Sleep, 14(5):448-453 © 1991 Association of Professional Sleep Societies Enforced 24-Hour Recovery Following Sleep I)eprivation Leon Rosenthal, Lori Merlotti, Timothy A. Roehrs and Thomas Roth Sleep Disorders & Research Center, Henry Ford Hospital, Detroit, Michigan, U.S.A. Summary: The pattern of recovery sleep after slee:p deprivation was investigated in healthy young adults. Six subjects experience:d three experimental conditions (0, 24, and 48 hr sleep deprivation) in a Latin Square design. The recovery period consisted of a 24-hr enforced time in bed during which subjects were polysomnographically recorded beginning at 0800. To assess the differentiall effects of the deprivation conditions, the total sleep time on the 24-hr recordings was submitted to a six (4-hr block) by three (deprivation condition) multivariate analysis of variance. Subjects slept more following the 24- and 48-hr conditions when compared to the O-hr condition. Across conditions, subjects slept more during the first 4 hr when compared to the remaining five blocks. Importantly, there was a significant interaction of sleep deprivation by 4-hr block. In block I sleep was differentially recovered between each condition with more sleep being recorded following longer hours of deprivation. In block 2 subjects in the 24and 48-hr conditions slept comparable amounts and significantly more than those in the O-hr condition. In blocks 3 and 4 only the 48-hr condition exhibited significantly more sleep than the O-hr condition. However, significantly less sleep was found in block 6 following the 48-hr condition. Overall, subjects recovered 72% and 42% of the total amount of sleep lost during the 24- and 48-hr conditions, respectively. Key Words: Sleep-Sleep deprivationSleep duration-Sleep stages. Research on recovery sleep in humans following deprivation (l,2) has either scheduled an extended time in bed of 8-12 hr, or instructed subjects to rise only after they have met their sleep quota (ad lib sleep). Using these strategies, it is found that the loss of one night of sleep results in lengthening a subsequent night's sleep by approximately 10-20% (3,4). Thus, researchers have concluded that only a small fraction of the total sleep time (TST) lost during deprivation is recovered (5)_ The composition of the recovery sleep has also bt~en characterized. A selective enhancement of slow-wave nonrapid eye movement (NREM) sleep (stage 3~) has been documented following a night without sleep (6). Selective slow-wave sleep recovery has not only been found in human subjects but has been a consistl:!nt finding across other species subjected to comparable periods of wakefulness (7). When sleep deprivation is prolonged to more than a single night, the recov1:!ry sleep consists of enhanced stage 3~ NREM sleep and REM sleep (8). For example, in a classical study by Kales et al. (9) where four subjects were deprived for Accepted for publication April 1991. Address correspondence and reprint requests to Dr. Leon Rosenthal, HFH Sleep Disorders Center, 2921 West Grand Boulevard, Detroit, Michigan 48202, U.S.A. 205 hr of sleep and then recorded for three consecutive nights (12 hr the first night and 9 hr the subsequent nights) subjects regained 79% of stage 4 NREM sleep, 33% of stage REM sleep, but only 9% of TST (l0). However, it is important to note that the sleep efficiency on each of the three recovery nights was 100%_ The review of these findings raises important methodological considerations. It is possible that both strategies, ad lib sleep and slightly extended time in bed, terminate the recovery period prematurely. The latter underestimates recovery by scheduling a shorter than required time in bed and ad lib sleep by confounding the drive to sleep with the individual's motivation to get out of bed_ Although some subjects might elect to stay in bed, others might opt to curtail their sleep before recovery sleep is completed_ An additional consideration in the ad lib methodology is the possible influence of circadian factors. This would be especially important if motivation interacted with circadian rhythms. Thus, allowing subjects to terminate their sleep period may result in an equivocal assessment of recovery sleep. It is hypothesized that these strategies have resulted in a systematic underestimation of the duration of recovery sleep. In order to further determine the extent of sleep recovery a 24-hr enforced time in bed was utilized. Recovery sleep after 0, 24 and 48 hr sleep 448 ENFORCED 24-HOUR RECOVERY FOLLOWING SLEEP DEPRIVATION deprivation was assessed utilizing a 24-hr enforced bedtime. , 2200 METHODS I , 2200 I 1 I I I 0800 2200 J , I ! I I I ! 