Brain-Mind States: I. Longitudinal Field Study of Sleep/Wake Factors Influencing Mentation Report Length

Transcription

1 MENTATION IN WAKE AND SLEEP Brain-Mind States: I. Longitudinal Field Study of Sleep/Wake Factors Influencing Mentation Report Length Robert Stickgold PhD, April Malia BA, Roar Fosse DSCi, Ruth Propper PhD, and J. Allan Hobson MD Department of Psychiatry, Harvard Medical School Study objectives: To collect and analyze reports of mental activity across sleep/wake states. Design: Mentation reports were collected in a longitudinal design by combining our Nightcap sleep monitor with daytime experience sampling techniques. Reports were collected over 14 days and nights from active and quiet wake, after instrumental awakenings at sleep onset, and after both spontaneous and instrumental awakenings from REM and NREM sleep. Setting: All reports were collected in the normal home, work and school environments of the subjects. Participants: Subjects included 8 male and 8 female undergraduate students (19 26 years of age). Interventions: N/A Measurements and Results: A total of 1,748 reports, averaging 109 per subject, were collected from active wake across the day (n=894), from quiet wake in the pre-sleep onset period (n=58), from sleep onset (n=280), and from later REM (n=269) and nonrem (n=247) awakenings. Median report lengths varied more than 2-fold, in the order REM > active wake > quiet wake > NREM sleep onset. The extended protocol allowed many novel comparisons between conditions. In addition, while spontaneous REM reports were longer than those from forced awakenings, the difference was explained by the time within the REM period at which the awakenings occurred. Finally, intersubject differences in REM report lengths were correlated with similar differences in waking report lengths. Conclusions: The use of the Nightcap sleep monitoring system along with waking experience sampling permits a more complete sampling and analysis of mental activity across the sleep/wake cycle than has been previously possible. Key words: Sleep; dreams; mentation; sleep onset; Nightcap; experience sampling; REM; nonrem INTRODUCTION SYSTEMATIC EFFORTS TO CHARACTERIZE DREAMING AND TO CORRELATE THIS MENTAL STATE with its underlying brain physiology began in earnest with the discovery of REM sleep by Aserinsky and Kleitman in and the apparent correlation of dreaming with REM by Dement and Kleitman in ,3 This led many to conclude the physiological state of REM and the psychological state of dreaming were identical, a conclusion that was soon disproved by the finding that significant amounts of mentation, much of it distinctly dreamlike, is reported after NREM awakening. 4 Some scientists have interpreted this result to indicate that mental activity of a dreamlike nature is continuous across all states, varying only in intensity with the rises and falls of brain activation level 5,6 while others continue to argue for the qualitative differences between REM and NREM mentation. 7-9 Now, more than 50 years after the discovery of the link between REM sleep and dreaming, we are left without even agreement on a definition of dreaming, let alone when it occurs. Both methodological and ideological disputes over how to define dreaming and the appropriate measures of mental activity to Accepted for publication December 2000 Address correspondence to: Dr. Robert Stickgold, Laboratory of Neurophysiology, Massachusetts Mental Health Center, 74 Fenwood Road Boston, MA 02115; Fax: ; rstickgold@hms.harvard.edu study have left the field in disarray. What has become clear is that mental activity can occur in all stages of the sleep/wake cycle, but that the characteristics of this mentation vary dramatically across the cycle. To study these variations in mental activity across the sleep/wake cycle, and ultimately to explain this variation in terms of the robust shifts in the underlying cognitive, physiological, and molecular mechanisms of the brain, it would be desirable to begin with a large collection of mentation reports collected longitudinally, under naturalistic conditions, across the entire sleep/wake cycle. Because of the costs in time and personnel involved in sleep laboratory studies of dreaming, no such study has ever been conducted. Until now, most investigations have looked at only one or two states, and many have focused on a single dream characteristic. In order to obtain longitudinal data under naturalistic conditions and across a wide range of conditions, a method of collecting mentation reports in the field is required. The availability of the Nightcap sleep monitor 10,11 now makes such studies feasible. The Nightcap has been shown to reliably distinguish REM from NREM sleep 11,12 and to permit the rapid and efficient collection of large numbers of sleep mentation reports in the home from instrumental awakenings at sleep onset 13 and from spontaneous REM and NREM awakenings across the night. 14 In a study of the efficacy of the Nightcap, Ajilore et al. (1995) studied 10 subjects both in the sleep laboratory and in the home. Studies in the laboratory combined standard polysomnography with Nightcap recordings. Overall, 87% of one-minute epochs were scored the same by the two methods. Agreements for indi- SLEEP, Vol. 24, No. 2,

