Thermal load alters sleep

136

Brief Reports

BIOL PSYCHIATRY 19X9:26.733- 736

of multidimensional activation vation Emotion 2: l-34.

Gillin JC (1983): The sleep therapies of depression. Progr Neuro-Psychopharmacol Biol Psychiatry 7:35 l-364.

Moti-

Van den Burg W, Van den Hoofdakker RH (1975): Total sleep deprivation in endogenous depression. Arch Gen Psychiatn’ 32:1121-l 125.

Horne JA (1978): A review of the biological effects of total sleep deprivation in man. Biol Psycho/ 7:55-102.

Van den Hoofdakker RH, Beersma DGM (1984): Sleep deprivation, mood and sleep physiology. Exp Brain Res (Suppl) 8:297-309.

Purcell AT (1982): The structure of activation and emotion. Multivariate Behavioral Res 17122l-25 1. Russell JA (1980): A circumplex model of affect. J Per Sot Psychol, vol 39: 6:1161-l 178.

Van den Hoofdakker the contribution explanation and Psychiatr Stand

Siegel S (1956): Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill, pp 229-239.

RH, Beersma DGM (1988): On of sleep wake physiology to the treatment of depression. Acta [Suppl] 34153-71.

Van den Hoofdakker RH, Beersma DGM, Dijk DJ, Bouhuys AL, Dols LCW (1986): Effects of total sleep deprivation on mood and chronophysiology in depression. In Shagass C, Josiassen RC, Bridger WH, Weiss KJ, Stoff D, Simpson GM (eds), Biological Psychiatry 1985, New York, Amsterdam, London: Elsevier. pp 969-971.

Tellegen A (1985): Structures of mood and personality and their relevance to assessing anxiety, with an emphasis on self-report. In Hussain Tuma A, Maser JD (eds), London, Hillsdale: Lawrence Gilbaum Associates., pp 681-706. Thayer RE (1967): Measurement of activation through self-report. Psycho1 Rep 20:663-678.

Von Zerssen D (1986): Clinical self-rating scales (CSRS) of the Munich Psychiatric Information System (PSYCHIS Mtinchen). In Sartorius N. Ban TA (eds), Assessment of Depression. Berlin: Springer, pp 270-303.

Thayer RE (1978a): Factor analytic and reliability studies on the activation-deactivation adjective check list. Psycho1 Rep 42~747-756. Thayer RE (1978b): Toward a psychological

(arousal).

theory

_

Thermal Load Alters Sleep Colin M. Shapiro, Moira Allan, Helen Driver, and Duncan Mitchell

Introduction The interaction among sleep, thermoregulation, and mood is complex. The characteristic changes in the sleep of depressed patients has recently

From the University Department of Psychiatry, Royal Edinburgh Hospital, Edinburgh, Scotland (C.M.S.); and the Edblo Sleep Laboratory, Department of Physiology, University of the Witwatersand Medical School Address reprint requests to Dr. Cohn M. Shapiro, Department of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Momingside Park, Edinburgh EHIO 5HF. Received September 7, 1988: revised January 23, 1989.

been reviewed by Reynolds and Kupfer ( 1987). The key changes include increased sleep disruption, a decrease in rapid eye movement (REM), sleep onset time, and a suppression of slow wave sleep (SWS). There is evidence from a variety of sources that there is a two-way interaction between sleep and mood state (Gillin et al. 1978; Duncan et al. 1980; Vogel et al. 1980; Wehr et al. 1987), although some view sleep change as an epiphenomenon of mood change (Mullen et al. 1986). With regard to the interaction between tem-