0800 o hr 0800 2JOO 0800 CONDITION I 0800 0800 0800 0800 0000 24 hr CONDITION Subjects The subjects were six male normal sleeping (as defined below) volunteers, aged 20-30 yr. All subjects had a history free of drug abuse, medical or psychiatric disorders. The subjects signed an informed consent and were paid for their participation. ! I 449 , 2200 0800 , I ! I , , I 2200 ! I , , J I , , , ! t I I 0800 , , 48 hr CONDITION FIG. 1. Schedule for each of the three experimental conditions. The black bars indicate the time in bed periods. Procedure All subjects passed medical and sleep laboratory screening. They were required to have a normal physical examination and a drug-free urine toxicology screen prior to entering the study. The sleep screening consisted of having subjects spend 8 hr in bed (2330-0730 hr) while being polysomnographically monitored using electrodes attached at standard placements to record electroencephalogram (EEG), electrooculogram (EOG), and electromyogram (EMG). Subjects also wore a nasal/oral thermistor to monitor air flow and EMG leg electrodes to monitor leg movements. They all had a screening polysomnogram with a sleep efficiency of at least 88%, no evidence of periodic leg movements during sleep, sleep disordered breathing or indication of other pathologies during sleep. For all the subsequent sleep recordings electrodes were attached to record EEG, EOG, and EMG only. The day following the screening polysomnogram, subjects were tested for level of sleepiness using the standard multiple sleep latency testing (MSLT) procedures (11). Subjects were required to have a mean sleep latency on the MSLT of > 8 min in order to qualify for the study. All subjects were exposed to the three experimental conditions over a 4-wk period with at least 5 days between conditions. Experimental conditions were assigned in a Latin Square design. Prior to each experimental condition subjects reported to the laboratory at 2100 hr and were required to stay in bed for 10 hr (2200-0800 hr) to minimize the possibility of a sleep debt prior to each deprivation condition. The following day, they were tested for level of sleepiness using the standard MSLT procedure. An average sleep latency on the MSLT of > 8 min was required to assure comparable levels of sleepiness at the beginning of each experimental condition. Then, depending on the deprivation condition subjects were allowed a normal night of sleep (2300-0700) or were kept awake for 24 or 48 hr. The recovery period started at 0800 and lasted 24 hr in each of the three conditions (Fig. 1). No caffeinated beverages or excessive exercise were allowed during the deprivation period and subjects were monitored to assure compliance with the experimental protocol. During the entire 24-hr recovery period, subjects were required to remain in bed in a darkened bedroom with provisions for toileting and meals made according to the following protocol. Food was offered at three specified times and only if subjects were awake (07000900, 1200-1430, and 1800-2030). Subjects had to awaken spontaneously and stay awake for 10 min before food was offered. If subjects were asleep the meal was delayed until the next specified meal period. The food offered at each meal consisted of a sandwich, fruit and a noncaffeinated beverage. Thirty minutes were allowed for the consumption of food with the exception of the third period, which was extended to 45 min to allow for the replacement of electrodes. Subjects remained in their rooms during the