Human Non-24-Hour Sleep-Wake Cycles in an Everyday Environment

Transcription

1 Sleep, 2(3): Raven Press, New York Human Non24Hour SleepWake Cycles in an Everyday Environment * Anita L. Weber, *Mark S. Cary, tned Connor, and :j:patricia Keyes *Department of Psychology, Indiana University, Bloomington, Indiana; tdepartment of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania; and tportland State University, Portland, Oregon Summary: A sighted college student maintained a sleepwake cycle longer than 24 hr in his everyday environment for more than half of nearly four years, The range of sleepwake periods and the amount and regularity of sleep are consistent with those found in timefree environments, Episodes of 24 hr periodicity suggest that social cues or obligations are effective entraining agents, He reported more sleep difficulties while on a 24 hr than a non24hr schedule. Key Words: Circadian rhythmshypernychthemeralfree running cycle Sleep disorderssocial zeitgebers. Most humans show sleepwake cycles longer than 24 hr when isolated in timefree environments like caves (Mills, 1964), underground bunkers (Aschoff, 1965; Wever, 1979), and windowless rooms (Webb and Agnew, 1974). Thus, a person in the everyday environment who isolates himself from 24 hr time cues, is insensitive to these cues, or has some other disorder of entrainment mechanisms should show a longer than 24 hr period ("hypernychthemeral," as Kokkoris et ai., 1978, have named it) similar to that in a timefree environment (Webb and Agnew, 1972). Elliott et al. (1971) briefly reported the existence of such a person. Miles et al. (1977) reported a hypernychthemeral rhythm in a blind man in normal society. Recently, Kokkoris et al. (1978) found such a rhythm in a sighted subject being treated for a sleep disorder. We report here the case histories of two sighted persons, one of whom maintained a hypernychthemeral sleepwake period for most offour years. One habitually maintained a 24 hr period but briefly synchronized to the other's longer period. This report confirms and extends the previous report by Kokkoris et al. (1978). Accepted for publication February 198. Address reprint requests to Dr. Weber at Department of Psychology. Indiana University, Bloomington, Indiana

2 348 A. L. WEBER ET AL I I \ I I 1971 JUNE JULY. \ DO 48. I I I I I JUNE } MAY JUNE I AUG _. " JULY AUG JULY = ~. ~ 16 SEPT I SEPT =:.~ = ~ ~ ]8 9 AUG OCT } OCT =. := SEPT \8 19 NOV 3 NOV 1 OCT OEC 1972 JAN i ~ = ~ ~ ~~. = ~ = OEC 1973 JAN ==. _. NOV OEC 2 FE8 4 FE8 = ~ ~ ~ ~~ II 1974 JAN ~:... J21 22 MAR APR MAY 5 MAR APR FE8 MAR APR = == == ~.:=.. :=: =...:""':": ~ ~.=. = = ~ == Sleep, Vol. 2, No.3, 198