2 vidual subjects varied from 81% to 93%. In contrast, inter-rater reliability for the manually scored polysomnograph data was 95%, a value only 8% higher than that of the Nightcap. Mean REM latency was 111 minutes based on polysomnographic records and 107 minutes based on Nightcap data. Similar results were reported by Yun et al. 12 We now report the collection of 1,867 mentation reports from 16 subjects, over 14 days and nights as the subjects moved through their normal work, home, and school environments. 15 These reports, collected by experience sampling across the day and with the Nightcap sleep monitor at night in subjects homes, provide the opportunity to compare reports collected from waking, sleep onset, NREM and REM sleep, and within sleep both from forced awakenings at predetermined points in the sleep cycle and from spontaneous awakenings across the night. The fully transcribed text contains 200,700 words describing mental activity and has now been analyzed for the prevalence and intensity of 30 mentation features. In this first paper, we characterize the data set and then present an analysis of variations in report lengths across sleep/wake states, awakening conditions, circadian phases, times in stage, gender, and individual reporting styles. These comparisons confirm the robustness of physiological-state-dependent variations in mentation, provide new insights into the sources of differences seen between dream studies, and offer an explanation of the difference in length seen between spontaneous and laboratory reports. They also demonstrate that the impact of individual reporting styles on the lengths of reports is correlated across sleep/wake states. METHODS Sixteen undergraduate students (19 26 years of age, 8 male, 8 female) provided informed consent and were paid for participation in the study. Subjects began with a preliminary seven-day training protocol during which they were asked to produce a spontaneous mentation report each morning when they woke up and were also paged once each day for a daytime mentation report. Following completion of the preliminary protocol, subjects carried a pager during the day and wore the Nightcap, a home-based sleep monitoring system, 11 at night for 14 additional days. The 14 days could be consecutive or broken into two or three blocks as individual schedules demanded. Subjects provided dictated mentation reports four times each day when paged, as well as when they awoke from sleep during the 14 nights. In some cases, subjects continued to provide waking reports between blocks, resulting in more than 14 days of waking reports. Reports from the preliminary protocol were not included in the database. Report collection protocol: To obtain daytime mentation reports, subjects were paged four times each day using standard pagers in tone mode. These reports were categorized as active wake (aw) reports. For each day, subjects defined their available time during the day. This was divided into four equal time divisions and subjects were paged at a random time within each quartile of their day. Subjects were given the following instructions: When you are beeped, think back and try to remember what was going on in your mind in the time prior to your being beeped (i.e., anywhere up to fifteen minutes before the beep). Where were you? Who else was there? What were you doing? What were you seeing, thinking, and feeling? What was happening around you? To obtain nocturnal mentation reports, subjects wore the Nightcap sleep-monitoring system, 10,11 connected to a Macintosh computer. 13 The Nightcap monitors head movements with a multi-polar cylindrical mercury switch on the forehead and eyelid movements with a piezoelectric film adhered to the upper eyelid. Sleep/wake states were distinguished for one-minute epochs based on activity in both channels (wake), in neither channel (NREM), or in the eyelid channel only (REM). The algorithm has been described in detail elsewhere. 11 Analyses were performed by the Nightcap, and instrumental awakenings made based on protocol requirements. On four nights, no instrumental awakenings were performed; on two nights instrumental awakenings were made during the sleep onset period, and on the remaining eight nights, instrumental awakenings were made Week One 4X - 4X SO 4X R 4X N 4X - 4X N 4X R d1 d2 d3 d4 d5 d6 d7 Week Two 4X - 4X SO 4X N 4X R 4X - 4X R 4X N d8 d9 d10 d11 d12 d13 d14 d1-14 protocol day wake sleep 4X - SO 4 daytime reports no forced awakenings sleep onset awakenings R N REM then NREM awakenings NREM then REM awakenings Figure 1 Report collection protocol. Reports were collected four times each day during waking as well as following all awakenings from sleep at night. On nights 1, 5, 8, and 12, no forced awakenings were made. On all other nights, forced awakenings were made as indicated. TRC = total recall count; aw = active wake; qw = quiet wake; SO = sleep onset; NREM = nonrem sleep; REM = rapid eye movement sleep SLEEP, Vol. 24, No. 2,