consumption of their meal, but were allowed to get out of bed, sit at a table and use the rest room. Subjects remained in bed with lights off and were polysomnographically recorded the rest of the time. Subjects were not allowed watches or alarm clocks in their rooms and their interaction with laboratory personnel was limited to the meal periods. An additional 15-min bathroom break, between 2300 and 0100 was provided. At other times use of the bathroom was allowed only if the subject had been awake for 10 min or longer. Polysomnographic recordings were scored in 30-sec epochs according to the standards of Rechtschaffen and Kales (12) by scorers blind to the experimental condition. The interrater reliability was maintained at 90% or higher. Data were analyzed using the general linear model analysis procedure (SAS Institute) with one withingroup variable being sleep deprivation condition and the other within-group variable being hour block (six 4-hr blocks). The probabilities reported are corrected by the Greenhouse-Geisser method. Post hoc contrasts were done comparing the three conditions and the six 4-hr blocks. Sleep, Vol. 14, No.5, 1991 450 L. ROSENTHAL ET AL. TABLE 1. Mean (standard deviation) of total sleep time for each 4-hr block of the recovery periodfollowing 0,24 and 48 hr of sleep deprivation (sip dep) Block (timer Sip dep 1 (0800-1159) 2 (1200-1559) 3 (1600-1959) 4 (2000-2359) 5 (2400-0359) 6 (0400-0759) Total o hr 195 (33) 229 (7)* 237(3)t 41 (44) 181 (62)* 224(21)* 43 (54) 101 (61) 146(81)* 21 (45) 110 (103) 124(64)* 145 (90) 116 (80) 131(83) 208 (34) 204 (39) 131(77)* 653 (103) 941 (180) 992 (109) 24 hr 48hr a Post-hoc comparisons of significant interaction (p < 0.05): * vs. O-hr condition; t vs. both 0- and 24-hr conditions. RESULTS Baseline sleep-wake function The total sleep times (TSTs) on the nocturnall0-hr recordings, prior to each experimental condition, were comparable (564 min ± 34 for the O-hr condition' 545 min ± 40 for the 24-hr condition; and 544 min ± 34.06 for the 48-hr condition). The mean sleep latency on the MSLT the following day was also comparable among the three experimental conditions (13 min ± 6 for the O-hr condition, 13 ± 4 for the 24-hr condition, and 12 ± 4 for the 48-hr condition). Recovery sleep time To evaluate the pattern of recovery sleep the 24-hr recovery period was divided into six (4-hr) blocks. Thus, the blocks represent clock hours 0800-1159 (block 1), 1200-1559 (block 2), 1600-1959 (block 3),2000-2359 (block 4),2400-0359 (block 5) and 0400-0759 (block 6). To assess the differential effects of the sleep deprivation conditions, the total sleep time on the 24-hr recordings were submitted to a six (4-hrblock) by three (deprivation condition) multivariate analysis of variance (MANOYA). The results of this analysis showed TABLE 2. Mean (standard deviation) of sleep stages (minutes and percentages) during the recovery sleep period following 0, 24 and 48 hr of sleep deprivation Condition Minutesa .b Percent' Stage 1 0 24 48 21 (5) 14 (5}i 13 (3)i Stage 2 0 24 48 136 (48) 137 (66) 133 (37) 330 (64) Sleep Stage 3/4 0 24 48 REM stage 495 (105)d 548 (72)d 51 (40) 112 (66)d 123 (56)d 0 135 (29) 24 197 (55) 48 188 (51) a Significant main effect for stage 2 (p < 0.01). b Significant main effect for stage 3/4 (p < 0.01). , Significant main effect for stage 1 (p < 0.05). d Post-hoc comparisons (p < 0.05): vs. O-hr condition. Sleep, Vol. 14, No.5, 1991 51 (8) 53 (6) 55 (4) 8 (6) 13 (8) 13 (6} 21 (3} 21 (2} 19 (4) a significant main effect of sleep deprivation (df 2, 10; F 17.41; P < 0.01). Post-hoc comparisons showed that subjects slept significantly more following the 24- and 48-hr sleep deprivation conditions (941 ± 180 min and 992 ± 109 min) when compared to the O-hr condition (653 ± 103 min). There was no statistically significant difference between the 24- and 48-hr conditions (see Table 1). A main effect of hour block was also found (df 5,25; F = 7.53; p < 0.01). Post-hoc comparisons showed that subjects slept significantly more in block 1 when compared to all other blocks. Also, subjects