Elsevier

Behavioural Brain Research

Volume 222, Issue 2, 23 September 2011, Pages 351-356
Behavioural Brain Research

Research report
Sharing stressful experiences attenuates anxiety-related cognitive and sleep impairments

https://doi.org/10.1016/j.bbr.2011.03.065Get rights and content

Abstract

Anxiety is a growing public health concern that has been shown to impair both sleep and learning, and these associations have been extensively studied in recent years. In the rodent model, oftentimes various foot-shock paradigms are employed to induce stress, and subsequent sleep recordings and/or learning task results are analyzed. Previous studies have focused primarily on an individual animal's response to stress following individual stressor exposure, thereby emulating only an isolated condition. The goal of this study was to investigate the effects of socialization on stress response, and the resultant effects on sleep architecture and aversive learning. A pair-housing/pair-exposure paradigm was utilized, and the effects of unavoidable foot-shock-induced stress on sleep architecture and aversive learning were examined. The results of the present study indicate a large, positive impact of cohabitation and shared stressful experience, as rats failed to develop sleep disturbances or learning deficits. While these results indicate the benefits and importance of companionship, the underlying mechanism of this phenomenon is yet to be elucidated.

Highlights

► Pair-housing and pair-exposure effect on sleep and learning after stressor exposure. ► Socialization mitigates changes in sleep architecture after stressor exposure. ► Socialization mitigates changes in aversive learning after stressor exposure.

Introduction

Stress and anxiety are serious issues that have negative, long-lasting effects on individual physical and mental health, as well as costly implications to society as a whole [1], [2]. Anxiety and its related disorders are responsible for considerable financial and productivity losses [1]. A vast number of studies have suggested that stress and anxiety are linked to a variety of mental health disorders and neurodegenerative diseases, and that even low levels can trigger comorbidities including depression and insomnia [3], [4], [5], [6], [7], [8]. In animal models, a single brief exposure to social stress can elicit gradual but chronic behavioral changes, characteristic of depression and post-traumatic stress disorder [9], [10], [11], [12], [13], [14], [15], and can also induce long-term changes in the neuroendocrine system [12], [16], [17], [18], [19], [20], [21], [22]. Additionally, previous studies have indicated that social anxiety and stress may be linked to drug abuse, as defeated male rats developed self-administration cocaine habits twice as quickly as non-defeated males [23]. It has also been shown that stressful and traumatic events are often followed by persistent disturbances in sleep, and these sleep disturbances may be predictive of future psychiatric pathologies [24], [25]. Alternatively, problems initiating and maintaining sleep may trigger anxiety disorders [24], [26], [27]. Interestingly, both insomnia and hypersomnia are common complaints of patients with anxiety disorders [27], [28], [29].

To study the immediate effects of anxiety and stress, many researchers utilize the rodent model as a convenient method for analyzing behavioral and pharmacological responses to stress. One of the most popular methods is fear conditioning training associated with stress induced by unavoidable foot-shock [15], [30], [31], [32], [33], [34]. Animals used to study anxiety and stress, using this type of unavoidable foot-shock, were housed and exposed to foot-shock individually [7], [8], [9], [14], [15], [30], [31], [32], [33], [34], [35], [36]. This type of animal model is ideal to measure acute responses to a foot-shock stressor by emulating a condition of an individual living in isolation and facing a stressor alone. In reality, however, socialization and cohabitation are common, and the likelihood of people encountering stressful experiences together is far greater, in which case they are likely to respond differently from isolated individuals. In order to study the effects of stress in this type of social condition, experimental animals should be housed and foot-shocked in pairs. To our knowledge, no published study has used this paired-subject model to describe the effects of foot-shock-induced stress on an individual's sleep architecture or capacity for aversive learning.

