Effects of Chronic Empathic and Reversed Empathic Stress on Anxiety-like Behaviors in Male Rats

Document Type : Original Article(s)

Authors

1 MSc Student, Department of Physiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

2 PhD, Department of Physiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

Abstract

Background: Empathy is critical for social interactions. Nevertheless, the sharing of excessive negative emotions may affect the behaviors of the observer and demonstrator in social equality and inequality conditions. The present study investigated the effects of chronic empathic and reversed empathic stress on anxiety-like behaviors and their correlation with serum corticosterone levels in male rats.
Methods: Forty-eight male Wistar rats were divided into six groups: Control, Pseudo-Observer, Pseudo-Demonstrator, Observer, Demonstrator, and Co-Demonstrator. Various types of stress included dyadic stress in social inequality conditions, such as empathic and reversed-empathic (restrained) stress, dyadic stress in social equality (receiving common stress), and single stress (restrained and unrestrained) as sham stress groups. All of these stressors were induced for 2h/day for 21 days. The time spent in the open arms and the number of entries in the open arms were measured during the elevated plus maze test to assess anxiety-like behavior. The correlations between serum corticosterone levels and OAT% were evaluated for all experimental groups.
Findings: The percent of total time spent in the open arms and the number of open arm entries were significantly decreased in all stressed groups. Moreover, there was a significant negative correlation between serum corticosterone levels and the percent of total time spent in the open arms in all experimental groups, except the control and pseudo-observer groups.
Conclusion: According to the present findings, chronic empathic stress (observing others' psychological stress or distress) could induce anxiety in the observers. In addition, the reversed empathic stress (receiving restraint stress in the presence of a familiar cagemate in social inequality condition) can be unexpectedly effective in the induction of anxiety. It seems that the gradual changes in serum corticosterone levels play an essential role in the development of anxiety-like behaviors.

