Elsevier

Psychoneuroendocrinology

Volume 45, July 2014, Pages 192-201
Psychoneuroendocrinology

Cortisol increase in empathic stress is modulated by emotional closeness and observation modality

https://doi.org/10.1016/j.psyneuen.2014.04.005Get rights and content

Summary

Stress disorders are among the most commonly occurring of all mental disorders. In this context, the question arises whether the stress inevitably unfolding around us has the potential to “contaminate” and compromise us. In the current multi-center study, we investigate the existence of such empathic stress (defined as a full-blown physiological stress response that arises solely by observing a target undergo a stressful situation), and whether empathic stress permeates to the core of the stress system, the hypothalamic-pituitary-adrenal (HPA) axis. Additionally, we investigate whether empathic stress responses may be modulated by the familiarity between observer and target (partners vs. strangers), the modality of observation (real-life vs. virtual) and observer sex (female vs. male). Participants were tested in dyads, paired with a loved one or a stranger of the opposite sex. While the target of the dyad (n = 151) was exposed to a psychosocial stressor, the observer (n = 211) watched through a one-way mirror or via live video transmission. Overall, 26% of the observers displayed physiologically significant cortisol increases. This empathic stress was more pronounced in intimate observer-target dyads (40%) and during the real-life representation of the stressor (30%). Empathic stress was further modulated by interindividual differences in empathy measures. Despite the higher prevalence of empathic stress in the partner and real-life observation conditions, significant cortisol responses also emerged in strangers (10%) and the virtual observation modality (24%). The occurrence of empathic stress down to the level of HPA-axis activation, in some cases even in total strangers and when only virtually witnessing another's distress, may have important implications for the development of stress-related diseases.

Introduction

Stress is a major health threat in today's fast-paced society. Stress disorders are among the most commonly occurring of all mental disorders (WHO International Consortium in Psychiatric Epidemiology, 2000). Whether or not we directly suffer from stress, the question arises how much the stress inevitably unfolding around us has the potential to negatively affect us. While phenomena like “stress contagion” or “empathic stress” receive major media coverage, solid empirical evidence for such empathic stress permeating to the endocrine level is lacking. The aim of this project was to examine whether empathic stress indeed exists on different levels of the physiological stress system.

No matter how strongly we perceive ourselves as autonomous entities emphasizing our individuality, our affective states are linked with those of our fellow human beings. The theory of Einfühlung (“feeling into”) by the philosopher Lipps (1897) marked the first scientific approach to explain how humans understand the affective states of others. Following this early philosophical perspective, social psychologists (Stotland, 1969, Batson, 1991, Eisenberg, 2000, Hoffman, 2000, Batson, 2009, Hatfield et al., 2009) and neuroscientists have stressed the notion of empathy (Preston and de Waal, 2002, de Vignemont and Singer, 2006, Decety, 2011, Singer, 2012), showing that affective resonance permeates to the autonomic nervous system (Levenson and Ruef, 1992, Harrison et al., 2006, Hein et al., 2011) and the brain (Singer and Lamm, 2009, Keysers et al., 2010, Lamm et al., 2011). In the context of the social neurosciences, empathy was defined as the process by which an individual infers the affective state of another by generating an isomorphic state in the self, all the while realizing that the source of the affective state lies in the other, not the self (de Vignemont and Singer, 2006, Singer and Lamm, 2009).

Considering the growing interest in empathy research, it is curious that affective sharing on the level of the physiological stress system has virtually been ignored. Few studies addressed the topic: Sethre-Hofstad et al. (2002) examined mother–child dyads while mothers observed their children in a challenging situation, and found attunement of adrenocortical activity between high maternally sensitive mothers and their children. However, neither the mothers nor the children exhibited physiologically significant adrenocortical responses to the challenging situation. Examining facial thermal imprints of mother-child dyads while mothers observed their own and unknown children in a distressing situation, Ebisch et al. (2012) and Manini et al. (2013) found sympathetic attunement but neglected the endocrine stress component. Buchanan et al. (2012) examined participants who had the dual role of inducing stress in others while observing the resulting stress responses. Considering that the task of stress induction may be quite stressful in itself, the authors might have confounded firsthand and empathic stress responses.

To fill this gap, we conducted multiple studies across different laboratories searching for evidence of true empathic stress responses down to the hormonal level. Beyond sympathetic nervous system (SNS) activation as unspecific sign of general arousal, stress experience requires the activation of the hypothalamic-pituitary-adrenal (HPA) axis resulting in cortisol release (Chrousos, 2009, Hellhammer et al., 2009). We accordingly defined empathic stress as an endocrine stress response that arises solely by observing a target undergo a stressful situation, while any simultaneous SNS activation is referred to as empathic arousal. We further differentiated between two components of empathic stress: Vicarious stress is suggested to arise through the projection of an observer's own stress response onto the target, irrespective of the target's response. Stress resonance requires the degree of the observer's stress response to be a function of the degree of the target's stress response. Thus, while the magnitude of a vicarious stress response is independent of the target's stress response, observer's and target's stress responses are correlated in the occurrence of stress resonance. The same differentiation was applied to empathic arousal.