3 from both REM and NREM sleep. The order for awakenings across the 14 days is shown in Figure 1. On sleep onset nights, subjects were repeatedly prompted for reports during the first hour after retiring for the night. Quiet wake reports were collected four and eight minutes after the Nightcap was turned on if the subject had not yet fallen asleep. Additional reports were collected each night after multiple awakenings, 15, 45, 75, 120, and 300 seconds into Nightcap-identified sleep, in a pseudorandom order. 13 Reports were collected continuously for the first hour of the night, after which subjects were allowed to sleep undisturbed through the remainder of the night. Reports collected from the sleep onset period but while the subject was awake were categorized as quiet wake (qw) reports. All others were classified as sleep onset (SO) reports. On REM first nights, subjects were awakened 10 minutes into their second REM period and then 15 minutes into the fourth NREM period of the night. On NREM first nights, they were awakened 15 minutes into their third NREM period and then 10 minutes into their third REM period. The use of the Nightcap to monitor sleep and to awaken subjects has been previously described for each of the awakening protocols: 1) no awakenings; 14 2) sleep onset awakenings; 13 and 3 & 4) awakenings in balanced order from both REM and NREM. 16 Regardless of protocol, reports were collected after all instrumental, spontaneous, and morning awakenings. Subject were given the same instructions for all conditions: When you awaken, think back and try to remember what was going on in your mind in the time prior to waking. Where did you think you were? Who else was there (i.e., in your dream)? What were you doing? What were you seeing, thinking, and feeling? What was happening around you? If no mentation was recalled, subjects were instructed to report this fact. In addition to reports collected in response to computer-directed awakenings, subjects were also instructed to report any mental activity they could remember from the period preceding every spontaneous awakening on the 14 nights. By definition, these represented all awakenings not initiated by the computer and thus included truly spontaneous awakenings as well as those triggered by environmental stimuli, such as roommates making noise or alarm clocks in the morning. Sleep recording: Sleep was monitored with the Nightcap sleep monitoring system Use of this compact recording system can be easily taught to subjects, who run the entire protocol without technical assistance. It s use with college students, 16 clinical patients, 17 and on-board the Mir space station 18 has been previously described. Report lengths: All reports were collected by dictation into hand-held microcassette recorders (Sony, Model M-770V), which automatically recorded the time and date of each report on the tape. Tapes were transcribed verbatim and subsequently edited for Total Recall Count, or TRC, 19 removing all extraverbal utterances (e.g., sighs, coughs, yawns), nonwords (um s and er s), repeated words (e.g., I was thinking about, thinking about ), and secondary elaborations (e.g., descriptions of related waking events). TRCs were obtained using the word-count function of Microsoft Word v5.1. TRC reports were put into a random order and provided to the judges, who were blind to the stage and subject from which each report originated. Statistical analyses: Statistical analyses were performed using StatView v4.5 and SuperANOVA v1.11. Because of the number of reports collected from each subject, as well as the number collected in each major report category, analyses could be carried out in a repeated measures design, with within-subject comparisons as well. Further breakdowns permitted analyses within each of the five major report categories, as described below. Descriptive statistic: All mean report times in Tables 1 and 2 were averaged across all reports in a given category. Similarly, all report frequencies are the ratios of the number of all reports with content to the number of reports in a given category. Median and mean TRCs were calculated for all reports in a given category. In general, median values are presented for clarity, and did not differ substantially from log-transformed values (see below). ANOVA s: All ANOVA s were calculated as repeated measures ANOVA s, with the dependent variable being the mean log- Table 1 Distribution of reports into major categories. The distribution of reports among the five major reporting conditions are given. Mean time of report - average clock time of reports in each condition, with nocturnal times prior to midnight treated as continuous with the subsequent AM period; time into Nightcap recording average time between turning on of Nightcap and initiation of report in minutes; Time into N/REM period average time between computer identified start of a REM or NREM period and the subsequent initiation of reports within that period. TOTAL ACTIVE WAKE QUIET WAKE SLEEP ONSET NREM REM Mean time of report - 5:02 PM 2:04 AM 2:27 AM 6:47 AM 6:59 AM Time into Nightcap recording (min) Time into N/REM period (min) # of reports # of reports with content (90%) (99%) (98%) (87%) (67%) (85%) # reports per subject - mean min max SLEEP, Vol. 24, No. 2,

