35
1 8 t 11
2 2 t 17
11+5
18-r 5
Sleep Latency (Ti: SD)
9 . 2 + .34
9.5-r.58
8 . 8 + .96
NREMP’s (TtSD)
6 2 + 33
9 . 6 + 1.60
6 7 + 2 1 9.2r.80
5 3 + 11
84t21
6 8 t 19
REM Latency ( d *SD)
t
7
59+ 6
65t6
66+ 6
62t3
67
IRI (2+ SD)
5 5 8 t 33
5 8 5 + 36
549 + 32
606t11
6 0 9 %15
(Pi:SD)
TST
aAll values (except NREMP’s) are in minutes. bFor comparative purposes, this row contains normative values previously obtained from 8 similar-aged, group-living infants who were recorded a total of 31 nights (from Riete e r al., 1976). ‘t tests were performed for each variable using the mean value for each animal (one group of 3 and one group of 8). Only significant t scores are listed.
4
4
M
M
149
Sex
183
No. Nights
11.3
Age (days)
11.4
Animal Number
Telemetered Sleep Recordings.
TABLE 1. Nocturnal Sleep Variables Recorded from 3 Surrogate-Reared Socially Isolated M. nemestrina Infants During 13 All-Night
2
2
1/1
zU
SLEEP IN ISOLATION-REARED MONKEYS
559
similar for socially-isolated, surrogate-reared pigtailed monkey infants and groupliving, mother-reared infants. The fact that the considerably less complex (“impoverished”) environment of isolation-reared infants did not significantly influence basic sleep stage organization is suggestive that such organization may, in large part, be intrinsically determined. Individual (and presumably genetically determined) differences in the organization of sleep-waking cycles in the newborn rhesus (M.rnulatta) monkey were also found by Meier and Berger (1965), although we should emphasize that the infants reported in this study were not newborn. Studies in rodents have suggested a significant genetic component to sleep pattern regulation (Friedman, 1974; Van Twyver, Webb, Dube, & Zackheim, 1973), but similar experiments have yet t o be reported in primates. We, of course, do not suggest that sleep patterns are free of environmental influences. Sander has demonstrated that the nature of the early caretaker-infant interaction can significantly influence sleep-waking patterns in the human newborn (Sander, Stechler, Burns, & Julia, 1970), although even in these studies he (Sander, 1969) reported evidence of a non-environmental (possibly genetic) influence intrinsic t o the organism, observations supported by the recent work of Emde, Swedberg, and Suzuki (1975). Bert and Pegram (1972) have demonstrated that environmental differences can significantly influence sleep patterns in adult baboons. What does seem apparent, however, is that those specific elements of the early rearing environment that were different in our isolation-reared infants and our group-reared infants did not significantly influence sleep pattern organization, even though they were of a nature and magnitude sufficient to alter markedly the organism’s development. Although the environments in which the isolated monkeys and group-living monkeys were raised were very different, they did contain one important element in common, the 13: 1 1-hr light-dark cycle. Certainly this may represent a significant environmental variable whose role may be considerable in terms of shaping the sleep pattern. Of considerable interest is the fact that not only were mean sleep values very similar, but so was the degree of variability. The considerable night-to-night sleep pattern variability previously found in group-living monkey infants was thought at the time to be related to as of yet undetected social influences (e.g., stresses) which had occurred during the day (Reite et al, 1976). The present data suggest, however, that because the variability persists in an environment in which relatively few changes occur, such night-to-night sleep stage variability may well be in large part intrinsic to the organism, and essentially free of environmental determinants. This persistent night-to-night variability suggests that researchers who purport t o demonstrate the influence of short-term environmental or experimental alterations on sleep should approach the problem from the standpoint that the intrinsic “noise” (variability) in the system is large, and a signal (environmentally induced sleep pattern changes) may be small by comparison. Thus, by failing to consider the problem from the standpoint of the signal-to-noise ratio, with the data processing techniques so mandated, the researcher may lose considerable valuable experimental data and that which he reports may be especially prone to “Type 11” statistical errors.
560
REITE AND SHORT
In summary, we were surprised that sleep patterns in the restricted condition, with the absence of social interaction and stimulation (and the immense amount of learning this must entail), did not differ from the group-living situation. We hope that continued experimental work of this nature will help devine the role of sleep pattern organization in the developing organism, the critical variables that influence such organization, and how those influences become manifest.
