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Empathy for Distress in Humans and Rodents

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Many animals, however, certainly sympathise with each other’s distress or danger.

Charles Darwin

Abstract

Empathy is traditionally thought to be a unique ability of humans to feel, understand, and share the emotional state of others. However, the notion has been greatly challenged by the emerging discoveries of empathy for pain or distress in rodents. Because empathy is believed to be fundamental to the formation of prosocial, altruistic, and even moral behaviors in social animals and humans, studies associated with decoding the neural circuits and unraveling the underlying molecular and neural mechanisms of empathy for pain or distress in rodents would be very important and encouraging. In this review, the author set out to outline and update the concept of empathy from the evolutionary point of view, and introduce up-to-date advances in the study of empathy and its neural correlates in both humans and rodents. Finally, the author highlights the perspectives and challenges for the further use of rodent models in the study of empathy for pain or distress.

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References

  1. Martin LJ, Tuttle AH, Mogil JS. The interaction between pain and social behavior in humans and rodents. Curr Top Behav Neurosci 2014, 20: 233–250.

    Article  PubMed  Google Scholar 

  2. Mogil JS. Social modulation of and by pain in humans and rodents. Pain 2015, 156: S35–S41.

    Article  PubMed  Google Scholar 

  3. Williams AC, Craig KD. Updating the definition of pain. Pain 2016, 157: 2420–2423.

    Article  PubMed  Google Scholar 

  4. Merskey H, Bogduk N. Classification of Chronic Pain. Seattle: IASP Press, 1994.

    Google Scholar 

  5. Craig KD. Social communication model of pain. Pain 2015, 156: 1198–1199.

    Article  PubMed  Google Scholar 

  6. Hadjistavropoulos T, Craig KD, Duck S, Cano A, Goubert L, Jackson PL, Mogil JS, et al. Abiopsychosocial formulation of pain communication. Psychol Bull 2011, 137: 910–939.

    Article  PubMed  Google Scholar 

  7. Jensen KB, Petrovic P, Kerr CE, Kirsch I, Raicek J, Cheetham A, Spaeth R, et al. Sharing pain and relief: neural correlates of physicians during treatment of patients. Mol Psychiatry 2014, 19: 392–398.

    Article  CAS  PubMed  Google Scholar 

  8. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science 2004, 303: 1157–1162.

    Article  CAS  PubMed  Google Scholar 

  9. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997, 277: 968–971.

    Article  CAS  PubMed  Google Scholar 

  10. Lamm C, Decety J, Singer T. Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 2011, 54: 2492–502.

    Article  PubMed  Google Scholar 

  11. Li Z, Lu YF, Li CL, Wang Y, Sun W, He T, et al. Social interaction with a cagemate in pain facilitates subsequent spinal nociception via activation of the medial prefrontal cortex in rats. Pain 2014, 155: 1253–1261.

    Article  PubMed  Google Scholar 

  12. Ren LY, Lu ZM, Liu MG, Yu YQ, Li Z, Shang GW, et al. Distinct roles of the anterior cingulate cortex in spinal and supraspinal bee venom-induced pain behaviors, Neuroscience 2008, 153: 268–278.

    Article  CAS  PubMed  Google Scholar 

  13. Gong KR, Cao FL, He Y, Gao CY, Wang DD, Li H, et al. Enhanced excitatory and reduced inhibitory synaptic transmission contribute to persistent pain-induced neuronal hyper-responsiveness in anterior cingulate cortex. Neuroscience 2010, 171: 1314–1325.

    Article  CAS  PubMed  Google Scholar 

  14. Lu YF, He Y, Wang Y, Zhang FK, He T, Wang RR, et al. Spatial and temporal plasticity of synaptic organization in anterior cingulate cortex following peripheral inflammatory pain: multi-electrode array recordings in rats. Neurosci Bull 2014, 30: 1–20.

    Article  PubMed  Google Scholar 

  15. Geng KW, He T, Wang RR, Li CL, Luo WJ, Wu FF, et al. Ethanol increases mechanical pain sensitivity in rats via activation of GABAA receptors in medial prefrontal cortex. Neurosci Bull 2016, 32: 433–444.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Liu MG, Chen J. Preclinical research on pain comorbidity with affective disorders and cognitive deficits: challenges and perspectives. Prog Neurobiol 2014, 116: 13–32.

    Article  PubMed  Google Scholar 

  17. de Waal FBM. Putting the altruism back into altruism: The evolution of empathy. Annu Rev Psychol 2008, 59: 279–300.

    Article  PubMed  Google Scholar 

  18. de Waal FBM. The antiquity of empathy. Science 2012, 336:874–876.

    Article  PubMed  CAS  Google Scholar 

  19. de Waal FBM. The Bonobo and the Atheist. In Search for Humanism among the Primates. New York: W.W. Norton & Company, 2013.