Highlights

Maryam Radahmadi: Google Scholar, PubMed

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References

  1. Dimitroff SJ, Kardan O, Necka EA, Decety J, Berman MG, Norman GJ. Physiological dynamics of stress contagion. Sci Rep 2017; 7(1): 6168.
  2. Riess H. The science of empathy. J Patient Exp 2017; 4(2): 74-7.
  3. Chen J. Empathy for distress in humans and rodents. Neurosci Bull 2018; 34(1): 216-36.
  4. Klimecki OM, Leiberg S, Ricard M, Singer T. Differential pattern of functional brain plasticity after compassion and empathy training. Soc Cogn Affect Neurosci 2014; 9(6): 873-9.
  5. White CN, Buchanan TW. Empathy for the stressed. Adapt Human Behav Physiol 2016; 2(4): 311-24.
  6. Watanabe S. Empathy and reversed empathy of stress in mice. PloS One 2011; 6(8): e23357.
  7. Blons E, Arsac LM, Grivel E, Lespinet-Najib V, Deschodt-Arsac V. Physiological resonance in empathic stress: Insights from nonlinear dynamics of heart rate variability. Int J Environ Res Public Health 2021; 18(4): 2081.
  8. Lezak KR, Missig G, Carlezon Jr WA. Behavioral methods to study anxiety in rodents. Dialogues Clin Neurosci 2017; 19(2): 181-91.
  9. Davis MT, Holmes SE, Pietrzak RH, Esterlis I. Neurobiology of chronic stress-related psychiatric disorders: evidence from molecular imaging studies. Chronic Stress 2017; 1: 2470547017710916.
  10. Adams TG, Kelmendi B, Brake CA, Gruner P, Badour CL, Pittenger C. The role of stress in the pathogenesis and maintenance of obsessive-compulsive disorder. Chronic Stress (Thousand Oaks) 2018; 2: 2470547018758043.
  11. Watanabe S, Hofman MA, Shimizu T. Evolution of the Brain, Cognition, and Emotion in Vertebrates. Princeton, NJ: Springer Publication; 2017. p. 273-99.
  12. Kvarta MD, Bradbrook KE, Dantrassy HM, Bailey AM, Thompson SM. Corticosterone mediates the synaptic and behavioral effects of chronic stress at rat hippocampal temporoammonic synapses. J Neurophysiol 2015; 114(3): 1713-24.
  13. Gonzalez-Liencres C, Juckel G, Tas C, Friebe A, Brüne M. Emotional contagion in mice: the role of familiarity. Behav Brain Res 2014; 263: 16-21.
  14. Bartal IB-A, Decety J, Mason P. Empathy and pro-social behavior in rats. Science 2011; 334(6061): 1427-30.
  15. Atrooz F, Alkadhi KA, Salim S. Understanding stress: Insights from rodent models. Curr Res Neurobiol 2021; 2: 100013.
  16. Trofimiuk E, Walesiuk A, Braszko JJ. St John's wort
    (Hypericum perforatum) diminishes cognitive impairment caused by the chronic restraint stress in rats. Pharmacol Res 2005; 51(3): 239-46.
  17. Bagheri Y, Fathi E, Maghoul A, Moshtagh S, Mokhtari K, Abdollahpour A, et al. Effects of Achillea tenuifolia Lam. hydro-alcoholic extract on anxiety-like behavior and reproductive parameters in rat model of chronic restraint stress. Hum Exp Toxicol 2021; 40(11): 1852-66.
  18. de Oliveira PC, Zaniboni CR, Carmona IM, Fonseca AR, Canto-de-Souza A. Preliminary behavioral assessment of cagemates living with conspecifics submitted to chronic restraint stress in mice. Neurosci Lett 2017; 657: 204-10.
  19. Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2007; 2(2): 322-8.
  20. Hafez MH, Gad SB. Zinc oxide nanoparticles effect on oxidative status, brain activity, anxiety-like behavior and memory in adult and aged male rats. Pak Vet J 2018; 38(3): 311.
  21. Zarrindast MR, Khalifeh S, Rezayof A, Rostami P, Sereshki AA, Zahmatkesh M. Involvement of rat dopaminergic system of nucleus accumbens in nicotine-induced anxiogenic-like behaviors. Brain Res 2012; 1460: 25-32.
  22. Han Y, Dong J, Xu C, Rao R, Shu S, Li G, et al. Application of 9.4 T MRI in wilson disease model TX mice with quantitative susceptibility mapping to assess copper distribution. Front Behav Neurosci 2020: 14: 59.
  23. Mohammadi F, Ahmadi-Zeidabadi M, Nazeri M, Ghasemi A, Shabani M. Nitric oxide modulates cognitive, nociceptive and motor functions in a rat model of empathy. Int J Neurosci 2020; 130(9): 865-74.
  24. Buchanan TW, Bagley SL, Stansfield RB, Preston SD. The empathic, physiological resonance of stress. Soc Neurosci 2012; 7(2): 191-201.
  25. Rosenkranz JA, Venheim ER, Padival M. Chronic stress causes amygdala hyperexcitability in rodents. Biol Psychiatry 2010; 67(12): 1128-36.
  26. Felix-Ortiz AC, Beyeler A, Seo C, Leppla CA, Wildes CP, Tye KM. BLA to vHPC inputs modulate anxiety-related behaviors. Neuron 2013; 79(4): 658-64.
  27. Watanabe S. Social factors modulate restraint stress induced hyperthermia in mice. Brain Res 2015; 1624: 134-9.
  28. Acero-Castillo MC, Ardila-Figueroa MC, Botelho de Oliveira S. Anhedonic type behavior and anxiety profile of Wistar-UIS rats subjected to chronic social isolation. Front Behav Neurosci 2021; 15: 663761.
  29. Gądek-Michalska A, Bugajski A, Tadeusz J, Rachwalska P, Bugajski J. Chronic social isolation in adaptation of HPA axis to heterotypic stress. Pharmacol Rep 2017; 69(6): 1213-23.
  30. Nahvi RJ, Nwokafor C, Serova LI, Sabban EL. Single prolonged stress as a prospective model for posttraumatic stress disorder in females. Front Behav Neurosci 2019; 13: 17.
  31. Tejada J, Oliveira R, Salum C, Morato S, Roque A. A model for the rat exploratory behavior in the elevated plus-maze. BMC Neurosci 2007; 8(Suppl 2): P37.
  32. Mällo T, Alttoa A, Kõiv K, Tõnissaar M, Eller M, Harro J. Rats with persistently low or high exploratory activity: behaviour in tests of anxiety and depression, and extracellular levels of dopamine. Behav Brain Res 2007; 177(2): 269-81.
  33. Tucker LB, McCabe JT. Behavior of male and female C57BL/6J mice is more consistent with repeated trials in the elevated zero maze than in the elevated plus maze. Front Behav Neurosci 2017; 11: 13.
  34. Mazaheri M, Radahmadi M, Sharifi MR. Effects of chronic social equality and inequality conditions on passive avoidance memory and PTSD-like behaviors in rats under chronic empathic stress. Int J Neurosci 2024; 1-12.
  35. Török B, Sipos E, Pivac N, Zelena D. Modelling posttraumatic stress disorders in animals. Prog Neuropsychopharmacol Biol Psychiatry 2019: 90: 117-33.
  36. Steimer T. The biology of fear-and anxiety-related behaviors. Dialogues Clin Neurosci 2002; 4(3): 231-49.
Journal of Isfahan Medical School
Volume 42, Issue 758
2nd Week, May
May and June 2024
Pages 124-131

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History

  • Receive Date: 01 May 2024
  • Accept Date: 10 June 2024

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