Biological Psychology 7 (1978) 3 7 - 5 3 © North-Holland Pubhshmg Company

BEHAVIORAL AND PSYCHOPHYSIOLOGICAL CORRELATES OF I R R E G U L A R I T Y IN C H R O N I C S L E E P R O U T I N E S * JOHN M TAUB** Sleep and Dream Laboratory, Department of Psychiatry, Umverstty of Vtrgmla Medical School, Charlottesvtlle, Vtrglnta, U S A Accepted for pubhcation 13 June 1978

Behavioral and psychophyslologlcal correlates of Irregularity m chromc sleep routines were studied Two groups each of 18 healthy male unxverslty students were classified as either trregular sleepers or control subjects according to retrospectwe questlonnatres, and sleep chart criteria The control group was composed of persons who slept naturally from 1 2 - 8 00 a m for 7 - 8 hr Irregular sleepers were defined as those whose rettrmg and awakening times vaned by about 2 - 4 hr Measurements were obtained from an auditory reaction time task, a mood adjectwe check hst, of subhngual temperature and pulse rate 30 mln after awakening m the (a) mornmg, at (b) noon, m the (c) afternoon and (d) early evening foUowmg an electroencephalographlcally recorded 1 2 - 8 00 a m. sleep mght At various points m the dmrnal cycle irregular sleepers compared with the control group had slgmflcantly lower levels of pulse rate and body temperature, but slgmficantly longer reaction times During the four time periods negative affects (deactivation-sleep, depression, general deactlvatton, mext-fatlgued) were significantly greater and posltwe mood states (cheerful, energetic, general actlvatmn- significantly less m the irregular sleepers The irregular sleepers averaged significantly less stage 4, and REM, but more stage 2 and transmons between sleep stages The present results indicate that relatively lowered levels of physiological arousal indexes, psychomotor performance and subjective mood are assocmted with trregularlty m chronic sleep routines of young adult males. These psychobehaworal correlates of chromcally maintained sleep pattern varmtlons complement and extend prevaous findings on degradations in waking functions foUowmg acute 2 - 4 hr temporal shifts of habitual sleep periods It is postulated that there were psychobehavloral deficits m the irregular sleepers attributable either to selectwe sleep stage (REM and/or stage 4) deprwation or to the more general consequence of disturbed sleeping patterns per se or to both of these factors.

1. Introduction P e r f o r m a n c e , physiological actwatlon, affecttve state a n d o t h e r such f u n c t i o n s are i n f l u e n c e d n o t o n l y b y p r i o r sleep or w a k e f u l n e s s , b u t also t~me o f day ( B a r r e t t * These results were presented m part at the Assocaatlon for the Psychophyslologlcal Study of Sleep, Houston, Texas, 27 April-1 May, 1977. ** Present address (to which requests for reprints should be sent) Sleep Laboratory, Department of Psychology, St Louis Umverslty, 221 N Grand Blvd, St Louis, MO 63103, U S A. 37

38

J M Taub / Correlates o¢ lpregular sleep

and Ekstrand, 1972, Blake, 1967, Hockey and Colquhoun, 1972, Rutenfranz, Aschoff and Mann, 1972, Taub and Berger, 1976b) Previous studies have demonstrated that acTlte alterations of the 24-hr or circadian sleep/waking cycle produce behavioral and psychological deficits Available evadence furthermore indicates that phase-shifts m this cycle not only affect sleep onset, the temporal dastnbutlon of various EEG sleep stages (Berger, Walker, Scott, Magnuson and Pollack, 1971, Hume and Mills, 1977, Taub and Berger, 1973b, Webb and Agnew, 1977), but also disrupt the normal biological rhythms of certain functions including neuroendocrme processes (Weltzman, 1975), vigilance, subjectave mood (Blatt and Qumlan, 1972, Taub and Berger, 1973a, 1974, 1976b), complex behavioral tasks and body temperature (Klein, Wegmann and Hunt, 1972) Sleep as a blorhytm (Webb, 1971) as entrained to the 24-hr day by recurrent envxronmental contingencies (or zettgebers) including behavioral scheduling (Webb and Agnew, 1974), our overall hvmg routine and social cues (Aschoff, Fatranska and Gledke, 1971) which are potent synchronizing agents for H o m o sapiens When zettgebers are altered, ehmmated or Ineffectual (see, e g, Miles, Raynal and Wilson, 1977) such that an accustomed clrcadaan sleeping pattern is not followed, diminished integrity m behavioral functions and disruption of the sleep cycle would appear to be a predictable result Is a sustained routine of regular sleeping tnnes equally essential to total sleep or its various stages for optimal behavioral effectavehess, subjective mood and physaologlcal arousal0 Changes m retmng and awakening times are among the most frequently occurring variations in the individual normal sleep/wakefulness cycle (Taub and Berger, 1973b, Taub, Hawkins and Van de Castle, 1978) Interlndlvldual differences are an important but neglected aspect of dmrnal vanatlon and activation (Akerstedt and Froberg, 1976) not extensively investigated with respect to sleep behawor In some persons changes m the phase and duration of sleep may be experienced continuously Little is known about the behaworal and psychophyslologlcal characteristics which may be related to thxs aspect of sleep habits 0 e , irregularity) The present study then was intended as one limited but feasible approach to further examine whether adequate sleep and optimal waking behavior would be assocmted with stablhty of chromc sleeping schedules It was not within the scope of this investigation to examine daytime rhytms m morning- or evening-active persons, but rather to study ~rregular sleepers with average sleeping schedules that fell in the vicinity of 12-8 00 am., and whose chromc sleep pattern varmtlons were also within the range typically occurring for the general population. Dmrnal varmtlons m waking behavior and the infrastructure of sleep itself in young adult human subjects whose nocturnal sleeping routines were chronically irregular were compared with yoked controls who habitually slept from mldmght to 8 00 am.