4 transformed TRC for all reports within condition and subject. The log-transform was calculated as log 10 (TRC+1) 19. Correlations: Pearson correlation coefficients and significance tests were performed on log-transformed TRCs, either on a per report basis (REM and NREM reports; circadian and sleep time effects) or on per subject means (individual differences). RESULTS Distribution of Reports Each of the 16 subjects produced, on average, 117 reports, for a total of 1,867 reports, of which 1,748 (94%, mean=109 per subject) were validated for time and wake/sleep stage. Approximately half of these reports (51%) were obtained from the daytime paging protocol (mean=56 reports per subject), 20% from the sleep onset period (quiet wake and sleep onset; mean=22 per subject), and the remaining 29% from later REM and NREM awakenings (mean=32 per subject). These were almost evenly split between sleep stages (52% REM, 48% NREM). The specific breakdown of reports along with their mean report times is shown in Table 1. The frequencies of recall across sleep states 87%, 85%, and 67% for sleep onset, REM, and NREM are similar to the values obtained by Foulkes and Schmidt, 5 whose recall rates in sleep laboratory studies were 93%, 83% and 67%. Wake reports: Active wake reports were obtained four times a day by paging subjects at pseudorandom times. A total of 881 reports with content were collected. The distribution of reports among the four time periods, as well as mean report lengths, are given in Table 2 (wake). In most cases (90%) subjects produced at least three reports on a given day. The fourth scheduled report was collected on only 73% of the days. Report numbers permit both within and between subject comparisons across the four daily reports. Sleep onset reports: All told, 338 reports were obtained from the sleep onset period, including 58 from periods of quiet wake (qw) and the remainder after periods of of sleep (SO). The distribution of reports among these six conditions is given in Table 2 (sleep onset). Approximately equal numbers of reports (54 58) were obtained from each of the six conditions. Report numbers permitted comparisons across the six conditions, but did not permit within subject comparisons. REM and NREM reports: All told, 516 reports were obtained after the initial sleep onset period, either through computer-initiated forced awakenings at specific times in the REM/NREM cycle or following spontaneous awakenings. The distribution of reports among the four conditions (2 [spontaneous, forced] x 2 [REM, NREM]) is shown in Table 2 (REM/NREM). Approximately equal numbers of REM (n = 269) and NREM (n=247) reports were collected, but with almost twice as many spontaneous reports (n=336) as forced reports (n=180) in each state (REM: 175 vs. 94; NREM: 161 vs. 86). Report numbers permitted comparisons across the four conditions, as well as within subject for total REM and NREM reports and for spontaneous reports, but not for forced awakening reports. Report Length as a Function of State The length of reports was measured both by the total number of words in the reports (word count) and the number of distinct words used to describe the mental content from the period requested (total recall count, TRC). 19 On average, TRCs excluded 21% of the words in reports as redundancies, nonwords, and descriptions of material other than prior mental content. 19 The percent and absolute number of words removed per report varied by stage (repeated measures ANOVA s: for percent reduction, df = 4, F = 18.0, p < ; for word reduction, df=4, F=13.7, p<0.0001). For percentages, NREM report were reduced by Table 2 Distribution of reports into subcategories of major conditions. Columns are as described in Table 1; active wake: 1st through 4th reports are sequential reports on each reporting date; sleep onset: conditions are as described in methods; REM/NREM: REM and NREM conditions are divided into reports collected following Nightcap-calculated awakenings (forced) and reports collected following spontaneous awakening (spont.) Clock Time NC Time N/REM Time REPORTS REPORTS PER SUBJECT (total) w/content w/content (mean) (min) (max) ACTIVE WAKE 1st rpt 1:13 PM % nd rpt 4:08 PM % rd rpt 7:00 PM % th rpt 8:59 PM % SLEEP ONSET quiet wake 1:48 AM 13' % " 2:22 AM 33' % " 2:22 AM 35' % " 2:30 AM 34' % ' 2:12 AM 36' % ' 2:35 AM 37' % REM/NREM spont. REM 7:24 AM 354' 20.7' % spont. NREM 7:10 AM 333' 25.2' % forced REM 5:44 AM 241' 11.8' % forced NREM 5:46 AM 254' 18.9' % SLEEP, Vol. 24, No. 2,

5 35%, while the other four stages were reduced by only 17% 23%. For absolute lengths, qw and SO were reduced by words, while W, REM, and NREM were reduced by words per report. Even larger differences were seen across subjects whose average word reduction ranged from 14% 34% (33 55 words). Statistical analyses were carried out on TRCs, which are thought to more accurately reflect prior mental content. 