BIOL PSYCHIATRY 1989:26:736-740

Brief Reports

perature regulation and mood, depressed patients have been found to have both decreased amplitude of circadian temperature rhythm and raised nocturnal temperatures (Kramer and Katz 1978; Pflug et al. 1981; Avery et al. 1982a,b). Conversely, two reports suggest that altered environmental temperature may have an impact on mood state (Wehr et al. 1987; Kasper et al. in press). Considering the interaction of sleep and temperature, there is evidence that the occurrence of REM sleep is related to the circadian temperature cycle (Czeisler et al 1980), but paradoxically during REM sleep there is an inhibition of thermoregulatory function (Shapiro et al. 1974; Parmeggiani 1977, 1988). This disruption of thermoregulatory function during REM sleep is part of a wider disruption of autonomic nervous system control during REM sleep (Shapiro 1983) and may be relevant to the observation that suppression of REM sleep can induce an alteration of mood (Vogel et al. 1980). The interaction of SWS and temperature change has been conceptualized in two different ways. Some authors (Weitzman 1982, Shapiro et al. 1984) have considered the fall in body temperature during SWS as secondary to the sleep state. Other authors have seen the duration of SWS as a function of the fall in body temperature (Home and Reid 1984; Sewitch 1987). In a study on 6 women subjected to a cold stress on two consecutive nights, Sewitch et al. (1986) found that the cold stress impaired the continuity of sleep state, increased stage 4 sleep (but decreased stage 3 sleep), and induced a lengthening of the first non-REM period. There is evidence that pharmacological treatments used in affective disorders influence circadian rhythms (Wirz-Justice et al. 1979; Wehr and Wirz-Justice, 1982). Avery et al. (1986) noted that the circadian temperature rhythm is closely coupled to REM events and hypothesized that the short REM latency in depressed patients may be linked to the time of circadian temperature minimum. These observations led US to consider the manipulation of temperature and hence sleep as a possible way of altering

137

mood. Sewitch et al. (1986) recognized that a thermoregulatory challenge may be used as a nonpharmacological vehicle for normalizing sleep architecture in a certain subset of the insomnias. In view of these specific proposals, we have studied the limited effect of daytime thermal load on sleep patterns in a group of normal subjects to ascertain if a thermal load can induce changes in sleep opposite to those characteristically described as occurring in depression.

Method Twelve healthy young men aged 18-22 yr were selected from a student population. Subjects were studied in four groups of three and each group spent a total of 5 evenings in the sleep laboratory. Night 1 was an adaptation evening with full electrode attachments, but no sleep recording was carried out. Recording nights 2-5 were preceded by a 4-hr exposure to one of four preselected temperatures which were selected randomly in a Latin square design. The temperatures were 15X, 25”C, 35”C, and 45°C. The subjects were placed lightly clad in the temperature-controlled room (2.45 m X 2.75 m x 2.25 m) for 4 hr from 17.30 hr to 21.30 hr. They were allowed to move around freely but not to exercise or to alter the state of their clothing. They had no advance warning of the order of the test temperatures. They received an evening meal at their usual eating time while in the test environment. Oral body temperature was recorded hourly. No subject needed to be removed from the thermal exposure because of an inability to tolerate the thermal stress. The humidity was kept constant throughout. After leaving the test environment, each subject was prepared for sleep recording. Electroencephalograph, electro-oculograph, and submental electromyograph recordings were made throughout the night. Lights out was within a few min. of 11 PM, i.e., 1.5 hr after leaving the test environment. The laboratory environment and individual bedroom temperatures were not controlled but a record was made of the ambient temperature; this varied from 19°C to 26°C. The time lapse between test days was l-2 days.

Brief Reports

BIOL PSYCHIATRY 19X9:26:73&740

738

Minutes

\ F .\\

,lO No. of nocturnal

\

>I:

20

\ \ \ E \ \

\ \ 1 \ \

1

6

\ \

1

P

4

-.

1

'.

9

120'

1 150

I 25'

3&J

.2

I 450

Figure 1. Mean total slow wave sleep (in min) and total number of awakenings on each night after exposure total to four temperatures for 4 hr ending 1.5 hr prior to sleep onset. Total slow wave sleep (mins): -; number of awakenings: - - -.

One subject was removed from the study following the adaptation and first test night because of an allergy he experienced. The results are therefore based on 11 subjects who completed A = ls" o = 25' . = 35O .= 4P

L 55

s!

E

!

a 8

35 25

20

15

10 5

B

OL

1

2

no. of sleep

3

cycle

Figure 2. REM and slow wave sleep in each of the first three sleep cycles following exposure to different pre-sleep thermal loads. SWS: -; REM: - - -.

the full series of test scored “blind” at the to standard criteria 1968). The definition from first appearance of REM.

nights. Sleep records were end of the study according (Rechtschaffen and Kales for REM latency was time of stage 2 sleep to onset