J M Taub / Correlates of trregular sleep

39

2 Method

2 1 Subjects Two groups each of 18 male university students were selected as subjects. An initial sample of 127 subjects was screened with a questionnaire that had both a forced- and multiple-choice format It was similar to that used previously (Taub, 1971) and contained Items from another sleep inventory (Agnew, 1970) Subjects were considered for further study according to questionnaire response criteria that ln&cated no obtrusive medical problems (e g , hypothyroidism, narcolepsy), psychiatric &sorders, daytime napping, disturbed nocturnal sleep, alcohol or drug abuse At thls stage in the screening procedure a group of irregular sleepers and of control subjects were selected Table 1 lists some of the major response criteria by which respondents were classified The controls reported having slept from 1 2 - 8 00 a m. for 7 - 8 hr over at least an tmmedlately preceding period of two years Irregular sleepers were defined as those whose subjective responses showed that during a corresponding period (two years), times of awakening, retmng and sleep duration vaned by about 2 - 4 hr The irregular group was categorized as such since previous findings (Taub and Berger, 1973a, 1974, 1976b) indicated that whenever an estabhshed 7 - 8 hr or 9 5 - 1 0 . 5 hr monophaslc nocturnal sleep period was acutely extended, phase-shifted or reduced by the same magnitude ( 2 - 4 hr) such mampulatlons all had detrimental effects on subsequent mood and psychomotor performance We were, therefore, interested to determine whether a self-selected and maintained Irregular sleeping regime would be analogous to deficits in measurable aspects of waking functmns. Sleep charts were the given to the potential subjects with instructions to record

Table 1 Subject selection-criteria quesnons Control group

1 2 3 4 5

I have fauly regular times for going to bed and getting up. I sleep at least 7 hours per mght I usually go to bed at about 12 mldmght. I wake up m the morning at about 8 a m. Most of the time I go to sleep at a certain time because it is a habit w~th me

Irregular sleepers

1 2

I have no fixed times for going to bed and/or waking up. The amount of sleep I obtain on any given mght usually fluctuates between 6 and 10 hours My time of going to bed is not very regular During the past two years my times for sleeping have varied from 2 to 4 hours My sleep habits have always been very Irregular

3 4 5

40

J 3I Taub / Correlates of Irregular sleep

for two weeks each 30-rain period of sleep SubJects were exchlded 1~questionnaire and chart indexes of sleep behavior differed by mole than 1 hr during that period The charts of subjects considered acceptable as controls indicated that they usually slept from mldnaght to 8 00 a m wathout evident sleep &sturbances or daytame naps. Subjects who quahfied as Irregular sleepers needed to have repolted tames of retiring, awakenang and sleep length that fluctuated by 2 - 4 hr at least 4 of every 7 nights So that predlsposatmns for extremely early or late retmng and awakening times would not confound the findings on diurnal rhytans (Home and Osterberg, 1977), we carefully selected irregular sleepers whose average sleeping schedules fell within the vacmlty of 12-8 00 a m The fllst subjects who satisfied the above cNterla were accepted into the study and paad $ 40.00 after completing their participation The subjects' ages ranged from 18 to 24 years and were similar an each group as were body weaghts (control group, X = 78 86 kg, irregular sleepers,X = 77 82 kg) The mean duratmn of arregular sleeping patterns was almost 8 years Two-week self-report records showed the average sleep length fo~ controls as 7 63 hr, and m the Irregular group It was 7 31 hr The subjects all had a samllar dally routine and none reported recent illness The final sample of irregular sleepers and control subjects were also admlnastered the California Personahty Inventory (CPI) Although we selected the groups with respect to sleep-wake habits, these factors reflected other personahty characteristics (Taub and Hawkins, 1978) Control subjects scored slgnaficantly (all p s < 0 002, 2-tailed U-tests) hagher on the CPI scales of Do (dominance), Sy (sociabilIty, Sa (self-acceptance), Sc (self-control), Ac (achievement wa conformance), and Ie (intellectual efficiency), but lower, p < 0 002, on the Fx (flexabahty) scale 2.2 Dependent variables