Empathic stress was examined in the following setting: While one participant underwent the Trier Social Stress Test (TSST; Kirschbaum et al., 1993, Kudielka et al., 2007), a psychosocial laboratory stressor, another solely observed the situation. HPA-axis activation was captured by repeated measurements of salivary cortisol in observers and targets. As sympathetic indicators, we assessed the salivary enzyme alpha-amylase (Nater and Rohleder, 2009) and heart rate. As potential modulatory factors of empathic stress we systematically manipulated the familiarity between observer and target (partners vs. strangers), the modality of observation (real-life vs. virtual) and observer sex (female vs. male). Heterosexual partners constituted the intimate and opposite-sex strangers the distant relationship group. In the real-life observation modality, observers watched the TSST through a one-way mirror. In the virtual observation modality, they watched a close-up live video of the target's face. Observers always watched an opposite-sex target (see Fig. 1A and B for an overview).

Our first goal was to find evidence for empathic stress down to the endocrine response level. Further, with regard to the two subcomponents of empathic stress, we expected a positive association between observers’ and targets’ cortisol responses as evidence for stress resonance. A significant portion of empathic stress was additionally expected to be independent of the targets’ cortisol levels, thus providing evidence for vicarious stress. Regarding potential modulatory factors, empathic stress was expected to be higher in intimate (partners) than distant (strangers) observer-target dyads and when observing from the real-life (one-way mirror condition) as compared to the virtual (video transmission) perspective. Given controversial evidence regarding sex differences in empathy (Eisenberg and Lennon, 1983, Baron-Cohen and Wheelwright, 2004, Singer et al., 2006, Rueckert and Naybar, 2008), no a priori hypothesis was formulated. Finally, previous work has shown correlations of subjective empathy measures (questionnaires or affect ratings) with empathy-related brain responses (Lamm et al., 2011). Based on these findings, we expected the magnitude of vicarious stress and stress resonance to be modulated by interindividual differences in trait and state empathy with higher empathy scores facilitating the occurrence of empathic stress.

Section snippets

Participants

This project was a collaboration between two research institutes. At the Max Planck Institute for Human Cognitive and Brain Sciences in Leipzig, 51 opposite-sex couples and 40 male-female stranger dyads participated in the study. At the Technische Universität Dresden, 60 opposite-sex couples and 60 strangers were tested. To simplify the already complex study design, we limited the investigation to opposite-sex dyads. Couples had been in a relationship for at least six months. All participants

Results

The original sample size of 211 observers was reduced to 206 for alpha-amylase and to 163 for heart rate data due to an insufficient quantity of sampled saliva and technical problems with the heart rate registration devices. All 211 observers displayed valid cortisol data. The Supplementary Table shows the distribution of participants per laboratory and experimental conditions.

Discussion

We conducted a large-scale multi-center and -study project testing whether we could find evidence for true empathic stress permeating to the level of endocrine activation. Our results reveal that full-blown stress responses including HPA-axis and SNS activation can indeed be elicited by the mere observation of an individual undergoing psychosocial stress. In total, 54 out of 211 observers (26%) showed a physiologically (not just statistically) significant increase in cortisol levels. This

Role of funding source

The funding for this study was provided by the Department of Social Neuroscience, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, and the Department of Psychology, Technische Universität Dresden, Germany. This work was additionally supported by a grant to T.S. from the European Research Council under the European Community's Seventh Framework Program (FP7/2007-2013)/ERC Grant agreement no. 205557 [EMPATHICBRAIN].

Conflict of interest

All of the authors declare that they have no conflicts of interest.

Acknowledgements

We thank our student assistants for their help with data collection and preprocessing

References (56)

  • L. Sethre-Hofstad et al.

    Attunement of maternal and child adrenocortical response to child challenge

    Psychoneuroendocrinology

    (2002)
  • T. Singer

    The past, present and future of social neuroscience: a European perspective

    Neuroimage

    (2012)
  • S. Baron-Cohen et al.

    The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences

    J. Autism Dev. Disord.

    (2004)
  • C.D. Batson

    The Altruism Question: Toward a Social Psychological Answer

    (1991)
  • C.D. Batson

    These things called empathy

  • C.D. Batson et al.

    Perspective taking: imagining how another feels versus imagining how you would feel

    Pers. Soc. Psychol. Bull.

    (1997)
  • L.S. Benjamin

    Statistical treatment of the law of initial values (LIV) in autonomic research: a review and recommendation

    Psychosom. Med.

    (1963)
  • T.W. Buchanan et al.

    The empathic, physiological resonance of stress

    Soc. Neurosci.

    (2012)
  • M. Carpenter et al.

    Social cognition, joint attention, and communicative competence from 9 to 15 months of age

    Monogr. Soc. Res. Child Dev.

    (1998)
  • G.P. Chrousos

    Stress and disorders of the stress system

    Nat. Rev. Endocrinol.

    (2009)
  • R.B. Cialdini et al.

    Reinterpreting the empathy–altruism relationship: when one into one equals oneness

    J. Pers. Soc. Psychol.

    (1997)
  • M.F. Dallman et al.

    Hypothalamo-pituitary-adrenal axis

  • M.H. Davis

    Measuring individual differences in empathy: evidence for a multidimensional approach

    J. Pers. Soc. Psychol.

    (1983)
  • J. Decety

    The neuroevolution of empathy

    Ann. N. Y. Acad. Sci.

    (2011)
  • S.S. Dickerson et al.

    Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research

    Psychol. Bull.

    (2004)
  • N. Eisenberg

    Emotion, regulation, and moral development

    Annu. Rev. Psychol.

    (2000)
  • N. Eisenberg et al.

    Sex differences in empathy and related capacities

    Psychol. Bull.

    (1983)
  • R. Feldman et al.

    Mother-infant affect synchrony as an antecedent of the emergence of self-control

    Dev. Psychol.

    (1999)
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