Reducing social stress elicits emotional contagion of pain in mouse and human strangers

Current Biology

Volumn 25, Issue 3, 2015, Pages 326-332

  Martin, Loren J ^a   Hathaway, Georgia ^a   Isbester, Kelsey ^a   Mirali, Sara ^a   Acland, Erinn L ^a   Niederstrasser, Nils ^a   Slepian, Peter M ^a   Trost, Zina ^a,b   Bartz, Jennifer A ^a   Sapolsky, Robert M ^c   Sternberg, Wendy F ^d   Levitin, Daniel J ^a   Mogil, Jeffrey S ^a,e  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF NORTH TEXAS   (United States)

^c STANFORD UNIVERSITY   (United States)

^d HAVERFORD COLLEGE   (United States)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MUS;

METYRAPONE;

ANALYSIS OF VARIANCE; ANIMAL; DRUG EFFECTS; EMOTION; EMPATHY; HUMAN; MALE; MENTAL STRESS; MOUSE; NOCICEPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; SOCIAL BEHAVIOR;

ANALYSIS OF VARIANCE; ANIMALS; EMOTIONS; EMPATHY; HUMANS; MALE; METYRAPONE; MICE; PAIN PERCEPTION; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84922837748     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.11.028     Document Type: Article

References (46)

1. L. Goubert, K.D. Craig, T. Vervoort, S. Morley, M.J.L. Sullivan, A.C. de C Williams, A. Cano, and G. Crombez Facing others in pain: the effects of empathy Pain 118 2005 285 288
2. D.J. Langford, S.E. Crager, Z. Shehzad, S.B. Smith, S.G. Sotocinal, J.S. Levenstadt, M.L. Chanda, D.J. Levitin, and J.S. Mogil Social modulation of pain as evidence for empathy in mice Science 312 2006 1967 1970
3. D.J. Langford, A.H. Tuttle, C. Briscoe, C. Harvey-Lewis, I. Baran, P. Gleeson, D.B. Fischer, M. Buonora, W.F. Sternberg, and J.S. Mogil Varying perceived social threat modulates pain behavior in male mice J. Pain 12 2011 125 132
4. J.S. Mogil, W.F. Sternberg, H. Balian, J.C. Liebeskind, and B. Sadowski Opioid and nonopioid swim stress-induced analgesia: a parametric analysis in mice Physiol. Behav. 59 1996 123 132
5. T. Romero, A. Konno, and T. Hasegawa Familiarity bias and physiological responses in contagious yawning by dogs support link to empathy PLoS ONE 8 2013 e71365
6. M.L. Miller, A.C. Gallup, A.R. Vogel, S.M. Vicario, and A.B. Clark Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): an observational study of yawning and stretching Behav. Processes 89 2012 264 270
7. 2+ channels in ACC Nat. Neurosci. 13 2010 482 488
8. E. Knapska, M. Mikosz, T. Werka, and S. Maren Social modulation of learning in rats Learn. Mem. 17 2010 35 42
9. Q. Chen, J.B. Panksepp, and G.P. Lahvis Empathy is moderated by genetic background in mice PLoS ONE 4 2009 e4387
10. P. Atsak, M. Orre, P. Bakker, L. Cerliani, B. Roozendaal, V. Gazzola, M. Moita, and C. Keysers Experience modulates vicarious freezing in rats: a model for empathy PLoS ONE 6 2011 e21855
11. D.J. Langford, A.H. Tuttle, K. Brown, S. Deschenes, D.B. Fischer, A. Mutso, K.C. Root, S.G. Sotocinal, M.A. Stern, J.S. Mogil, and W.F. Sternberg Social approach to pain in laboratory mice Soc. Neurosci. 5 2010 163 170
12. I. Ben-Ami Bartal, J. Decety, and P. Mason Empathy and pro-social behavior in rats Science 334 2011 1427 1430
13. J. Panksepp, and J.B. Panksepp Toward a cross-species understanding of empathy Trends Neurosci. 36 2013 489 496
14. J.B. Panksepp, and G.P. Lahvis Rodent empathy and affective neuroscience Neurosci. Biobehav. Rev. 35 2011 1864 1875
15. L.J. Martin, A.H. Tuttle, and J.S. Mogil The interaction between pain and social behavior in humans and rodents Curr. Top. Behav. Neurosci. 20 2014 233 250
16. T. Kikusui, J.T. Winslow, and Y. Mori Social buffering: relief from stress and anxiety Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 2006 2215 2228
17. J.L. Brown, D. Sheffield, M.R. Leary, and M.E. Robinson Social support and experimental pain Psychosom. Med. 65 2003 276 283
18. A.E. López-Martínez, R. Esteve-Zarazaga, and C. Ramírez-Maestre Perceived social support and coping responses are independent variables explaining pain adjustment among chronic pain patients J. Pain 9 2008 373 379
19. C. Krahé, A. Springer, J.A. Weinman, and A. Fotopoulou The social modulation of pain: others as predictive signals of salience - a systematic review Front. Hum. Neurosci. 7 2013 386
20. H. Flor, R.D. Kerns, and D.C. Turk The role of spouse reinforcement, perceived pain, and activity levels of chronic pain patients J. Psychosom. Res. 31 1987 251 259