A different but equally popular rodent model to study stress and anxiety is the resident-intruder paradigm in which two male rodents are placed into a single cage and allowed to fight for a predetermined amount of time [13], [37], [38]. Such an encounter is known as “social defeat” and the winner is generally referred to as the dominant animal; the loser is referred to as the subordinate. Unfortunately, this type of behavior is not exclusive to animals, and in fact humans sometimes also use aggression to establish their social dominance [39]. More importantly, this type of aggressive encounter, in humans, occurs not only between strangers, but also between siblings, close friends, life partners, and neighbors. Aggression has also been linked to numerous psychiatric disorders, including autism, schizophrenia, affective disorders, and suicidal behaviors [40], [41], [42], [43], [44]. To our knowledge, no published study has systematically examined the effects of aggressive encounters on the sleep–wake activity or learning ability in humans or animals.

The present study, for the first time, examines the immediate effects of cohabitation, stressor exposure, and stressor-induced aggressive encounters on sleep–wake architecture, contextual fear memory, and avoidance learning in the rat model. Both dominant and subordinate members of a socially housed pair were tested, to determine whether social rank has any effect on the aforementioned parameters. In this study, dominant and subordinate rats were housed in a single cage and also received foot-shock together. The results of the present study have been compared with our recently published studies which used an identical experimental protocol, except in those two studies animals were single-housed and individually exposed [30], [32]. Compared to single-housed, individually exposed animals, this study shows that when two rats living together are subjected to a foot-shock stressor and incited to aggression, these rats exhibit normal sleep–wake architecture, contextual memory, and avoidance learning ability. These results, for the first time, indicate that social support during stressful experiences may have an attenuating effect on the susceptibility to sleep disturbances and learning impairments.

Section snippets

Subjects and housing

Experiments were performed on 20 adult male Wistar rats (Charles River Laboratories, Wilmington, MA) weighing between 350 and 450 g. The rats were housed in pairs (two animals per cage) at 24 °C with ad libitum access to food and water. A 12-h light/dark cycle was maintained, with lights on from 7:00–19:00 h and darkness from 19:00–7:00 h. The principles for the care and use of laboratory animals in research, as outlined by the National Institutes of Health Guide for the Care and Use of Laboratory

Results

A total of six pairs of rats expressed SIA behavior. Based on the behavioral criteria described above, one rat within each pair was labeled dominant and the other rat was labeled subordinate. Within each pair, the dominant animal was slightly heavier (2–3% of total body weight) than its subordinate cage mate. However, the mean body weight of the dominant group was not significantly different than the mean body weight of the subordinate group (t-test; df = 5; t = 1.33; p = 0.24). The following results

Discussion

The principal findings of this study demonstrate that animals assuming a dominant or a subordinate role develop no significant differences in sleep architecture, fear memory or aversive learning after exposure to fear-inducing foot-shock. Shock-induced aggressive stimulus had no significant effect on sleep architecture in either experimental group. Furthermore, shock-induced aggression did not affect the animals’ ability for aversive learning, as compared to non-shocked control animals. The

Conclusion

The present study indicates that social buffering may be a useful tool for mitigating the anxiogenic effects of a stressful experience, while leaving cognitive abilities unimpaired. The findings of this animal study have important implications, and may impact clinical research ranging from panic attacks to post-traumatic stress disorder. The use of cohabitation as a clinical tool provides an alternative or a supplementary treatment for myriad psychiatric afflictions, and may provide a framework

Disclosure/conflict of interest

The authors declare there is no conflict of interest. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Acknowledgements

This research was supported by National Institutes of Health Research Grants MH59839 and NS34004. We acknowledge and thank Ms. Holly Carria for technical assistance.

References (83)

  • S.M. Korte

    Corticosteroids in relation to fear, anxiety and psychopathology

    Neurosci Biobehav Rev

    (2001)
  • J.A. Costa e Silva

    Sleep disorders in psychiatry

    Metabolism

    (2006)
  • M.P. Huang et al.

    Effects of eszopiclone and zolpidem on sleep–wake behavior, anxiety-like behavior and contextual memory in rats

    Behav Brain Res

    (2010)
  • Y.J. Ho et al.