Results Despite describing a greater sensation of fatigue at the high temperatures, there was no significant alteration in sleep onset latency among the various temperature exposures. Similarly, slow wave sleep onset latency showed no difference among the temperatures. However, total slow wave sleep (see Figure 1) and total sleep time were both significantly increased following exposure to 35°C and 45°C for 4 hr. Continuity of sleep was improved after exposure to the higher temperatures (see Figure 1). REM onset latency and total REM time were both longest after exposure to 2X, which is closest to a thermoneutral environment, and decreased both at the lower and two higher temperatures. The enhancement of SWS after higher temperature and the suppression of REM sleep with deviation from thermoneutrality, i.e., following ex-

BIOL PSYCHIATRY 1989:?6:736740

Brief Reports

Table 1. Sleep Stage Data Sleep

parameter (min)

15°C

25°C

35°C

45°C

10 6) 13 (17) 12 (6) 12 (3) Sleep onset 11 (7) 18 (19) 11 (6) 15 (6) Slow wave stg 3 sleep onset 85 (41) 110 (46) 88 (39) 87 (28) REM onset latency 446 (22) 447 (12) 462 (9) 460 (19) Total sleep time 3.2 (3) Wakefulness” 13.7 (10) 14.3 (13) 4.2 (6) 124 (49) 127 (49) 176 (25) 183 (35) Total slow wave sleep time” 93 (18) 85 (20) 96 (20) 105 (27) Total REM time Mean and (Standard Deviations) Te\t Temperature. ‘p < 0.01.

in Minutes (n =

11)for

739

alter both circadian rhythm and core temperature (Mellerup et al. 1978; Avery et al. 1982; Dilsaver and Majchrzak 1987). We have shown that the effect of heat stress produces sleep changes in normals similar to the effects induced by exercise, which is known to have mood elevating effects (Griest et al. 1979; Roth and Holmes 1987). As these sleep changes are opposite to those that occur during depression, it now remains to be seen whether one can induce mood changes in depressed subjects by altering thermal balance directly. The authors wish to thank Edblo (Africa) Ltd. and the Edinburgh Sleep Research Trust (REST) for support. We thank Mrs. Dodd for typing the manuscript.

Each

posure to temperatures of 15°C 35°C and 45°C

applied to each of the first three sleep cycles (Figure 2). Further details of sleep effects are shown in Table 1.

Discussion The results have borne out some of the predictions by Sewitch et al. (1986) but not others. Despite the marked increase in SWS and sleep continuity after exposure to heat, REM latency is shortened. This latter feature is in contrast with the effect of exercise on sleep (Shapiro et al. 198 1; Shapiro and Driver 1988). Depending on the level and intensity of exercise and the fitness of the subjects, exercise tends to prolong REM sleep onset latency (Montgomery et al. 1985; Driver et al, 1988). Home and Staff (1983) have inferred from indirect studies that the effect of exercise may be secondary to an effect on thermoregulation. We have briefly reviewed the interaction between the three biological processes: sleep, mood, and temperature regulation. There are clearly links between each pair of these processes. Furthermore, many of the treatments for depression

References Avery DH, Wildschiodtz G, Rafaelsen OJ (1982a): Noctumal tem~rature and affective disorder. I Ajjkt Disord 4% l-7 1. Avery DH, Wildschiodtz G, Rafaelsen OJ (1982b): REM latency and temperature in affective disorder before and after treatment. Biol P pchiatn; 17:463470. Avery DH, Wildschiodtz G, Smallwood RG, Martin D, Rafaelsen OJ (1986): REM latency and core temperature reIationships in primary depression. Acta P~chiatr Czeisler

&and 74:269-280.

CA, Zimmerman

JC, Ronda JM, Moore-

Ede MC, Weitzman ED (1980) Timing of REM sleep is coupled to the circadian rhythm of body temperature in man. Sleep 2:329-346. Dilsaver SC, Majchrzak MJ (1987): Decrease in core temperature as an indication of cholinergic overdrive during amitriptyline withdrawal. Biol Psychiatry 22: 1485-1487.

Driver HS, Meintjes AF, Rogers GG, Shapiro CM f 1988): Submaximal exercise effects on sleep patterns in young women before and after an aerobic training programme. Acta Physiol Scand 133, Supp 574: 8-13. Duncan WC, Gillin JC, Post RM, Gemer RH, Wehr TA ( 1980): Relationship between EEG sleep patterns and clinical improvement in depressed patients treated with sleep deprivation. Rioi Psych~ut~, 15:879-889. Gillin JC, Wyatt RJ, Fram D, Snyder F (1978): The relationship between changes in REM sleep and clinical improvement in depressed patients treated

740

Brief Reports

BIOL PSYCHIATRY 1989:26:136-140

with amitriptyline. 272.