Notes 'Trademark registered, Ross Laboratories, Columbus, Ohio 43216. *The lights-out period was 11 hr (660 min) long; this would be the maximum amount of sleep an animal could obtain, assuming a zero sleep latency. Time Awake included only those awakenings occurring after sleep onset (e.g., sleep latency not included) and prior to the final morning awakening (which often preceded lights-on). Thus the total of sleep latency, TST, and Awake will approximate 660 min, differing significantly from this only when the animals awakened prior to lights-on in the morning. 'All values in Table 1 do not add up exactly due to computer roundoff error in the sleep scoring program (see Reite et al., 1976).
This research was supported by USPHS Research Grant No. MH19514 and NIMH Research Scientist Development Award No. 5 K 0 2 MH46335, both t o M. Reite. We thank Dr. I. Charles Kaufman for his thoughtful and helpful criticism of this manuscript.
References Bert, J., and Pegram, V. (1972). Sleep and Environment. In J. Moor-Janowski (Ed.), Proceedings 3rd Conference on Experimental Medicine and Surgery in Primates, Part II. New York: Karger. Pp. 244-249. Bert, J., Pegram, V., and Balzano, E. (1972). Comparison du sommeil de deux macaques (Macaca radiata et Macaca mulatta). Folia Primat., 1 7 : 202-208. Clausen, J., Sersen, E. A., and Lidsky, A. (1974). Variability of sleep measures in normal subjects. Psychophysiol., I 1 : 509-516. Emde, R. N., Swedberg, J., and Suzuki, B. (1975). Human wakefulness and biological rhythms after birth. Arch. Gen. Psychiat., 3 2 : 780-783. Friedman, J . K . (1974). A diallel analysis of the genetic underpinnings of mouse sleep. Physiol. Behav., 1 2 : 169-175. Harlow, H. F. (1964). Early social deprivation and later behavior in the monkey. In A. Abrams, H. H. Garner, and J. E. P. Tomal (Eds.), Unfinished Tasks in the Behavioral Sciences. Baltimore: Williams and Williams. Pp. 154-173. Mason, W. A. (1968). Early social deprivation in the nonhuman primates: Implications for human behavior. In D. C. Glass (Ed.), Environmental Influences. New York: The Rockefeller University Press. Pp. 70-101. Meier, G. W., and Berger, R. J . (1965). Development of sleep and wakefulness patterns in the infant rhesus monkey. Exp. Neurol., 1 2 : 257-277. Pauley, J. D., Reite, M. L., and Walker, S. D. (1974). An implantable multichannel biotelemetry system. Electroencephalogr. Clin. Neurophysiol., 3 7 : 153-160. Reite, M., Pauley, J . D., Kaufman, I. C., Stynes, A. J., and Marker, V. (1974a). Normal physiological patterns and physiolopcal-behavioral correlations in unrestrained monkey infants. PhysioZ. Behav., 1 2 : 1021-1033. Reite, M., Pauley, J. D., Walker, S., Kaufman, I. C., and Stynes, A. J. (1974b). A systems approach to studying physiology and behavior in infant monkeys. J. Appl. Physiol., 3 7 : 4174;!3.
SLEEP IN ISOLATION-REARED MONKEYS
56 1
Reite, M. L. Rhodes, J. M., Kavan, E., and Adey, W. R. (1965). Normal sleep patterns in macaque monkeys. Arch. Neurol., 12: 133-144. Reite, M., Stynes, A. J., Vaughn, L., Pauley, J. D., and Short, R. A. (1976). Sleep in infant monkeys: Normal values and behavioral correlates. Physiol. Behav., 16: 245-251. Sackett, G. P., Holm,R. A., and Ruppenthal, G. C. (1976). Soda1 isolation rearing: Species differences in behavior of macaque monkeys. Devel. Psychol. 12: 283-288. Sander, L. W. (1969). Regulation and organization in the early infantcaretaker system. In R. J. Robinson (Ed.), Brain and Early Behavior. New York: Academic Press, Pp. 31 1-333. Sander, L. W., Stechler, G., Burns, P., and Julia, H. (1970). Early mother-infant interaction and 24-hour patterns of activity and s1eep.J. Am Acad. Child. Psychiat., 9 : 103-123. Van Twyver, H., Webb, W. B., Dube, M., and Zackheim, M. (1973). Effects of environmental and strain differences on EEG and behavioral measurement of sleep. Behm. BioZ.,9: 105-110.