    Individual response profiles of male Wistar rats in animal models for anxiety and depression

    Behav Brain Res

    (2002)
  • R.R. Maclean et al.

    The relationship between anxiety and sleep–wake behavior after stressor exposure in the rat

    Brain Res

    (2007)
  • L.D. Sanford et al.

    Tetrodotoxin inactivation of pontine regions: influence on sleep–wake states

    Brain Res

    (2005)
  • J.M. Koolhaas et al.

    The temporal dynamics of the stress response

    Neurosci Biobehav Rev

    (1997)
  • M. Fava

    Psychopharmacologic treatment of pathologic aggression

    Psychiatr Clin North Am

    (1997)
  • S. Datta et al.

    A novel role of pedunculopontine tegmental kainate receptors: a mechanism of rapid eye movement sleep generation in the rat

    Neuroscience

    (2002)
  • N. Adams et al.

    Development of dominance in rats in laboratory and seminatural environments

    Behav Processes

    (1989)
  • S. Datta et al.

    Identification of cholinergic and non-cholinergic neurons in the pons expressing phosphorylated cyclic adenosine monophosphate response element-binding protein as a function of rapid eye movement sleep

    Neuroscience

    (2009)
  • R.J. Blanchard et al.

    Aggressive behavior in the rat

    Behav Biol

    (1977)
  • X. Tang et al.

    Strain differences in the influence of open field exposure on sleep in mice

    Behav Brain Res

    (2004)
  • X. Tang et al.

    Interactions between brief restraint, novelty and footshock stress on subsequent sleep and EEG power in rats

    Brain Res

    (2007)
  • G. Vazquez-Palacios et al.

    Effect of electric foot shocks, immobilization, and corticosterone administration on the sleep–wake pattern in the rat

    Physiol Behav

    (2000)
  • T.L. Creer

    Hunger and thirst in shock-induced aggression

    Behav Biol

    (1973)
  • M.A. Ruis et al.

    Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat

    Psychoneuroendocrinology

    (1999)
  • T. Nakayasu et al.

    Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats

    Behav Processes

    (2008)
  • J.C. Von Frijtag et al.

    Defeat followed by individual housing results in long-term impaired reward- and cognition-related behaviours in rats

    Behav Brain Res

    (2000)
  • M.B. Hennessy et al.

    Social buffering of the stress response: diversity, mechanisms, and functions

    Front Neuroendocrinol

    (2009)
  • K. Karelina et al.

    Social contact influences histological and behavioral outcomes following cerebral ischemia

    Exp Neurol

    (2009)
  • B. Chua et al.

    Effects of pair versus individual housing on the behavior and performance of dairy calves

    J Dairy Sci

    (2002)
  • A. De Paula Vieira et al.

    Effects of pair versus single housing on performance and behavior of dairy calves before and after weaning from milk

    J Dairy Sci

    (2010)
  • D.A. Gust et al.

    Effect of a preferred companion in modulating stress in adult female rhesus monkeys

    Physiol Behav

    (1994)
  • L.A. Pohorecky et al.

    Social housing influences the composition of volatile compounds in the preputial glands of male rats

    Horm Behav

    (2008)
  • J.H. Wilson

    A conspecific attenuates prolactin responses to open-field exposure in rats

    Horm Behav

    (2000)
  • M. Marciniak et al.

    Medical and productivity costs of anxiety disorders: case control study

    Depress Anxiety

    (2004)
  • B.S. McEwen

    Physiology and neurobiology of stress and adaptation: central role of the brain

    Physiol Rev

    (2007)
  • T. Esch et al.

    The role of stress in neurodegenerative diseases and mental disorders

    Neuro Endocrinol Lett

    (2002)
  • F. Marinia et al.

    Single exposure to social defeat increases corticotropin-releasing factor and glucocorticoid receptor mRNA expression in rat hippocampus

    Brain Res

    (2006)
  • L.L. Wellman et al.

    Contextual fear extinction ameliorates sleep disturbances found following fear conditioning in rats

    Sleep

    (2008)
  • Cited by (0)

    View full text