A continuous 10-mln task of simple audatory reaction time (Lisper and Ericsson, 1973, Lisper and Kjellberg, 1972) was used as a pelfo~mance measure Two selfreport inventories, the Actlvatlon-Deactavataon Adjective Check List (Thayer, 1970) and a multlfactorlal adjectave check last (Lol r, Daston and Smith, 1967) were used to measure mood. Pulse rate and subhngual temperature were used as andexes of physaologlcal actlvataon All testang was conducted in a semi-soundproof room whmh was darkened throughout the test (performance) phase of the experiment Reactton time For thas task the subjects were anstructed to press a mlcroswltch held in the preferred hand lmme&ately whenever an audatory stamulus was presented The reaction time signal was a 10kHz tone, 300 msec an duration wath rase and decay times of 10 msec A Sony Model TC-270 stereo tape recorder was used to present 150 of these stamuh to the subjects binaurally through headphones at 70-dB (SPL) mtensaty for a 10-man period The mean rater-stimulus anterval was sec with a range of 2 - 6 sec Four audiotapes were used with the sequence of presentation counterbalanced among subjects Reactaon tames were measured an 1-msec

J M Taub / Correlates of irregular sleep

41

units by an electronic timer (ERC Model 2613-31) and printed on a moduprmt &gital printer. Performance was measured as the mean reaction time for the entire I0 mln (150 stmauh) of the task About 5 - 7 days before the expertment, subjects practiced the task twice for 10 min Phystology. All physiological indexes except body temperature, but including the sleep variables, were recorded on a Grass Model 78 polygraph at a chart speed of 10mm/sec Pulse rate was measured continuously dunng the performance testing sesssxons with a photoplethysmograph (Brown, Gldden and Dean, 1965) attached to the index finger of the non-preferred hand. Mean values of pulse rate (per mm) were deterrmned from samples during each 30-sec recording epoch. The pulse rate was not corrected for respiration. Subhngual temperature was measured with a chmcal thermometer for 5 mm at the end of each testing session No food or beverages had been consumed during the 30-mm preceding measurement, and all recordings were obtained at thermoneutral temperature. Self-report The subjective rating scales were adjectives presented In randomized sequence Each adjective was scored on a 6-point intensity scale as 0 (not at all), 3 (moderately), and 5 (definitely) Five words served as a response-set measure 'ashamed,' 'careless,' 'comphant,' 'dizzy,' and 'truthful.' The multlfactor adjective check list was scored for seven factor-analytically determined scales as were the four factors from the Actwation-Deactwatlon inventory. 2 3. Design All subjects slept in the laboratory on two nights from 1 2 - 8 00 a.m under Identical conditions. Not more than five days of non-laboratory sleep intervened between adaptation and the sleep night of the study. The subjects were studied Individually during the same seasons of the year Since the irregular group reported chronic varlabihty in sleeping times, it was assumed that the dependent variables would not be directly Influenced by the imposed 12-8 00 a m . sleep schedule Itself Behavioral responses, pulse rate, subjective affective states and subhngual temperature were assessed at 4 time periods following the night of sleep (a) 30 rain after the subjects were awakened at 8 30 a m , before meals at (b) 12 00 noon, (c) 4 00 p m and (d) at 8 00 p.m. (testing periods are hereafter designated mornIng, midday, afternoon and evening respectwely). Although subjects did not remain m the laboratory during the time between these intervals, this was nevertheless preferred over confinement there for 12 hr In that respect the study approximated a normal waking day (cf Akerstedt and Froberg, 1976, Patkal, 1971) 2 4 Procedure Subjects were instructed not to nap or to dnnk caffelnated beverages, but to maintain their usual physical activity and food and fluid intake throughout the