Previous studies of nocturnal sleep in several primate species have demonstrated both considerable variability in sleep patterns among closely related species (Bert, Pegram, & Balzano, 1972) and prominent night-to-night variability in members of the same species (Clausen, Sersen, & Lidsky, 1974; Reite Stynes, Vaughn, Pauley, & Short, 1976). Bert and Pegram (1972) have suggested that 3 factors influence the organization of sleep: (1) a genetic factor; (2) a learning factor; and (3) an environmental factor. Our laboratory has been studying the influence of altered early environments on behavioral and physiological development in pigtailed macaque (Macaca nemestrina) monkeys, including the effects of partial social isolation. Social isolation rearing may produce significant deficits in later individual and social competence in monkeys, as well as varying degrees of individual behavioral peculiarities (Harlow, 1964; Mason, 1968; Sackett, Holm, & Ruppenthan, 1976). Relatively little is known of the physiological development of such infants, however. In the present study, nocturnal sleep patterns were recorded from 3 pigtailed infants raised in partial social isolation on cloth surrogate mothers, and were compared t o similar data previously obtained from 8 mother-reared social-group-living pigtail infants. Of special note is the fact that these data were obtained utilizing totally implantable multichannel biotelemetry systems. With few exceptions, most previous studies on sleep in man and other species have entaded variations on hard-wire Reprint requests should be sent to Martin Reite, M.D., Department of Psychiatry, Box C 2 6 8 , University of Colorado Medical Center, 4200 East Ninth Avenue, Denver, Colorado, U.S.A. Received for publication 1 November 1976 Revised for publication 14 December I976
Developmental Psychobiology, lO(6): 555-561 (1977)
@ 1911 by John Wiley & Sons, Inc.
555
556
REITE AND SHORT
recording systems which, unavoidably, induce some degree of environmental change merely to collect the sleep data. Implantable telemetry technology bypasses this requirement. No changes at all need to be introduced into the environment in order to collect the sleep data, and the data should be considerably more reliable.
Methods The 3 experimental infants were born of feral-born mothers who had been living in the Department of Psychiatry Primate Laboratory for several years. The infants were removed from their mothers within approximately 24 hr of birth and were housed initially in cardboard boxes lined with towels. Supplemental heat was provided by an electric heating pad in the bottom of the box. l l i e infdnts were fed by hand from standard nursing bottles. During the 1st 24 hr they were @en 1OCh glucose and water; during the 2nd 24 hr, a 50-SO mixture of 1% glucose and Similac' ; and after 48 hr, undiluted Similac. Initially, feedings were essentially on demand. As soon as the infants were able to support themselves adequately, a nursing bottle on a ring stand was added to the box and they were allowed to feed as often as they desired. They were provided with a brown cloth surrogate within the 1st several weeks of life and evidenced attachment to this surrogate quite early. Between the ages of 3 and S weeks, they were moved to a 50 x SO x 50-cm epoxy-coated, wooden cage that was kept in a well-ventilated room where the ambient temperature was maintained at a nominal 25°C. Their cages contained only the surrogates and plastic chains suspended from the tops of the cages. No supplemental heating was provided after the move to the surrogate cage. Timercontrolled lights were off between 2000 and 0700 hours. The infants were raised with a mininzum of human contact except that necessary for cage cleaning and maintenance. They had n o visual contact with other animals and limited visual and auditory contact with ongoing activity in the laboratory. Thus, their social isolation (from other monkeys) was total; other sensory input was only slightly attenuated. By 3 months of age they were being fed twice daily at 0900 and 1600 hours; their diet consisted primarily of Purina monkey biscuits. The infants were surgically implanted with a multichannel biotelemetry system at the ages of 19, 24, or 28 weeks (mean: 23.7 weeks). Th: telemetry systems have been described previously (Pauley, Reite, & Walker, 11974). The infants were returned to their surrogate cages following recovery from surgical anesthesia; sutures were removed 10 days following surgery. Physiological and behavioral data collection began shortly thereafter. Details of our data collection system have been previously described (Reite, Pauley, Walker, Kaufman, & Stynes, 1974b). Briefly, the telemetered signal was received on a modified commercial FM receiver, demodulated, and recorded timelocked on a polygraph and a 7-channel FM instrumentation tape recorder. Physiological data relevant to sleep recordings included EOG. EMG, and 3 channels of extradural EEG. The infants were continuously monitored during the day with an infrared-sensitive closed-circuit video system, and were episodically rnonitored during the night with infrared illumination,
SLEEP IN ISOLATION-REARED MONKEYS
557
The data described in this report were obtained during 4-5 normal (baseline) 24-hr periods recorded from each infant that preceded other experimental manipulations. All baseline recordings were conducted on weekdays (i.e., Monday through Friday). Nocturnal sleep (2000 to 0700 hours) was recorded from the paper record. Sleip scoring criteria were based on previous work in adult M. nernestrina monkeys (Reite, Rhodes, Kavan, & Adey, 1965) with modifications appropriate to the younger animals (Reite, Pauley, Kaufman, Stynes, & Marker, 1974a). Sleep stages included Drowsy, Stage 2, Stage 3 4 (combined), and REM. Other sleep variables measured for each infant each night included sleep latency, time spent awake, total sleep time (TST), REM latency, number of REM periods (NREMP’s), and the inter-REM interval (IRI). Scoring procedures were identical to those used in a recent publication describing normal sleep patterns in group-living pigtailed infants (Reite et aZ., 19762).