21. C.T. Chambers, K.D. Craig, and S.M. Bennett The impact of maternal behavior on children's pain experiences: an experimental analysis J. Pediatr. Psychol. 27 2002 293 301
22. M.L. Loggia, J.S. Mogil, and M.C. Bushnell Empathy hurts: compassion for another increases both sensory and affective components of pain perception Pain 136 2008 168 176
23. M. Botvinick, A.P. Jha, L.M. Bylsma, S.A. Fabian, P.E. Solomon, and K.M. Prkachin Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain Neuroimage 25 2005 312 319
24. P.L. Jackson, A.N. Meltzoff, and J. Decety How do we perceive the pain of others? A window into the neural processes involved in empathy Neuroimage 24 2005 771 779
25. F. Godinho, M. Magnin, M. Frot, C. Perchet, and L. Garcia-Larrea Emotional modulation of pain: is it the sensation or what we recall? J. Neurosci. 26 2006 11454 11461
26. T. Singer, B. Seymour, J. O'Doherty, H. Kaube, R.J. Dolan, and C.D. Frith Empathy for pain involves the affective but not sensory components of pain Science 303 2004 1157 1162
27. H. Meffert, V. Gazzola, J.A. den Boer, A.A. Bartels, and C. Keysers Reduced spontaneous but relatively normal deliberate vicarious representations in psychopathy Brain 136 2013 2550 2562
28. C. Lamm, J. Decety, and T. Singer Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain Neuroimage 54 2011 2492 2502
29. B.S. McEwen, L. Eiland, R.G. Hunter, and M.M. Miller Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress Neuropharmacology 62 2012 3 12
30. M. Joëls, H. Karst, R. DeRijk, and E.R. de Kloet The coming out of the brain mineralocorticoid receptor Trends Neurosci. 31 2008 1 7
31. H. Karst, S. Berger, M. Turiault, F. Tronche, G. Schütz, and M. Joëls Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone Proc. Natl. Acad. Sci. USA 102 2005 19204 19207
32. R. Dorey, C. Piérard, S. Shinkaruk, C. Tronche, F. Chauveau, M. Baudonnat, and D. Béracochéa Membrane mineralocorticoid but not glucocorticoid receptors of the dorsal hippocampus mediate the rapid effects of corticosterone on memory retrieval Neuropsychopharmacology 36 2011 2639 2649
33. M.R. Kruk, J. Haller, W. Meelis, and E.R. de Kloet Mineralocorticoid receptor blockade during a rat's first violent encounter inhibits its subsequent propensity for violence Behav. Neurosci. 127 2013 505 514
34. S.M. Rodrigues, L.R. Saslow, N. Garcia, O.P. John, and D. Keltner Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans Proc. Natl. Acad. Sci. USA 106 2009 21437 21441
35. I.D. Neumann Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo-pituitary-adrenal axis Prog. Brain Res. 139 2002 147 162
36. G. Domes, M. Heinrichs, A. Michel, C. Berger, and S.C. Herpertz Oxytocin improves "mind-reading" in humans Biol. Psychiatry 61 2007 731 733
37. R. Hurlemann, A. Patin, O.A. Onur, M.X. Cohen, T. Baumgartner, S. Metzler, I. Dziobek, J. Gallinat, M. Wagner, W. Maier, and K.M. Kendrick Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans J. Neurosci. 30 2010 4999 5007
38. J.A. Bartz, J. Zaki, N. Bolger, E. Hollander, N.N. Ludwig, A. Kolevzon, and K.N. Ochsner Oxytocin selectively improves empathic accuracy Psychol. Sci. 21 2010 1426 1428
39. S.D. Preston, and F.B.M. de Waal Empathy: its ultimate and proximate bases Behav. Brain Sci. 25 2002 1 20 discussion 20-71
40. C. Gonzalez-Liencres, G. Juckel, C. Tas, A. Friebe, and M. Brüne Emotional contagion in mice: the role of familiarity Behav. Brain Res. 263 2014 16 21
41. L. Beckes, J.A. Coan, and K. Hasselmo Familiarity promotes the blurring of self and other in the neural representation of threat Soc. Cogn. Affect. Neurosci. 8 2013 670 677
42. T.W. Buchanan, S.L. Bagley, R.B. Stansfield, and S.D. Preston The empathic, physiological resonance of stress Soc. Neurosci. 7 2012 191 201
43. M. Ono, M. Fujita, and S. Yamada Physiological and psychological responses induced by expressing empathy with others Jpn. J. Nurs. Sci. 9 2012 56 62
44. G. Buruck, J. Wendsche, M. Melzer, A. Strobel, and D. Dörfel Acute psychosocial stress and emotion regulation skills modulate empathic reactions to pain in others Front. Psychol. 5 2014 517
45. B. von Dawans, U. Fischbacher, C. Kirschbaum, E. Fehr, and M. Heinrichs The social dimension of stress reactivity: acute stress increases prosocial behavior in humans Psychol. Sci. 23 2012 651 660
46. T.W. Buchanan, and S.D. Preston Stress leads to prosocial action in immediate need situations Front. Behav. Neurosci. 8 2014 5