Research reportSharing stressful experiences attenuates anxiety-related cognitive and sleep impairments
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.
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