Results AS has been reported in other studies in which monkey infants were raised under varying conditions of social isolation, these infants exhibited self-clasping, self-mouthing, and rocking behaviors. They avoided human contact and would retreat to their surrogate, rocking and screaming, when approached. A total of 13 all-night sleep recordings were obtained from the 3 surrogatereared infants. A summary of sleep data is presented in Table 1. As inspection of Table 1 indicates time spent awake, time spent in Stage 2 sleep, Stage 3-4 sleep, and REM sleep were virtually identical in the socially-isolated and the groupliving infants. The number of REM periods, inter-REM interval, and total sleep time were very similar in the 2 groups, which were not separable by statistical tests. The surrogate-reared infants did exhibit a greater amount of Stage Drowsy during the night than did the group-living infants (t = 5.02, df = 9, p < .Ol) and a significantly shorter sleep latency ( t = 2.91, df = 9 , p < .05).3 Sleep latency in group-living infants has been shown to be related to maternal dominance (Reite et al., 1976), with infants of low dominance mothers tending to have longer sleep latencies, possibly because low dominance animals require a longer period of time to settle securely into a sleeping location. Thus, this appears to be a mother- or social-group-related variable and, thus, we were not surprised that our surrogate-reared infants, without these influences, had shorter sleep latencies. We have no explanation at this point as to why the surrogate-reared infants exhibited a greater amount of Stage Drowsy than did the group-reared infants. This difference may have accounted for the slight differences in TST between the 2 groups, however, as when TST minus Drowsy was compared for the 2 groups they were, too, nearly identical.
Discussion Although we believe our results should not, because of the relatively small N , be considered definitive, they strongly suggest that nocturnal sleep is remarkably
5
13
31
F
208
180 r 30
15.4
Group means
Normal valuesb 180 + 25
5 0 + 32
S O + 23
67 + 2 3
44i9
3 4 1 12a
Awake ( j i SD)
t = 5.02‘ p < .01
16-r 7
39-r 13
28+ 7
52t13
41 2 4
Drowsy (b+SD)
_
_
302i: 31
151 t 27
1 6 8 t 22 1 5 1 + 21
301 + 39
130+9
149t 5
(bt SD)
St. 3 + 4
2 6 6 + 27
321i.35
3 2 3 + 22
St. 2 (2-rSD)
~ ~
9 0 2 20
8 9 t 16
8 4 + 14
97+21
8 6 t 11
REM ( g +SD)
~~~~~
t
14
t = 2.91 p < .05
35
1 8 t 11
2 2 t 17
11+5
18-r 5
Sleep Latency (Ti: SD)
9 . 2 + .34
9.5-r.58
8 . 8 + .96
NREMP’s (TtSD)
6 2 + 33
9 . 6 + 1.60
6 7 + 2 1 9.2r.80
5 3 + 11
84t21
6 8 t 19
REM Latency ( d *SD)
t
7
59+ 6
65t6
66+ 6
62t3
67
IRI (2+ SD)
5 5 8 t 33
5 8 5 + 36
549 + 32
606t11
6 0 9 %15
(Pi:SD)
TST
aAll values (except NREMP’s) are in minutes. bFor comparative purposes, this row contains normative values previously obtained from 8 similar-aged, group-living infants who were recorded a total of 31 nights (from Riete e r al., 1976). ‘t tests were performed for each variable using the mean value for each animal (one group of 3 and one group of 8). Only significant t scores are listed.