  20. Panksepp JB, Lahvis GP. Rodent empathy and affective neuroscience. Neurosci Biobehav Rev 2011, 35: 1864–1875.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Panksepp J, Panksepp JB. Toward a cross-species understanding of empathy. Trend Neurosci 2013, 36: 489–496.

    Article  CAS  PubMed  Google Scholar 

  22. Gonzalez-Liencres C, Shamay-Tsoory SG, Brüne M. Towards a neuroscience of empathy: ontogeny, phylogeny, brain mechanisms, context and psychopathology. Neurosci Biobehav Rev 2013, 37: 1537–1548.

    Article  PubMed  Google Scholar 

  23. Keum S, Shin HS. Rodent models for studying empathy. Neurobiol Learn Mem 2016, 135: 22–26.

    Article  PubMed  Google Scholar 

  24. Sivaselvachandran S, Acland EL, Abdallah S, Martin LJ. Behavioral and mechanistic insight into rodent empathy. Neurosci Biobehav Rev 2016, doi:10.1016/j.neubiorev.2016.06.007.

    PubMed  Google Scholar 

  25. Meyza KZ, Bartal IB, Monfils MH, Panksepp JB, Knapska E. The roots of empathy: Through the lens of rodent models. Neurosci Biobehav Rev 2016, doi:10.1016/j.neubiorev.2016.10.028.

    PubMed  Google Scholar 

  26. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, et al. Social modulation of pain as evidence for empathy in mice. Science 2006, 312: 1967–1970.

    Article  CAS  PubMed  Google Scholar 

  27. Langford DJ, Williams AC. The caring, sharing rat? Pain 2014, 155: 1183–1184.

    Article  PubMed  Google Scholar 

  28. Chen J, Li Z, Lv YF, Li CL, Wang Y, Wang RR, et al. Empathy for pain: A novel bio-psychosocial-behavioral laboratory animal model. Acta Physiol Sin 2015, 67: 561–570. (In Chinese with abstract in English).

    Google Scholar 

  29. Pigman GW. Freud and the history of empathy. Int J Psychoanal 1995, 76 :237–256.

    PubMed  Google Scholar 

  30. Preston SD, de Waal FBM. Empathy: Its ultimate and proximate bases. Behav Brain Sci 2002, 25: 1–72.

    PubMed  Google Scholar 

  31. de Vignemont F, Singer T. The empathic brain: how, when and why? Trend Cogn Sci 2006, 10: 435–441.

    Article  Google Scholar 

  32. Leiberg S, Anders S. The multiple facets of empathy: a survey of theory and evidence. Prog Brain Res 2006, 156: 419–440.

    Article  PubMed  Google Scholar 

  33. Bernhardt BC, Singer T. The neural basis of empathy. Annu Rev Neurosci 2012, 35: 1–23.

    Article  CAS  PubMed  Google Scholar 

  34. Decety J, Norman GJ, Berntson GG, Cacioppo JT. A neurobehavioral evolutionary perspective on the mechanisms underlying empathy. Prog Neurobiol 2012, 98: 38–48.

    Article  PubMed  Google Scholar 

  35. Decety J, Bartal IB, Uzefovsky F, Knafo-Noam A. Empathy as a driver of prosocial behaviour: highly conserved neurobehavioural mechanisms across species. Philos Trans R Soc Lond B Biol Sci 2016, doi:10.1098/rstb.2015.0077.

    PubMed  PubMed Central  Google Scholar 

  36. Ben-Ami Bartal I, Decety J, Mason P. Empathy and pro-social behavior in rats. Science 2011, 334: 1427–1430.

    Article  PubMed  CAS  Google Scholar 

  37. Ben-Ami Bartal I, Rodgers DA, Bernardez Sarria MS, Decety J, Mason P. Pro-social behavior in rats is modulated by social experience. Elife 2014, 3: e01385.

  38. Márquez C, Rennie SM, Costa DF, Moita MA. Prosocial choice in rats depends on food-seeking behavior displayed by recipients. Curr Biol 2015, 25: 1736–1745.

    Article  PubMed  CAS  Google Scholar 

  39. Hernandez-Lallement J, van Wingerden M, Marx C, Srejic M, Kalenscher T. Rats prefer mutual rewards in a prosocial choice task. Front in Neurosci 2015, 8: 443.

    Article  Google Scholar 

  40. Zaki J, Ochsner KN. The neuroscience of empathy: progress, pitfalls and promise. Nat Neurosci 2012, 15: 675–680.

    Article  CAS  PubMed  Google Scholar 

  41. Shamay-Tsoory SG, Aharon-Peretz J, Perry D. Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 2009, 32: 617–627.

    Article  Google Scholar 

  42. Darwin C. The descent of man. 2nd edition. London: Penguin Group, 1879.

    Google Scholar 

  43. Darwin C. The expression of the emotions in man and animals. 2nd edition. London: Penguin Group, 1890.

    Google Scholar 

  44. Langford DL, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, et al. Coding of facial expressions of pain in the laboratory mouse. Nat Methods 2010, 7: 447–449.