14,19 TRC varied by major reporting state (Fig. 2; repeated measures ANOVA of log(trc+1), five states x 16 subjects, df=4, F=27.2, p<0.0001). Reports were significantly longer in REM (median=94 words) than quiet wake (median=55 words), sleep onset (median=44 words), and NREM (median=45 words) (contrast analyses, p< and F>26 for qw, SO, and NREM), and active wake reports (median=78 words) were significantly longer than quiet wake (F=11.8, p=0.001), sleep onset (F=43.8, p<0.0001), and NREM (F=37.6, p<0.0001). Quiet wake reports were also longer than sleep onset (F=10.1, p=0.002) and NREM reports (F=7.3, p=0.009). The only comparisons that failed to reach significance were those between NREM and sleep onset (F 100 df=5, F=1.7, p=0.16), although the mean decrease of 20% between waking reports and five min reports was nearly identical to the 21% decrease seen in a larger study of 865 sleep onset reports 13 and TRC showed a similar overall pattern of decreasing length with increasing sleep time. REM and NREM reports: REM and NREM reports were obtained either through forced awakenings at specific times in the REM/NREM cycle or when subjects awakened spontaneously. On average, reports from REM awakenings were twice as long as those from NREM (Fig.3) (median TRC = 94 vs. 45; repeated measures ANOVA of log(trc+1): 2 (sleep stage; REM and NREM) X 2 (awakening protocol; forced and spontaneous), n=16, main effect of sleep stage: df=1, F=48.7, p<0.0001). In contrast, the median length of spontaneous reports was only 27% greater than of forced awakening reports (median TRC=79 vs. 62; mean TRC=135 vs. 97), and the difference failed to reach significance (df=1, F=0.63, p=.44). Interestingly, an interaction between the awakening protocol and sleep stage was significant (df=1, F=7.4, p=0.02), with spontaneous REM reports longer aw qw SO NREM REM State Figure 2 TRC by major reporting state. Values are medians for all reports collected in each of the major reporting states. Error bars = s.e.m s. = 0.23, p = 0.63) and between active wake and REM (F = 3.0, p = 0.09). Thus, while SO reports have often been noted for their similarities to REM reports, their lengths were in fact even shorter than NREM. Wake reports: Wake reports were obtained four times a day by paging subjects at pseudorandom times. Median TRCs for the four times ranged from 74.0 to 79.5 words and did not differ significantly from one another (repeated measures ANOVA of log(trc+1), df=3, F=0.05, p=0.98). Thus, the length of reports obtained from subjects in the wake state did not depend on the time of day at which they were collected. Sleep onset reports: Sleep onset reports obtained from the pre-sleep quiet wake period and after periods of 15, 45, 75, 120, and 300 seconds of sleep varied in median length. Reports collected prior to sleep onset were significantly longer than those collected after sleep onset (paired t-test for log(trc+1), df=14, t=3.1, p=.008). When all six conditions were compared, the differences did not reach significance (repeated measures ANOVA, 0 REM NREM REM NREM Spontaneous Forced Figure 3 Median TRC as a function of REM/NREM stage and awakening protocol. Median TRCs and s.e.m s are shown for all reports collected from sleep reports obtained outside of the sleep onset protocol. Forced reports are those collected following computer-initiated awakenings. Spontaneous reports are reports collected from all other awakenings. than forced REM reports (df=15, t=2.66, p=0.02), but forced REM and NREM reports not significantly different in length (df=13, t=1.0, p=0.31). Because forced awakenings occurred at constant times within the REM/NREM cycle (10 minutes into REM or 15 minutes into NREM), no correlation could be measured between report length and time in REM or NREM. For spontaneous awakenings, however, a wide sample of times within stage was obtained. For these reports, TRC increased significantly with time in REM (log(trc+1), r=0.23, df=141, F=8.0, p=.005). While the median TRC increased by 59% from the first to third quarter hour of the REM period (Fig. 4A), the mean TRC increased by 134% (246 vs. 105 words). This difference between median and mean ratios reflects the presence of exceptionally long outliers in spontaneous reports from the third quarter-hour of the REM periods. In contrast, there was no significant change in TRC with time in SLEEP, Vol. 24, No. 2,

6 Time in stage (min) Figure 4 Median TRC as a function of elapsed time in REM and NREM for spontaneous awakenings. Spontaneous REM and NREM reports were classified by the time from start of the REM (filled circles) or NREM (open circles) period at which they were collected. No value for NREM, min. is given because only two reports were obtained. Error bars = s.e.m s. NREM (r=.07, df=96, F=0.49, p=.48) and the median TRC was actually greatest in the first quarter-hour of NREM (Fig. 4B). These results are similar to those reported previously. 2,3,14,20,21 One possible confound in these results would be if reports collected min into REM periods were generally collected later in the night than those collected 0 15 min into REM periods. But no such correlations were found. Across the four elapsed time in stage intervals for REM in Figure 4, mean time in bed differed by less than half an hour (range= min; ANOVA: df=3, F=0.41, p=0.74). Even less variation was found for NREM reports (range= min; ANOVA: df=2, F=0.10, p=0.96). Differences between forced and spontaneous report lengths: In our data set, the median TRC for spontaneous REM reports was 35% greater than for forced REM reports, and the mean difference was 48%. These values are important for the ongoing discussion of possible differences between home (spontaneous) reports and sleep laboratory (forced) reports. 