4
4
M
M
149
Sex
183
No. Nights
11.3
Age (days)
11.4
Animal Number
Telemetered Sleep Recordings.
TABLE 1. Nocturnal Sleep Variables Recorded from 3 Surrogate-Reared Socially Isolated M. nemestrina Infants During 13 All-Night
2
2
1/1
zU
SLEEP IN ISOLATION-REARED MONKEYS
559
similar for socially-isolated, surrogate-reared pigtailed monkey infants and groupliving, mother-reared infants. The fact that the considerably less complex (“impoverished”) environment of isolation-reared infants did not significantly influence basic sleep stage organization is suggestive that such organization may, in large part, be intrinsically determined. Individual (and presumably genetically determined) differences in the organization of sleep-waking cycles in the newborn rhesus (M.rnulatta) monkey were also found by Meier and Berger (1965), although we should emphasize that the infants reported in this study were not newborn. Studies in rodents have suggested a significant genetic component to sleep pattern regulation (Friedman, 1974; Van Twyver, Webb, Dube, & Zackheim, 1973), but similar experiments have yet t o be reported in primates. We, of course, do not suggest that sleep patterns are free of environmental influences. Sander has demonstrated that the nature of the early caretaker-infant interaction can significantly influence sleep-waking patterns in the human newborn (Sander, Stechler, Burns, & Julia, 1970), although even in these studies he (Sander, 1969) reported evidence of a non-environmental (possibly genetic) influence intrinsic t o the organism, observations supported by the recent work of Emde, Swedberg, and Suzuki (1975). Bert and Pegram (1972) have demonstrated that environmental differences can significantly influence sleep patterns in adult baboons. What does seem apparent, however, is that those specific elements of the early rearing environment that were different in our isolation-reared infants and our group-reared infants did not significantly influence sleep pattern organization, even though they were of a nature and magnitude sufficient to alter markedly the organism’s development. Although the environments in which the isolated monkeys and group-living monkeys were raised were very different, they did contain one important element in common, the 13: 1 1-hr light-dark cycle. Certainly this may represent a significant environmental variable whose role may be considerable in terms of shaping the sleep pattern. Of considerable interest is the fact that not only were mean sleep values very similar, but so was the degree of variability. The considerable night-to-night sleep pattern variability previously found in group-living monkey infants was thought at the time to be related to as of yet undetected social influences (e.g., stresses) which had occurred during the day (Reite et al, 1976). The present data suggest, however, that because the variability persists in an environment in which relatively few changes occur, such night-to-night sleep stage variability may well be in large part intrinsic to the organism, and essentially free of environmental determinants. This persistent night-to-night variability suggests that researchers who purport t o demonstrate the influence of short-term environmental or experimental alterations on sleep should approach the problem from the standpoint that the intrinsic “noise” (variability) in the system is large, and a signal (environmentally induced sleep pattern changes) may be small by comparison. Thus, by failing to consider the problem from the standpoint of the signal-to-noise ratio, with the data processing techniques so mandated, the researcher may lose considerable valuable experimental data and that which he reports may be especially prone to “Type 11” statistical errors.
560
REITE AND SHORT
In summary, we were surprised that sleep patterns in the restricted condition, with the absence of social interaction and stimulation (and the immense amount of learning this must entail), did not differ from the group-living situation. We hope that continued experimental work of this nature will help devine the role of sleep pattern organization in the developing organism, the critical variables that influence such organization, and how those influences become manifest.
Notes 'Trademark registered, Ross Laboratories, Columbus, Ohio 43216. *The lights-out period was 11 hr (660 min) long; this would be the maximum amount of sleep an animal could obtain, assuming a zero sleep latency. Time Awake included only those awakenings occurring after sleep onset (e.g., sleep latency not included) and prior to the final morning awakening (which often preceded lights-on). Thus the total of sleep latency, TST, and Awake will approximate 660 min, differing significantly from this only when the animals awakened prior to lights-on in the morning. 'All values in Table 1 do not add up exactly due to computer roundoff error in the sleep scoring program (see Reite et al., 1976).
This research was supported by USPHS Research Grant No. MH19514 and NIMH Research Scientist Development Award No. 5 K 0 2 MH46335, both t o M. Reite. We thank Dr. I. Charles Kaufman for his thoughtful and helpful criticism of this manuscript.
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