    Article  CAS  PubMed  Google Scholar 

  45. Condé F, Audinat E, Maire-Lepoivre E, Crépel F. Afferent connections of the medial frontal cortex of the rat. A study using retrograde transport of fluorescent dyes. I. Thalamic afferents. Brain Res Bull 1990, 24: 341–354.

    Article  PubMed  Google Scholar 

  46. Condé F, Maire-Lepoivre E, Audinat E, Crépel F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J Comp Neurol 1995, 352: 567–593.

    Article  PubMed  Google Scholar 

  47. Hoover WB, Vertes RP. Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 2007, 212: 149–179.

    Article  PubMed  Google Scholar 

  48. Christoff K, Irving ZC, Fox KC, Spreng RN, Andrews-Hanna JR. Mind-wandering as spontaneous thought: a dynamic framework. Nat Rev Neurosci 2016, 17: 718–731.

    Article  CAS  PubMed  Google Scholar 

  49. Taylor SF, Liberzon I. Neural correlates of emotion regulation in psychopathology. Trends Cogn Sci 2007, 11: 413–418.

    Article  PubMed  Google Scholar 

  50. Ranganath C, Ritchey M. Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 2012, 13: 713–726.

    Article  CAS  PubMed  Google Scholar 

  51. Tang YY, Hölzel BK, Posner MI. The neuroscience of mindfulness meditation. Nat Rev Neurosci 2015, 16: 213–225.

    Article  CAS  PubMed  Google Scholar 

  52. Liu D, Gu X, Zhu J, Zhang X, Han Z, Yan W, et al. Medial prefrontal activity during delay period contributes to learning of a working memory task. Science 2014, 346: 458–463.

    Article  CAS  PubMed  Google Scholar 

  53. Xu W, Südhof TC. A neural circuit for memory specificity and generalization. Science 2013, 339: 1290–1295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bushnell MC, Ceko M, Low LA. Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 2013, 14: 502–511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Gilmartin MR, Balderston NL, Helmstetter FJ. Prefrontal cortical regulation of fear learning. Trends Neurosci 2014, 37: 455–464.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Tovote P, Fadok JP, Lüthi A. Neuronal circuits for fear and anxiety. Nat Rev Neurosci 2015, 16: 317–331. (Erratum in: Nat Rev Neurosci 2015, 16:439).

  57. Bennett MR. The prefrontal-limbic network in depression: A core pathology of synapse regression. Prog Neurobiol 2011a, 93: 457–467.

    Article  CAS  PubMed  Google Scholar 

  58. Bennett MR. The prefrontal-limbic network in depression: Modulation by hypothalamus, basal ganglia and midbrain. Prog Neurobiol 2011b, 93: 468–487.

    Article  CAS  PubMed  Google Scholar 

  59. Rizzolatti G, Sinigaglia C. The mirror mechanism: a basic principle of brain function. Nat Rev Neurosci 2016, 17: 757–765.

    Article  CAS  PubMed  Google Scholar 

  60. Xu X, Zuo X, Wang X, Han S. Do you feel my pain? Racial group membership modulates empathic neural responses. J Neurosci 2009, 29: 8525–8529.

    Article  CAS  PubMed  Google Scholar 

  61. Sheng F, Liu Y, Zhou B, Zhou W, Han S. Oxytocin modulates the racial bias in neural responses to others’ suffering. Biol Psychol 2013, 92: 380–386.

    Article  PubMed  Google Scholar 

  62. Insel TR, Young LJ. Neuropeptides and the evolution of social behavior. Cur Opin Neurobiol 2000, 10: 784–789.

    Article  CAS  Google Scholar 

  63. Insel TR, Young LJ. The neurobiology of attachment. Nat Rev Neurosci 2001, 2: 129–136.

    Article  CAS  PubMed  Google Scholar 

  64. Winslow JT, Insel TR. Neuroendocrine basis of social recognition. Cur Opin Neurobiol 2004, 14: 248–253.

    Article  CAS  Google Scholar 

  65. Donaldson ZR, Young LJ. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 2008, 322: 900–904.

    Article  CAS  PubMed  Google Scholar 

  66. Heinrichs M, Domes G. Neuropeptides and social behavior: effects of oxytocin and vasopressin in humans. Prog Brain Res 2008, 170: 337–350.

    Article  CAS  PubMed  Google Scholar 

  67. Lee HJ, Macbeth AH, Pagani JH, Young3rd WS. Oxytocin: The great facilitator of life. Prog Neurobiol 2009, 88: 127–151.