3 HUMAN NON24HOUR SLEEP WAKE CYCLES I I I I I MAY JUNE JULY AUG SEPT OCT NOV DEC 1975 JAN = =.: FIG.!. John's sleepwake record doubleplotted in the conventional manner for I June March , Fall term begins, teaching assistant, no courses, 13 Sept. 71; 2, Visit with parents, change from Pacific Standard Time to Central Standard Time, 725 Oct. 71; 3, Change from Pacific Standard Time to Daylight Savings Time, 31 Oct. 71; 4, Spring term begins, teaching assistant, no courses, 31 Jan. 72; 5, Change from Pacific Daylight Savings Time to Standard Time, 25 Apr. 72; 6, No record, 1117 May 72. 7, Visit with parents, change from Pacific Standard Time to Central Standard Time, 319 June 72; 8, Visit to farm, 1922 Aug. 72; 9, Fall term begins, independent research, no teaching or courses, 4 Sept. 72; 1, Change from Pacific Standard Time to Daylight Savings Time, 29 Oct. 72; 11, Spring term begins, independent research, no teaching or courses, 29 Jan. 73; 12, 4. hr sleepwake period, 28 Feb. 13 March 73 (spectral analysis shown in Fig. 2C); 13, Visit to farm, 1517 March 73; 14, Change from Pacific Daylight Savings Time to Standard Time, 29 Apr , Visit to farm, 819 June 73; 16, Visit to farm, 1113 July 73; 17, No record (visit with parents), 22 July3 Aug. 73; 18, Moved to graduate school, change from Pacific to Eastern Standard Time, 2 Sept. 73; 19, Fall term begins, taking courses and doing research, 7 Sept. 73; 2, Change from Eastern Standard Time to Daylight Savings Time, 28 Oct. 73; 21, No record (sick), 37 Jan. 74; 22, Spring term begins, taking courses and doing research, 16 Jan , Change from Eastern Daylight Savings Time to Standard Time, 28 Apr. 74; 24, Record replotted with Mary's record in Fig. 3, I June31 Aug. 74; 25, Fall term begins, taking courses and doing research, 5 Sept. 74; 26, 25.3 hr sleepwake period, 215 Sept. 74 (spectral analysis shown in Fig. 2A); 27, 24. hr sleepwake period, 1629 Sept. 74 (spectral analysis shown in Fig. 2B); 28, Change from Eastern Standard Time to Daylight Savings Time, 27 Oct. 74; 29, Spring term begins, taking courses and doing research, 15 Jan. 75. FEB MAR Sleep, Vol. 2, No.3, 198

4 35 A. L. WEBER ET AL. SUBJECTS AND METHODS John, a psychology student, kept a comprehensive diary for nearly 4 years (1 June 1971 to 26 March 1975; the last 2~ years of undergraduate and first 1 ~ of graduate study, during which time he was 2428 years old), in part to increase his working productivity by analyzing the environmental determinants of his own behavior. The diary noted sleep and wake times, vacations, exams, caffeine intake, reactions to new foods, insomnia, drowsiness, alarm clock usage, and times spent working, relaxing, and exercising. Mary, a research assistant in psychology with a very flexible work schedule, kept a diary for 1 year (16 April 1974 to 21 May 1975; she was 21 years old), primarily due to John's influence. John's sleepwake record was divided into 93 successive two week intervals excluding diary gaps. Three measures were computed for each two week interval: (1) the maximum of the power spectral estimates, a measure of the predominant sleepwake cycle period; (2) the circadian variance quotient (CQ), a measure of sleepwake cycle regularity; and (3) total sleep time. The autocovariance function's power spectrum was calculated by computer program BMD2T (Dixon, 1971) with a hamming spectral window in a way similar to that of Halberg and Panofsky (1961) and Panofsky and Halberg (1961). The number of 15 min intervals in which sleep occurred was totaled every 6 hr for 56 data points every two weeks. The autocovariance function lag used was 4. The CQ was computed (following Halberg and Panofsky, 1961) by summing the maximum spectral estimate and its two adjacent estimates (to allow for smoothing in the spectral estimate procedure) and dividing by the total variance obtained by adding all the spectral estimates. The average sleep per day within each two week interval was also computed. RESULTS AND DISCUSSION SleepWake Periodicity, Regularity, and Sleep Length John's entire sleepwake record for four years is shown in Fig. 1. The spectral analyses for three sections (nos. 27, 24 hr period; 26, longer than 24 hr period; and 12, a very long period) are shown in Fig. 2. John also showed relative coordination. For example, from February to May 1972, John's cycle temporarily synchronized to 24 hr when sleep coincided with 24 to 8 clock time. Spectral analysis across such segments with relative coordination yields an average of the regular fluctuations in period with an increase in noise and a lowering of the CQ. The spectral analyses summarized in Table 1 show no single hypernychthemeral period. The overall average period length was 25.6 hr, with a range from 22.9 to 4. hr, which agrees roughly with the sleepwake period variability found in timefree environments (Colin et al., 1968; Mills, 1967; Jouvet et al., 1974; Wever, 1979). The high variability of John's period suggests that some regular hypernychthemeral geophysical period like the 24.8 hr lunar day was not synchronizing his cycle. The mean CQ was 47.6% (SO, 15.4; range, ). Regularity decreased with increasing period (r =.3, p <.1, N = 93, Pearson's correlation). Other Sleep, Vol. 2, No.3, 198