22,23 Several explanations have been offered for these differences, including differences in: 1) setting; 2) subject populations; 3) number of nights of report collection; 4) time lag between awakening and reporting; 5) detrimental effects of forced awakening on recall and; (6) biased sampling in spontaneous collection protocols. Although our protocol eliminates the first four of these differences, the last two options remain. But our data suggest yet another explanation. Since spontaneous reports were, on average collected 20.7 minutes into the REM period, while forced reports were collected 11.8 minutes into the period (Table 2), and since spontaneous reports collected minutes into the REM period had a median TRC 56% greater than for reports collected in the first 15 minutes (Fig. 4A), the 35% difference seen between spontaneous and forced REM reports might simply reflect the time in REM at which reports were collected. SLEEP, Vol. 24, No. 2, To test this hypothesis, we analyzed 85 spontaneous REM reports from the first 20 minutes of REM periods. Reports were collected, on average, 11.8±0.5 (s.e.m.) min into the periods, the same as the 11.8 minute average seen for all forced reports. For these spontaneous reports, the median TRC was only 91 words, or only a statistically insignificant 14% more than forced REM reports (unpaired t-test of log(trc+1), df=166, t=1.12, p=0.26). Thus, the difference in the lengths of spontaneous and forced REM reports can be largely explained simply by the difference in time into REM at which the reports were collected. It is worth noting that this explanation would predict the observed similarity in lengths of forced and spontaneous NREM reports based on the absence of variations in TRC with elapsed time in NREM. Circadian and sleep time effects: In addition to the analyses presented above, it is also important to ask how report length varies as a function of the time of night at which the report was collected and as a function of the time since retiring to bed. Wake reports: As noted above, there was no significant variation in the length of reports obtained from wake subjects during the day as a function of time of day. Across the four reporting periods, median TRCs ranged only from 74.0 to 79.5 words. Quiet wake and sleep onset: Quiet wake and sleep onset reports were collected for a period of 60 minutes after subjects retired for the night. While report length overall showed a trend toward shorter reports as the hour progressed (r=0.11, df=299, F=3.63, p=0.06), this resulted entirely from the contribution of quiet wake reports at the start of the hour. When reports collected from sleeping subjects (i.e., after seconds of sleep) were analyzed, no correlation with time within the hour was seen (r=0.02, df=242, F=0.11, p=0.74). Similarly, quiet wake reports showed only a trend toward shorter lengths across the hour (r=0.20, df=55, F=2.24, p=0.14), and explained only 4% of the variance. In contrast, significant variations were seen based on clock time. At later times of night, quiet wake and sleep onset reports became progressively shorter (r=0.27, df=299, F=4.82, p<0.0001), decreasing from a linear regression best fit value for TRC of 68 words at 11 PM to only 30 words at 5 AM. Similar results were seen when quiet wake reports and sleep onset reports are analyzed separately, with wake-state reports decreasing in length from 91 words to 30 words and sleep-state reports from 61 words to 30 words. Thus, the later a subject went to bed, the shorter the sleep onset reports became. REM and NREM reports: Spontaneous REM and NREM reports showed mixed dependencies on clock time. Thus a linear regression for REM report length showed trends toward significant increases in TRC with time of night (r=0.11, df=149, p=0.16), varying from 97 words at 2 AM to 198 words at 10 AM, while a similar regression for NREM reports showed no trend (r=0.03, df=110, p=0.72), with a best fit varying only from 80 to 92 words over the same time period. In contrast, when report length was regressed against the elapsed time since subjects went to bed, NREM reports showed a significant correlation (r=0.22, df=110, p<0.02), increasing from 45 words two hours after retiring to 126 words after 9 hours. REM reports showed a similar pattern, increasing from 103 to 211 words in length between two and nine hours after retiring

