Elsevier

Physiology & Behavior

Volume 194, 1 October 2018, Pages 177-183
Physiology & Behavior

The benefits of social buffering are maintained regardless of the stress level of the subject rat and enhanced by more conspecifics

https://doi.org/10.1016/j.physbeh.2018.05.027Get rights and content

Highlights

  • We conditioned subject rats to have low, moderate, or high stress levels.

  • The intensity of social buffering was similar among the subject rats.

  • Three associate rats further reduced stress responses in high stress subjects.

Abstract

Social buffering is a phenomenon in which the presence of an affiliative conspecific (associate) mitigates stress responses in a subject. We assessed the relationship between the stress level of subjects and the benefit of social buffering. In Experiment 1, subjects fear-conditioned using 0.15-mA, 0.45-mA, or 0.70-mA foot shocks were re-exposed to a conditioned stimulus (CS) either alone or with an associate on the day following fear conditioning. We found that behavioral responses were reduced by the presence of an associate. The intensity of this decrease was similar among all subjects. These results suggest that the intensity of social buffering was similar regardless of the stress level of the subject. The high stress subjects showed residual stress responses after receiving social buffering, indicating that the residual stress responses may have been resistant to social buffering. To further examine this, subjects fear-conditioned using 0.70-mA foot shocks were re-exposed to the CS either alone, with one associate, or with three associates in Experiment 2. We found that behavioral responses decreased as the number of associates increased. These results suggest that residual stress responses are further ameliorated when the number of associates increases. Therefore, the residual stress responses were also sensitive to buffering. Taken together, our data indicate that the benefits of social buffering are maintained regardless of the stress level of the subject rat and enhanced by more conspecifics.

Introduction

The presence of an affiliative conspecific, or cues associated with a conspecific, has been found to reduce stress responses to a wide variety of stimuli ranging from novel environments [1,2] to specific aversive stimuli [[3], [4], [5]]. This phenomenon is called “social buffering” [6]. Investigating social buffering may illuminate the origins of sociality in animals. That the stress response of one animal can be reduced by the presence of another animal may have contributed to the tendency to live in groups, thus leading to sociality in specific species. Social buffering is similarly observed in humans and improves human health as a part of the benefit of social support [7,8]. Thus, a better understanding of social buffering in non-human animal models may have enormous translational values. Ample studies have demonstrated that, in addition to social buffering via the mother or mate of an individual [9,10], buffering can be induced by other conspecifics in a variety of non-human species, including laboratory rats [4,11,12].

We have previously investigated social buffering induced by a conspecific other than the mother or mate of an individual using fear conditioning. When a fear-conditioned subject rat is re-exposed to an auditory or contextual conditioned stimulus (CS) alone, conditioned fear responses including increased freezing and hypothalamic-pituitary-adrenal axis activity are observed. However, the presence of an unfamiliar rat (associate) has been found to block these responses, suggesting that social buffering can ameliorate conditioned fear responses [11,13,14]. Subsequent analyses revealed that the addition of a double wire-mesh partition that separated the subject and associate by 5 cm had no effect on this social buffering [15,16]. Social buffering has been observed both between males and between females, indicating that it is a biologically important phenomenon in all rats [17]. Furthermore, we observed social buffering primarily between rats derived from the same colony [18] and found that it enhanced extinction of conditioned fear responses [19]. As a result of our investigations regarding the neural mechanisms of social buffering, we have delineated a circuit underlying this phenomenon. Specifically, a volatile olfactory signal detected at the main olfactory epithelium [16,20,21] activates the posterior complex of the anterior olfactory nucleus [21,22], which in turn suppresses the activation of the lateral amygdala in response to the CS [14,20,21,23].