5 HUMAN NON24HOUR SLEEP WAKE CYCLES 351 (f) UJ I ~ 1 ~ 9 ~ 8 en 7. UJ...J 6 «Q: 5. 4 UJ 3 Q.. (f) 2 I Q: UJ ~ 7. Q B FIG. 2. Power spectra of selected sleep records shown in Fig. I. The abscissa is linear in I/period. Section A computed from section no. 26, B from 27, and C from PERIOD IN 24 2 HOURS 17.1 studies have also found that the regularity of the sleepwake cycle declines in timefree environments compared to 24 hr entrainment (Webb and Agnew, 1974; Mills, 1967; Jouvet et ai., 1974). The mean total amount of sleep was 7.6 hr per day (SD =.6; range, hr for the two week periods). John did not get less or more sleep as the sleepwake period increased (r =.4, ns; N = 93, Pearson's correlation). For example, in section 12 of Fig. 1, which has a period of 4. hr, there is a sleep episode of 18.5 hr. Despite this long sleep episode, the average sleep length for the two weeks was 7.9 hr, only slightly longer than the 7.6 hr for the entire record. Weitzman et al. (1979) have also found long sleep episodes in isolated SUbjects. Other studies in timefree environments have also shown no clear relationship between the amount of sleep and the sleepwake period. Jouvet et al. (1974) found that the amount of sleep decreased when the freerunning sleepwake period spontaneously increased from circadian (2527 hr) to bicircadian (485 hr). But Webb and Agnew (1974) found that the total amount of sleep increased during longer than 24 hr periods in a timefree environment compared to a 24 hr period in an everyday environment. Sleep. Vol. 2. No.3, 198

6 352 A. L. WEBER ET AL. TABLE 1. Distribution of John's sleep wake cycle lengths during two week periods for nearly four years (l Period No. Period No I I I I a Spectral analysis gives period estimates falling in an interval around each tested value; the tested periods are linear in frequency. Social Factors and Entrainment Although observational data are never conclusive, the detailed diary suggests that social cues could be significant entraining agents. For example, John showed a 24 hr cycle at the start of Fall classes in 1971, 1973, and 1974 for 4~, 2, and 1 month (points 1, 19, and 25 in Fig. 1). In Fall 1972 (point 9, Fig. 1), he had independent study courses with no scheduled classes and continued his hypernychthemeral cycle. John later recalled that he tried to maintain a 24 hr cycle to attend his classes but needed three alarm clocks to awaken, and he eventually gave up his attempt since daytime drowsiness severely disrupted his work. He scheduled Spring classes in a block to sleep around them, and tried to increase his work efficiency by going to bed only when sleepy and arising only when he felt rested. His diary recorded more insomnia (p <.2), drowsiness (p <.2), and alarm clock use (p <.1; all tests X 2, twotailed) on a 24 hr schedule than when on a longer schedule. To test for abeat frequency in sleep disorder between 24 and 2526 hr cycles, we added his notations of insomnia, rise time drowsiness, and alarm clock use together for the longest continuous 24 hr period (14 days from 1 September 1971 to 18 January 1972) and longest hypernychthemeral period (159 days from 29 June 1972 to 4 December 1972), but found no significant spectral component between 12 and 25 days (the expected beat period) using the BMD2T program with a hamming spectral window and a variety of lags. Trips to a farm with other students for outdoor physical work, relaxation, and socializing also coincided with a 24 hr sleepwake cycle (points 8,13,15, and 16, Fig. 1). Notice that on returning from the farm, John always experienced a large apparent change of phase of the sleepwake cycle close to the phase predicted by his prior period. Thus, synchronization to 24 hr may not have changed the phase of the underlying timing system; an example of masking rather than entrainment (Menaker and Eskin, 1966). Mary's sleep diary contains the best evidence for entrainment by social cues. Mary maintained a 24 hr period for the year she kept her diary except for a single Sleep, Vol. 2, No.3, 198

