Differential effects of acute cold and footshock on the sleep of rats

doi:10.1016/S0006-8993(00)02024-2

Brain Research

Volume 861, Issue 1, 7 April 2000, Pages 97-104

https://doi.org/10.1016/S0006-8993(00)02024-2 Get rights and content

Abstract

Several studies have shown that 1 h of immobilisation stress during the rat's active period results in rebound of paradoxical (PS) and slow wave sleep (SWS). Since the effects of stress on behaviour and physiological parameters vary according to the stimulus, the present study sought to examine the activation of the hypothalamic-pituitary-adrenal (HPA) axis and the sleep pattern of rats submitted to 1 h of footshock, immobilisation or cold, or 18 h of PS deprivation (PSD). Stress sessions began between 0900 and 0930 h. Immediately after the end of the stress session, or at the corresponding time for controls, animals were blood sampled for determination of ACTH and corticosterone (CORT) plasma levels. In Experiment 2, animals were implanted with electrodes for basal and post-stress polysomnographic recording (6 h long). The results showed that all stressors produced an activation of the HPA axis; however, footshock induced the largest ACTH levels, whereas cold resulted in the highest CORT levels. In regard to the sleep data, immobilisation and PSD led to a rebound of SWS (+16.87% and +9.37%, respectively) and PS (+42.45% and +55.25%, respectively). Immobilisation, however, induced an increased number of PS episodes, whereas PSD resulted in longer PS episodes. Cold stress produced an exclusive rebound of SWS (+14.23%) and footshock promoted sustained alertness during the animal's resting period (+47.18%). These results indicate that different stimuli altered the sleep pattern in a distinct manner; and these alterations might be related to the state of the HPA axis activation.

Introduction

Sleep, as any behaviour, is affected by several kinds of disturbances, such as stress. According to Opp [27], sleep patterning may be a useful response marker for a variety of stimuli for two reasons. First, it is based in established criteria and is well defined and quantifiable. Second, sleep represents the summation of multiple systems that may be differentially altered by stress. Thus, the degree by which the sleep–wake cycle is modified by a specific stressor may be an indicator of the magnitude of such stressor as well as the activation of the hypothalamic-pituitary-adrenal (HPA) axis.

The influence of stress on sleep has been the focus of a number of studies, both in humans and in laboratory animals. Stress has been associated to anxiety and depression [3]. In a recent survey, 95% of depressive and anxious patients reported sleep problems; insomnia was the most frequent complaint [40]. Moreover, depressive patients present, simultaneously, high cortisol plasma levels and reduced latency to REM sleep and augmented time of REM sleep on the first half of the night, when there is a predominance of slow wave sleep (SWS) 2, 15, 33.

In animals, altered sleep patterning is observed in rats submitted to a 2-h immobilisation stress (during their active period). Four hours after the stressor, these animals present a 32% rebound of paradoxical sleep (PS), without rebound of SWS [30]. If, however, the animals were submitted to 1 h of immobilisation, a 63% PS rebound and a 16% SWS rebound were observed [5]. Interestingly, repeated exposures to immobilisation lead to a progressive reduction of sleep rebound compared to single exposure [30]. A similar effect is observed following uncontrollable [21] and inescapable footshock [1], suggesting that habituation may take place 12, 34. Likewise, other stressors also influence sleep. Thus, exposure of animals to 1 h of social defeat results in 183.1% increase of the slow wave activity, suggesting that sleep may function as a compensation for the injuries to which the central nervous system is exposed during waking [24].

Data collected in other and our laboratories indicate that both physiological and behavioural responses to stress vary according to the stimuli. Thus, yawning is suppressed by constant prolonged exposure to stress, but not by prolonged intermittent exposure [38]. Similarly, sleep deprivation and isolation augment the activity of the immune system in an animal model of Lupus Erytemathosus, whereas immobilisation, footshock and swimming fail to induce any alteration [23]. Finally, 2 h of restraint stress results in down-regulation of 5-HT_1a serotonergic receptors, whereas 15- or 30-min of swimming stress leads to the opposite effect [29].

In view of the somewhat differential effects of different stressors on neurotransmitter systems and organic responses, we sought to investigate the consequences of the acute exposure to several stressors on the sleep architecture of rats.

Section snippets

Subjects

Wistar male rats, 3 to 4 months old, weighing 300 to 430 g and raised in the animal facility of the Department of Psychobiology (UNIFESP-EPM) were used in this study. The animals were maintained in plastic cages, in groups of five, inside a room with controlled temperature (23±2°C) and 12-h light/12-h dark cycle (lights on at 0700 h). Food and water were available ad libitum throughout the study.

Stress procedures

(1) Immobilization: 10 animals were placed, individually, inside plastic cylinders (21×6 cm

ACTH levels

Due to the large variability within groups, data were converted to log and reanalysed (Fig. 1, upper panel). ANOVA revealed a difference among the groups [F(4,43)=52.57; P<0.0001]. Post hoc comparison showed that all stress groups presented a higher response than control (P<0.0001); footshock, however, induced the highest ACTH response (P<0.0002). Both immobilization and PS deprivation resulted in levels higher than cold (P<0.001), which in turn was higher than control values (P<0.01).

CORT levels

ANOVA

Discussion

The results of the present study showed that the stimuli employed produced a reliable activation of the HPA axis, with elevated plasma levels of ACTH and CORT. Nonetheless, these augmented responses, as well as the effect of the stimuli on the sleep architecture of rats occurred in a differential fashion.

Footshock was the only stressor that produced a state of prolonged alertness, with a reduction of TST and of sleep efficiency, and an elevation of TAT, whereas cold stress was the only one to

Acknowledgements

This work was supported by grants from Associação Fundo de Incentivo à Psicofarmacologia (AFIP) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP). Beatriz Duarte Palma and Deborah Suchecki are fellows from FAPESP, grants # 96/12545-4 and 9704857-9. The authors would like to thank Denise Zeminiani Theodoro and Tomé Pimentel dos Anjos for their valuable assistance in the hormone assays and blood sampling and to Jackson Cionek for technical support on the polysomnography equipment.

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Research reportDifferential effects of acute cold and footshock on the sleep of rats

Abstract

Introduction

Section snippets

Subjects

Stress procedures

ACTH levels

CORT levels

Discussion

Acknowledgements

Physiol. Behav.

J. Affective Disorder

Adv. Neuroimmunol.

Neurophysiol. Clin.

Brain Res.

Behav. Brain Res.

Neurosci. Lett.

Life Sci.

Adv. Neuroimmunol.

Neurosci. Lett.

Brain Res.

Physiol. Behav.

Eur. J. Pharmacol.

Physiol. Behav.

Neuropeptides

Eur. J. Pharmacol.

The role of corticotropin-releasing factor in depression and anxiety disorders

J. Endocrinol.

Gluco- and mineralocorticoid effects on human sleep: a role of central corticoid receptors

Am. J. Physiol.

Possible involvement of the arcuate nucleus in the sleep rebound induced by an immobilization stress

J. Sleep Res.

Axonal and somato-dendritic modalities of serotonin release: their involvement in sleep preparation, triggering and maintenance

J. Sleep Res.

Voltammetric detection of the release of 5-hydroxindole compounds throughout the sleep–waking cycle of the rat

Exp. Brain Res.

Research report
Differential effects of acute cold and footshock on the sleep of rats