To the best of our knowledge, previous investigations of social buffering used a single stressor, i.e., the stress level of the subjects was not manipulated. Therefore, the relationship between the stress level of the subjects and the benefit of social buffering has not been analyzed systematically. One possibility is that the benefit of social buffering is reduced because the high stress status of the subjects decreases the intensity of social buffering. In literature, substantial social buffering has been reported in subjects exposed to severe or even lethal stressors. For example, in rats, the odor of a predator (cat) is known to be a sever stressor [24]. When rats were exposed to cat fur, the presence of three conspecifics increased grooming, locomotor activity, and the number of contacts with the cat fur stimulus, and decreased Fos expression in the nuclei related to threat response [3]. In humans, assessing the benefit of social buffering on initial responses to severe stressors is accompanied by ethical challenges. However, retrospective studies have demonstrated the benefit of social support in individuals undergoing stressful life events. For example, people who received social support during stressful life events had a lower mortality rate [8]. In addition, patients with cancer [25], those undergoing dialysis [26], and individuals with massive burn injuries [27] had a lower mortality rate when they received higher levels of social support. Given that social buffering can also be evaluated as the enhancement of recovery from the adverse effects of stress [6,28] and that social buffering is a component of the benefits of social support [7,8], social buffering appears to take place in humans exposed to severe stressors. Based on these findings, we hypothesize that the intensity of social buffering will be similar regardless of the stress level of the subject.

High stress subjects show residual stress responses after receiving social buffering. Therefore, another possibility is that the benefit of social buffering is impaired because the high stress subjects show responses that are resistant to social buffering in addition to buffering-sensitive responses. To test this possibility, stronger social buffering must be presented to subjects. One possible method for accomplishing this is to increase the number of associates. Although this has not previously been assessed in rats or other rodents, a study using squirrel monkeys demonstrated that elevated cortisol levels in fear-conditioned subjects in response to a visual CS were slightly reduced in the presence of one associate and returned to pre-conditioning levels when five associates were present [29]. Based on this finding, we hypothesize that residual stress responses in high stress subject rats will decrease as the number of associates increases.

We conducted a series of experiments using rats to examine our hypotheses. In Experiment 1, we compared social buffering induced by one associate among subjects in low, middle, and high stress groups. We used a fear-conditioning paradigm to manipulate the stress status of the subject. Given that a higher foot shock intensity during the conditioning procedure is known to elicit a higher stress status in the fear-conditioned animal during CS re-exposure [[30], [31], [32]], we fear-conditioned the subjects to the CS with 0.15-mA, 0.45-mA, or 0.70-mA foot shocks. On the following day, these subjects were re-exposed to the CS either alone or with a non-conditioned associate. We assessed the efficacy of social buffering by measuring the behavioral responses of the subjects. We predicted that the presence of an associate would reduce behavioral responses in a similar manner among subjects with different stress levels. In Experiment 2, we compared social buffering induced by one vs. three associates using the subjects in the high stress group. The subjects were fear-conditioned to the CS with 0.70-mA foot shocks. On the following day, these subjects were re-exposed to the CS alone, with one non-conditioned associate, or with three non-conditioned associates. We predicted that three associates would lead to a greater reduction in behavioral responses compared with one associate.

Section snippets

Material and methods

All experiments were approved by the Animal Care and Use Committee of the Faculty of Agriculture at The University of Tokyo, according to guidelines adapted from the Consensus Recommendations on Effective Institutional Animal Care and Use Committees by the Scientists Center for Animal Welfare. A male experimenter (K.K.) cared for all the animals and conducted all the experiments.

Results

Data are expressed as means ± standard error of the means (SEM). The significance level was set at P < .05 for all statistical tests.

Discussion

In the present study, we assessed the relationship between the stress status of the subject and the benefit of social buffering. In Experiment 1, we assessed the hypothesis that the intensity of social buffering would be similar among subjects with different stress levels. The behavioral responses observed in the subjects tested in the Alone situation indicated that our procedure successfully produced different stress levels in the subjects. We observed fewer behavioral responses to the CS in

Conclusions

In Experiment 1, we found that the degree of social buffering was similar among the different stress status groups. In Experiment 2, we found that residual stress responses were further ameliorated when the subjects were exposed to a stronger buffering effect. Based on these findings, we suggest that the benefits of social buffering are maintained regardless of the stress level of the subject rat and enhanced by more conspecifics.

Declarations of interest

None.

Acknowledgments

This study was supported by JSPS KAKENHI Grant Numbers 15H05635 and 15H05782.

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