7 HUMAN NON24HOUR SLEEPWAKE CYCLES , I I I, I. oaoo 16 oapo 16. A = ~. c:a == ==== """""'... _ JOHN iifs'iii MARY 4 B C/) ~ o 5 "" C. ao ==...,;;;;;;;;;;, == 9 FIG. 3. The sleep records of John (black) and Mary (crossstripes). A: John and Mary are living together. B: John goes on vacation while Mary lives alone. C: John returns from vacation. seven week period. At this time she was living with John and working as a research assistant with a very flexible work schedule. Figure 3 shows three months of her sleepwake cycle plotted with John's. In section A, John shows a period of about 26.5 hr, while Mary maintains a 24 hr period. In section B, John leaves for two weeks to visit his parents and Mary continues her 24 hr schedule. Sleep. Vol. 2, No.3, 198

8 354 A. L. WEBER ET AL. In section C, John returns and their sleep onset times coincide with a period of about 24.5 hrintermediate to their individual lengths in section A. The mutual entrainment is only partially successful. From days 5963, John's sleepwake cycle assumes a 27 hr period, while Mary's shows a shorter than 24 hr transient until the sleep onset times of the pair resynchronize on day 66. Other studies have also found that social cues can effectively synchronize the human sleepwake cycle (reviewed in Wever, 1979). ACKNOWLEDGMENT We thank Drs. E. Weitzman, J. Alberts, F. Restle, and W. Timberlake for valuable criticism of the manuscript. J. Godollei and L. Tate provided technical assistance. This research was supported in part by PHS Grant S5 RR 731 to A.L.W. and by the Indiana University Wrubel Computing Center. REFERENCES Aschoff J. Circadian rhythms in man. Science 148: , Colin J, Timbal J, Boutier C, Houdas Y, and Siffre M. Rhythm of the rectal temperature during a 6month freerunning experiment. J Appl Physiol 25: 17176, Dixon JW. BMD Biomedical Computer Programs. Univ. California Press, Berkeley, 1971, pp Elliott AL, Mills IN, and Waterhouse JM. A man with too long a day. J Physiol (Lond) 212:331, Halberg F and Panofsky H. Thermovariance spectra 1. Method and clinical illustrations. Exp Med Surg 19:28439, Jouvet M, Mouret J, Chouvet G, and Siffre M. Toward a 48hour day: Experimental bicircadian rhythm in man. In: FO Schmitt and FG Worden (Eds), The Neurosciences: Third Study Program, MIT Press, Cambridge, Mass, 1974, pp Kokkoris CP, Weitzman ED, Pollak CP, Spielman AJ, Czeisler CA, and Bradlow H. Longterm ambulatory temperature monitoring in a subject with a hypernychthemeral sleepwake cycle disturbance. Sleep 1:17719,1978. Menaker M and Eskin A. Entrainment of circadian rhythms by sound in Passer domesticus. Science 154: , Miles LEM, Raynal OM, and Wilson MA. Blind man living in normal society has circadian rhythms of 24.9 hours. Science 198:421423, Mills IN. Circadian rhythms during and after three months in solitude underground. J Physio/ (Lond) 174:217231, Mills IN. Keeping in step away from it all. New Scient 33:35351, Panofsky H and Halberg F. Thermovariance spectra II. Simplified computational example and other methodology. Exp Med Surg 19:323338, Webb WB and Agnew HW Jr. A superdian rhythm and its consequences. (Abstr) Sleep Res 1:179, Webb WB and Agnew HW Jr. Sleep and waking in a timefree environment. Aerospace Med 45:617622, Weitzman ED, Czeisler CA, and MooreEde Me. Sleepwake, neuroendocrine and body temperature rhythms under entrained and nonentrained (freerunning) conditions in man. In: M Suda, o Hayaishi, and H Nakagawa (Eds), Biological Rhythms and Their Central Mechanism, Elsevier/ North Holland, Amsterdam, Wever R. The Circadian System of Man. SpringerVerlag, New York, Sleep. Vol. 2, No.3, 198