42

I M Taub / Correlates of Irregular sleep

experiment SubJects were told that the study concerned the relationship between sleep and personality functioning SubJects reported to the laboratory by 10 00 p m , were required to ret'.re at mlgnlght and were awakened at 8 00 a m Electrodes were placed for recording electroencephalographic (EEG), electromyographic, and electrooculographlc activity All records were coded and scored blind for sleep stages by 30 sec epochs according to standard techniques (Rechtschaffen and Kales, 1968) The first sleep spindle was used to identify sleep onset (cf Agnew and Webb, 1972) as recommended by Johnson (1975) Each daytime session of the study began with the 10-rain performance task Simultaneously, pulse rate was recorded Then subjects were administered the selfreport scales Subhngual temperature was recorded after performance testing and the subjective ratings There were no cues present in the laboratory setting nor from the experimenter to inform subjects about their performance The self-report scales were administered after the behavioral task to minimize the posslblhty that performance or pulse rate would be affected by a cognitive set (Schachter and Stager,

1962)

3. Results One-way analyses of variance were computed to assess the overall magnitude of group &fferences in mean daily values for the waking behavioral variables Comparisons were performed for the sleep cycle variables and in levels of the daytime measures at each time period (morning, midday, afternoon, evening) between groups (controls versus Irregular sleepers) The Intergroup differences were assessed with 2-tailed t-tests for independent means all based on 34 d f 1 Time-of-day effects on reaction time, the self-report affective state/activation scales, pulse rate and subhngual temperatute in each group were evaluated with a trend analysts for the best fit polynomial 3.1 Performance Figure l shows mean reaction time in the morning, at midday, afternoon and evening for both groups Responses wele longer, F = 9 14, p < 0 005, in Irregular sleepers than controls at all time periods (ts > 2 53, all ps < 0 02) except in the evening Reaction times for the control group shortened from morning to midday, but were more rapid in the afternoon and became longer at 8 00 p m This U-shaped function was reflected by a significant quadratic component, F = 12 83, p < 0 0 0 l , I n the control group

1 All t-tests were compared with 2-tailed values of the Mann-Whitney U-test (Siegel, 1956) A result is reported as stanstteally slgmficant only when both tests corresponded at p < 0 05

J M Taub / Correlates of trregular sleep

43

SUBJECT G R O U F IRREGULAR --1 ~SE ~

260

U LU

1

~

._J

CONTROL

1

240 - -

Z 1

LU

220 - -

m

I--

Z

O

200 --

i-,,.

,¢ LLI

180 --

160 --

I

I

I

8 30a m

12~0p m

4O0p m

I 8~0p m

TIME OF DAY F~g 1 Diurnal vanatlon m reaction time foUowmg a night of 1 2 - 8

00 a m. sleep.

3.2 Affecttve state Scores on four negatwe mood state subscales from the adjectwe check list which showed statistically significant intergroup differences are shown m fig. 2 Compared wxth controls, scores m the irregular group were significantly elevated at each period besides across the dmrnal times for general deactwatlon, F = 24.96, inertfatigued, F = 46.64, deactwatlon-sleep, F = 33.23, and depression, F = 14 27 (all ps < 0 001). Like reaction time these negatwe affectlve states in controls exhlbzted a U-shape curve decreasing from morning to midday, attaining lowest values m the afternoon and rising at 8 00 p.m A quadratic component most closely approximated this trend for general deactwatlon, F = 62 65, deactwatlon-sleep, F = 32.99, and depression, F = 11 10 (all ps < 0.001), but not Inert-fatigued. Fig 3 shows subjectwe ratings for positive affectwe state scales which varied significantly between groups with respect to the various diurnal times. Energetic mood scores were sxgmficantly lower following the sleep mght m the irregular group than controls at all times of day, F = 35 18, p < 0 001. Irregular sleepers scored lower overall, F = 10 16, p < 0.005, on the cheerful subscale at all times (ts > 2.68, ps < 0.01), but not midday. Mean dally values of general actwatlon vaned slgmficantly, F = 11 7 8 , p < 0.005, but were lower in the Irregular sleepers only at midday and m

J M. Taub / Correlates o f zr~egular sleep

44

SUBJECT GROUP C~

~

IRREGULAR

I~ .....

•

CONTROL

:~SE

General

Deactivation

Inert-Fatigued

18 m

16 14

o "0 0 0

:E Q >

12 10

r'-...t/

8

6

IJ

0 ° ~ .Q

Q o ~

4

2

"3

1

0

8 a.

I

I

I

_ Deactivation-Sleep 10

Depression

D

0 "0 :) ° ~

f.

O~ O

8 30 am

12 O0 pm

4 O0 pm,

8"00 pm

Time

I

1

1

8 30 am

12 O0 pm

4 O0 pm

8.00 pm

of Day

I'lg 2 Dmrnal variation in negatwely rated subjective affectwe states following a night ol 12 8 00 a.m sleep

the afternoon (ts > 2 64, both ps < 0 01) There was a slgmflcant quadratic component for energetic, F = 23 86, and general actwatlon, F = 29 98, self-report scores (both ps