slept more in blocks 2 and 6 when compared to blocks 3 and 4. Importantly, there was a significant interaction of sleep deprivation by hour block (df 10,50; F = 5.34; P < 0.01). The post-hoc comparisons showed that recovery sleep in blocks 1, 2, 3, 4 and 6 differed as a function of deprivation condition. In block 1 the TST for each experimental condition differed significantly (195 ± 33 min following the O-hr condition, 229 ± 7 following the 24-hr condition and 237 ± 3 following the 48-hr condition). In block 2 the TST in the O-hr condition (41 ± 44 min) was significantly lower than the 24- and 48-hr conditions, whereas the 24- and 48-hr conditions were comparable (181 ± 62 min and 224 ± 21 min, respectively). The pattern of recovery sleep was similar for blocks 3 and 4 with TST in the O-hr condition being significantly less (43 ± 54 min and 21 ± 45 min) than after 48 hr of deprivation (146 ± 81 and 124 ± 64 min). TST after 24 hr deprivation was intermediate and not different from the other two conditions (101 ± 61 and 110 ± 103 min). In the last block (hours 21-24) there was a reversal of this pattern. TST in the O-hr condition was the highest (208 ± 34 min) whereas TST in the 48-hr condition was the lowest (131 ± 77 min). The 24-hr condition was not significantly different from the 0- and 48-hr conditions (TST of 204 ± 39 min). Recovery sleep staging Although the primary purpose of this experiment was to study the amount of recovery sleep following deprivation, analyses of sleep stages was also carried out. However, not all sleep stages were present in each 4-hr block. Thus a one-factor (sleep deprivation con- 451 ENFORCED 24-HOUR RECOVERY FOLLOWING SLEEP DEPRIVATION TABLE 3. Sleep stage percent (mean and standard deviation) for each 4-hr block of the recovery period following 0, 24, and 48 hr of sleep deprivation (sip dep) Block (time)a <- Sip dep 1 (0800-1159) 2 (1200-1559) 3 (1600-1959) 4 (2000-2359) 5 (2400-0359) 6 (0400-0759) Stage 1 0 24 48 20 (5) 8 (2) 5 (4) 30 (38) 22 (13) 8 (3) 55 (41) 23 (II) 18 (9) 20 (40) 7 (6) 35 (25) 13 (7) 14 (8) 30 (35) 20 (5) 15 (9) 28 (24) Stage 2 0 24 48 51 (10) 45 (12) 41 (14) 38 (38) 54 (13) 66 (4) 17 (21) 54 (8)* 59 (7)* 9 (23) 43 (34) 49 (23)* 48 (28) 45 (25) 48 (27) 52 (10) 52 (8) 53 (16) Stage 3/4 0 24 48 2 (3) 30 (17)* 38 (15)t 5 (10) 4 (7) 4 (5) 9 (14) 1 (2) 1 (.1) 1 (3) 1 (3) 2 (5) 11 (15) 10 (14) 9 (8) 6 (10) 11 (14) 6 (13) REM stage 0 24 48 26 (7) 17 (4)* 16 (9)* 11 (16) 20 (11) 22 (2) 3 (6) 22 (12)* 23 (10)* 3 (8) 16 (13) 14 (14) 11 (8) 14(13) 13 (10) 22 (6) 22 (8) 13(11) Sleep stage a Post-hoc comparison of significant interaction (p < 0.05): * VS. dition) MANOVA was carried out for each stage of sleep. First, the total number of minutes spent in each stage during the 24-hr recovery was submitted to this analysis. There was no significant main effect on the total number of minutes spent in stage 1 NREM sleep (136 ± 48, 137 ± 66 and 133 ± 37 for the 0-,24- and 48-hr conditions, respectively) and REM stage sleep (135 ± 29, 197 ± 55 and 188 ± 51 for the 0-, 24- and 48-hr conditions, respectively). However, there was a main effect for stage 2 NREM sleep (df2,10; F= 14.18; p < 0.01). Post-hoc comparisons showed that the total number of minutes spent in stage 2 was significantly lower following 0 hr of sleep deprivation (330 ± 64) than after 24 and 48 hrofdeprivation (495 ± 105 and 548 ± 72, respectively). No statistically significant difference was found between the 24- and 48-hr conditions. There was also a main effect of condition for stage 3/4 NREM sleep (df2,1O; F= 15.82; p < 0.01). Post-hoc comparisons showed less stage 3/4 NREM following the O-hr condition (51 ± 40) when compared to the 24- and 48-hr conditions (112 ± 66 and 123 ± 56, respectively). Here again, the recovery of stage 3/4 NREM sleep was not different between the 24- and 48-hr conditions (see Table 2). The recovery of sleep stages was also analyzed as percentages of TST during the 24-hr recovery period. The percent of each sleep stage was derived and submitted to a one-factor (sleep deprivation condition) MANOVA. The