Psychopharmacology

59:267-

Greist JH, Klein MH, Eischeins JF, Gurman AS, Morgan WP (1979): Running as a treatment for depression. Camp Psychiatry 20:4 l-54. Horne, JA, Reid AJ (1984): Night-time sleep EEG changes following body heating in a warm bath. Electroenceph Clin Neurophysiol 60: 154- 157. Home JA, Staff LHE (1983): Exercise Body-heating effects. Sleep 6:36-46.

and sleep:

Kasper S, Wehr TA, Bartko JJ, Gaist PA, Rosenthal NA (1989): Epidemiological findings of seasonal changes in mood and behaviour (in press). Kramer BA, Katz JL (1978): Circadian temperature variation and depressive illness. J Clin Psychiatry 39:439-444.

Roth DL, Holmes DS (1987): Influence of aerobic exercise training and relaxation training on physical and psychologic health following stressful life events. Psychosom Med 49:355-365. Sewitch DE (1987): Slow-wave sleep deficiency insomnia: Problem in thermo-downregulation at sleep onset. Psychophysiology 24:200-2 15. Sewitch DE, Kittrell MW, Kupfer DJ. Reynolds CF (1986): Body temperature and sleep architecture in response to mild cold stress in women. Physiol Behav 36:95 l-957. Shapiro CM (1983): Autonomic nervous system dysfunction during REM sleep. In Sleep 1982. Koela, WK, (ed). Sleep 1982. Base1 Karger:. pp 80-88. Shapiro CM, Driver HS (1988): Exercise and Sleep: A review. NATO Colloquium. New York: Plenum Press (in press).

Mellerup ET, Widding A, Wildschiodtz G, Rafaelsen OJ C1978): Lithium effect on temperature rhythm in psychiatric patients. Acta Pharmacology and Toxicology 42: 125-129

Shapiro CM, Bortz R, Mitchell D, Bartel P. Jooste P (1981): Slow-wave sleep: A recovery process after exercise. Science 2 14: 1253- 1254.

Montgomery I. Trinder J, Paxton S, Fraser G, Meaney M, Koerbin G (1985): Sleep disruption following a marathon. J Sports Med 2.5~69-74.

Shapiro CM, Gall CC, Cohen GR, Oswald I ( 1984): Heat production during sleep. .I Appl Physiol 56:671-677.

Mullen PE, Linsell CR, Parker D (1986): Influence of sleep disruption and calorie restriction on biological markers for depression. Lancer ii: 105 l1058.

Shapiro CM, Moore AT, Mitchell D, Yodakien ML C1974): How well does man thermoregulate during sleep? Experientiu 30: 1279-l 28 I.

Parmeggiani PL (1977): Interaction between sleep and thermoregulation. Waking and Sleeping 1: 123132.

Vogel GW, Vogel F, McAbee RS. Thurmond AJ (1980): Improvement of depression by REM sleep deprivation. Arch Gen Psychiatry 37:247253.

Parmeggiani PL (1988): State of the art review. Interaction between sleep and thermoregulation: An aspect of the control of behavioural states. Sleep 10:426-436.

Wehr TA. Wirz-Justice A (1982): Circadian rhythm mechanisms in affective illness and in anti-depressant drug action. Pharmucopsychiutn 15:3 l39.

Pflug B, Johnson A, Ekse AT (1981): Manic depressive states in daily temperature. Some circadian studies. Acta Psychiatr Stand 63:277-289.

Wehr TA, Sack DA, Rosenthal ME (1987): Sleep reduction as a final common pathway in the genesis of mania. Am J Psychiatry 144:201204.

Rechtschaffen A, Kales A (eds) (1968): A Manual of Stundardized Terminology, Techniques and Scoring System ,for Sleep Stages of Human Subjects. Washmgton, DC: Public Health Service, U.S. Government Printing Office. Reynolds CF, Kupfer DJ (1987): Sleep research in affective illness: State of the art circa 1987. Sleep 10:199-215.

Weitzman ED (1982): Chronobiology temperature and neuroendocrine Neurobiol I: 173-I 83.

of man. Sleep. rhythms. Hum

Wirz-Justice A, Puhringer W, Hole G (1979) Rcsponse to sleep deprivation as a predictor of therapeutic results with antidepressant drugs. Am J Psychiutrv 136: 1222-1223.