7 (r=0.13, df=149, p=0.11). Gender differences: For four of the five main report states, women s reports were longer than men s, with the difference being greatest for NREM reports (65%) and smallest for sleep onset reports (-4%). However, a 2 (Gender; Men [n = 8] and Women [ n = 8]) X 4 (Stage; Wake, Sleep Onset, REM, and NREM) repeated measures ANOVA revealed no main effects or interactions of Gender on TRC (main effect of gender: df=1, F=2.15, p=0.16; interaction gender x report state: df=3, F=1.17, p=0.33). Individual differences: It has been known that the length of dream reports obtained from subjects shows large individual differences. But it has remained unclear whether these represent specific differences in dream recall or simply state-independent differences in reporting style. Because of the longitudinal design of the current study, we could address this question directly. If individual differences in dream report lengths reflected reporting style rather than varying intensities of dreaming, we would expect correlations between the lengths of a subjects waking and REM reports, or even between REM and SO reports, and that is what we found. The mean lengths of sleep onset reports for individual subjects was highly correlated with the mean lengths of their REM reports (r=0.74, df=14, p=0.001). The contingency table (Table 3), shows the correlation coefficients and p-values for all pairwise comparisons of active wake, sleep onset, NREM and REM report lengths. Quiet wake was not included because of the small number of reports per subject TRC qw NREM Figure 5 Distribution of qw and NREM report lengths. The percent of reports with TRCs within 25-word bins. NREM reports occur more frequently than qw reports in stippled regions, but at lower rates in the middle, striped region. 40% 30% Table 3 Contingency table for log transformed TRCs by report state. Pearson correlation coefficients and p-values (in parentheses) are given for all pairwise comparisons of mean TRC by subject (n=16) and reporting state. SO REM NREM aw (.11) (.13) (.14) SO (.001) (.046) REM.70 (.002) 20% 10% 0% Time in night (min) Figure 6 Frequency of long NREM reports across the night. The percent of NREM reports collected during each 90-minute interval of the sleep with TRC 125 is plotted for that interval. (mean=3.6) from this state. All three comparisons between sleep stages were significant, and active wake showed trends towards significant correlations with all three sleep stages (p<0.15 for each). Thus report length showed positive correlations at or near significance for all comparisons between the four states, aw, SO, NEM, and REM, again favoring the reporting style hypothesis. DISCUSSION To our knowledge, this is the first longitudinal study of waking, sleep onset, REM, and NREM mentation. Over 1800 reports were obtained from 16 subjects across wake and sleep states during 14 days, and with an average of 109 wake-sleep state validated reports per subject, individual differences could be analyzed. The collection of this large data set under naturalistic conditions was made possible by a combination of two techniques, portable sleep monitoring using the Nightcap and experience sampling. The Nightcap has been shown to reliably distinguish REM from NREM sleep 11,12 and to be effective in the collection of sleep mentation reports from instrumental awakenings at sleep onset 13 and from spontaneous REM and NREM awakenings across the night. 14 The effectiveness of experience sampling has been extensively documented by Csikszentmihalyi. 24 Report lengths: In this first paper we have focused on an analysis of the length of reports, quantified as the total recall count, or TRC. 19 Median lengths of reports from the five states active wake (aw), quiet wake (qw), sleep onset (SO), REM, and NREM varied in the order: REM aw > qw > NREM SO. But the use of a single number to describe report lengths is problematic. While the median TRC for NREM reports is 18% shorter than for qw reports, the mean NREM TRC is 26% longer. This difference reflects the dramatically different distributions of SLEEP, Vol. 24, No. 2,

8 TRCs in the two conditions (Fig.5). NREM is characterized by a relatively large number of very long reports (15% over 150 words, compared to none for qw), and very short reports (23% under 25 words, compared to 12% for qw. The breadth of the NREM TRC distribution results in part from the time of night effect described above. This finding of longer reports later in the sleep period is supported by those of others. 25 Indeed, the longest reports (TRC > 125) show a dramatic time of night effect (Fig. 6). Implications of report length findings: Our findings contradict the activation-only model of sleep mentation which proposes that all mental states exist on a single continuum, controlled by the level of activation of the brain, with a secondary determinant being the presence or absence of external sensory stimuli. But while overall brain activation, as indicated by EEG activity, is lower during NREM than either in quiet wake or at sleep onset, the mean TRC for NREM reports is 51% greater than at sleep onset and 26% larger than in quiet wake. Thus, report length is not positively correlated with level of brain activation across these sleep/wake states. Indeed, for many dream features, our results indicate that NREM mentation lies between sleep onset and REM, with sleep onset mentation closer to wake than to REM mentation. 30 It is only in terms of report frequency that sleep onset mentation shows a similarity to REM. This again argues against an activation-only model of dream construction. REM - NREM differences: Our finding that REM reports are longer than those from NREM is consistent with numerous prior studies. 5,14,19,21,31-33 But despite the robustness of this general finding, both absolute report lengths and the relative differences between the two states vary considerably between studies. Thus, Stickgold et al. 14 and Antrobus 19 found similar ratios of REM to NREM TRCs (4.9 and 4.1, respectively) while the TRC s reported by Stickgold et al. 14 were more than five times those of Antrobus. 