results only showed a main effect of condition for stage 1 NREM sleep percent (df2,10; F = 8.44; P < 0.05). The post-hoc comparisons showed a higher percent of stage 1 NREM sleep after 0 hr of deprivation (21 ± 5) when compared to the 24- and 48-hr conditions (14 ± 5 and 13 ± 3, respectively). No significant difference was found between the 24and 48-hr conditions. Finally, the recovery pattern of the different sleep O-hr condition; t vs. both 0- and 24-hr conditions. stages was analyzed. The data was submitted to a six (4-hr block) by three (deprivation condition) MANOVA. The reader is reminded that not all sleep stages were present in each 4-hr block and thus, the results of this analysis should be interpreted with caution. Table 3 shows the main sleep stage percentages for each 4-hr block across the three sleep deprivation conditions. Significant interactions of sleep deprivation by 4-hr block occurred for stage 2, stage 3/4 and REM stage sleep [df 10,50; F = 3.36 (p < 0.05), F = 9.12 (p < O.01)andF= 2.51 (p < 0.05), respectively]. Sleep deprivation was associated with significant increases in percent stage 3/4 NREM and REM in block 1, percent stage 2 NREM and REM in block 3 and percent stage 2 NREM in block 4. Relation of sleep recovered to sleep lost In order to estimate the amount of TST recovered vis a vis the amount lost during each of the deprivation conditions a percentage of recovery sleep was derived. The percentage was derived by subtracting the amount of total sleep after the 24- or 48-hr condition from the amount subjects had in the O-hr condition and then dividing this number by the TST on the nocturnal eight hours prior to the O-hr condition (x = 402 ± 33 min) (10). For the 48-hr condition the denominator was multiplied by 2 as subjects remained awake for two nights. The TST recovered was 72% following the 24hr sleep deprivation condition and 42% following the 48-hr condition. Similar estimates of the recovery of specific sleep stages were derived. As it can be observed in Table 4, there was an almost completely recovery of stage 3/4 (98%) after the 24-hr condition, which was drastically reduced to 59% after 48 hr of deprivation. A similar pattern was observed for stage 2 NREM and REM sleep (see Table 4). Sleep, Vol. 14, No.5, 1991 452 L. ROSENTHAL ET AL. TABLE 4. Amount of recovery sleep, overall and by stage, expressed as a percent of lost sleep Sleep stages (min) O-hr condition 24-hr condition 48-hr condition 2 3/4 REM Total 52 61 112 98 122 124 59 134 78 197 81 402 941 156 187 34 804 992 42 136 332 Amount lost Recovery sleep % Recovery 54 138 4 210 495 78 Amount lost Recovery sleep % Recovery 108 133 -3 420 549 52 DISCUSSION 653 72 vation, is intriguing. It is possible that subjects satiated their homeostatic sleep process by recovering more slow-wave sleep as it has been suggested previously (13,14). Alternatively, it could be argued that only a finite amount of sleep can be recovered in a 24-hr period. Extension of the scheduled time in bed, beyond 24 hr, would be necessary to evaluate this possibility. This hypothesis could also explain the lack of differences in TST following the 24- and 48-hr sleep deprivation conditions. The results of this experiment show that a greater amount of sleep is recovered following sleep dep:rivation than previously reported. This was the result of utilizing an enforced 24-hr time in bed and thus allowing for an unbiased measurement of the sleep recovery process. By minimizing the impact of possible competing motivators the extent of sleep recovery was allowed to be expressed. To maximize this respons(~ a concerted effort was made to keep all other possible Acknowledgement: This work was supported by NIMH behavioral motivators neutral. For example, meals were provided at times when subjects were awake so hunger grant MH-00860, awarded to Dr. Leon Rosenthal. would not interfere with the sleep recovery process. Relevant to this methodology is the lack of complaints REFERENCES by the participants who had no difficulty completing 1. 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