19 In contrast, the REM/NREM TRC ratio in the current study is only 2.1. These differences point out the necessity of using longitudinal studies when comparing different sleep/wake states. The source of these inter-study differences has been a matter of some dispute. We have shown here that dream reports collected from REM sleep in the home following spontaneous awakenings show no significant difference in length from those obtained following forced awakenings if and only if reports are collected at similar times within the REM period. These findings are consistent with previous results, 2,3,14 which showed a positive correlation between time into a REM period and report length. We suggest that differences in length previously reported between home and laboratory reports are simply due to differences in the time in REM from which the reports were collected. Wake-state reports: Very little work has been done comparing sleep mentation with waking mentation. Wollman and Antrobus 34 reported that subjects exposed to moderate sensory deprivation produced significantly longer mentation reports than when awakened from REM sleep. In contrast, Williams et al. 35 found that reports of waking fantasies were significantly shorter than spontaneous dream reports collected from the same subjects. In the current study, reports from active wake (median TRC=78) and quiet wake (median TRC=55) were both significantly shorter than those from REM (median TRC=94). Individual differences: We have shown that subjects who tend to produce longer REM dream reports also produce longer SLEEP, Vol. 24, No. 2, reports in all other sleep/wake states. While median REM TRCs for the 16 subjects ranged from words, over half of this variability could be predicted from the length of the subjects sleep onset reports. Thus this variation is not specifically due to enhanced REM mentation. While it is impossible to distinguish whether these individual differences reflect differences in the intensity of their experiences or simply the detail of their descriptions, we can conclude that they do not reflect inter-subject differences in the regulation of the basic sleep/wake mechanism. CONCLUSIONS The study of dream reports provides important clues to how mental activity is altered by changes in brain state. The current study permits us to draw two critical methodological conclusions. First, studies from different laboratories, and even from a single laboratory, can show enormous differences in the length of mentation reports collected under similar conditions. Attempts to compare mentation data from different states collected in different studies is thus likely to be unreliable, even for such simple measures as report frequency and report length. It is critical, therefore, that such studies be conducted in longitudinal design, so that sufficient numbers of reports can be collected from each subject to permit repeated measures analyses of state-dependent variations in mentation. The ability to perform such studies in the home instead of the sleep laboratory opens this area of research to a much wider range of scientists than has hitherto been possible. It now appears that a critical source of the disparity in report lengths for dreams collected in the home and laboratory condition may result not from the sleep environment or the awakening protocol, but simply from how long subjects remain in REM before awakening and reporting. This conclusion suggests that longer and more narratively complex dreams can be collected in the sleep laboratory simply by shifting report times to later in the night as well as later in the REM period, and serves to integrate earlier studies of the effects on report length of the time of night 25 and time in the REM period. 2,3 Finally, the variation in report lengths across sleep/wake states raises questions about activation-only models of human mentation. Such models predict that NREM reports will be shorter than those from sleep onset, since levels of EEG activation are lower in NREM. Instead, the opposite order was observed, with NREM reports significantly longer than those from sleep onset, a mismatch that extends across a range of dream features not reported here. 15,30 The consistent finding of such discrepancies provides strong evidence that brain parameters other than overall brain activation and the presence or absence of sensory input are required to explain the variable nature of mentation across sleep/wake states. By being able to collect large databases of mentation reports in a longitudinal design across multiple sleep/wake states, it is possible to re-address several important questions concerning the natural variations in and physiological underpinnings of mental activity. For example, it would be of interest to probe the similarities and differences between waking and REM mentation more deeply, looking both at intersubject variability and at variations within subjects across distinct wake-state conditions. It would also be valuable to look at links between wake-state and

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