  68. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 2011, 12: 524–538.

    Article  CAS  PubMed  Google Scholar 

  69. Church RM. Emotional reactions of rats to the pain of others. J Comp Physiol Psychol 1959, 52 :132–134.

    Article  CAS  PubMed  Google Scholar 

  70. Rice GE, Gainer P. “Altruism” in the albino rat. J Comp Physiol Psychol 1962, 55: 123–125.

    Article  CAS  PubMed  Google Scholar 

  71. Watanabe S, Ono K. An experimental analysis of “empathic” response: Effects of pain reactions of pigeon upon other pigeon’s operant behavior. Behav Processes 1986, 13: 269–277.

    Article  CAS  PubMed  Google Scholar 

  72. Edgar JL, Lowe JC, Paul ES, Nicol CJ. Avian maternal response to chick distress. Proc Biol Sci 2011, 278: 3129–3134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Edgar JL, Paul ES, Harris L, Penturn S, Nicol CJ. No evidence for emotional empathy in chickens observing familiar adult conspecifics. PLoS One 2012, 7: e31542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Nowbahari E, Scohier A, Durand JL, Hollis KL. Ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped relatives. PLoS One 2009, 4: e6573.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. de Waal FBM. Do animals feel empathy? Scientific American Mind 2007, 18(6): 28–35.

    Article  Google Scholar 

  76. Miller G. Animal behavior. Signs of empathy seen in mice. Science 2006, 312: 1860–1861.

    Article  CAS  PubMed  Google Scholar 

  77. Knapska E, Nikolaev E, Boguszewski P, Walasek G, Blaszczyk J, Kaczmarek L, et al. Between-subject transfer of emotional information evokes specific pattern of amygdala activation. Proc Natl Acad Sci U S A 2006, 103: 3858–3862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Knapska E, Mikosz M, Werka T, Maren S. Social modulation of learning in rats. Learn Mem 2010, 17: 35–42.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Chen Q, Panksepp JB, Lahvis GP. Empathy is moderated by genetic background in mice. PLoS One 2009, 4: e4387.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Jeon D, Kim S, Chetana M, Jo D, Ruley HE, Lin SY, et al. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat Neurosci 2010, 13: 482–488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Keum S, Park J, Kim A, Park J, Kim KK, Jeong J, et al. Variability in empathic fear response among 11 inbred strains of mice. Genes Brain Behav 2016, 15: 231–242.

    Article  CAS  PubMed  Google Scholar 

  82. Mikosz M, Nowak A, Werka T, Knapska E. Sex differences in social modulation of learning in rats. Sci Rep 2015, 5: 18114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Bruchey AK, Jones CE, Monfils MH. Fear conditioning by-proxy: social transmission of fear during memory retrieval. Behav Brain Res 2010, 214: 80–84.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Jones CE, Riha PD, Gore AC, Monfils MH. Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats. Anim Cogn 2014, 17: 827–834.

    Article  PubMed  Google Scholar 

  85. Jones CE, Monfils MH. Dominance status predicts social fear transmission in laboratory rats. Anim Cogn 2016, 19: 1051–1069.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Kim EJ, Kim ES, Covey E, Kim JJ. Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PLoS One 2010, 5: e15077.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Atsak P, Orre M, Bakker P, Cerliani L, Roozendaal B, Gazzola V, et al. Experience modulates vicarious freezing in rats: a model for empathy. PLoS One 2011, 6: e21855.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Yusufishaq S, Rosenkranz JA. Post-weaning social isolation impairs observational fear conditioning. Behav Brain Res 2013, 242: 142–149.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Akyazi I, Eraslan E. Transmission of stress between cagemates: a study in rats. Physiol Behav 2014, 123: 114–118.

    Article  CAS  PubMed  Google Scholar 

  90. Kiyokawa Y, Honda A, Takeuchi Y, Mori Y. A familiar conspecific is more effective than an unfamiliar conspecific for social buffering of conditioned fear responses in male rats. Behav Brain Res 2014, 267: 189–193.

    Article  PubMed  Google Scholar 

  91. Nowak A, Werka T, Knapska E. Social modulation in extinction of aversive memories. Behav Brain Res 2013, 238: 200–205.

    Article  PubMed  Google Scholar 

  92. Watanabe S. Distress of mice induces approach behavior but has an aversive property for conspecifics. Behav Processes 2012, 90: 167–173.

    Article  PubMed  Google Scholar 

  93. 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.

    Article  PubMed  Google Scholar 

  94. Langford DJ, Tuttle AH, Briscoe C, Harvey-Lewis C, Baran I, Gleeson P, et al. Varying perceived social threat modulates pain behavior in male mice. J Pain 2011, 12: 125–132.

    Article  PubMed  Google Scholar 

  95. Martin LJ, Hathaway G, Isbester K, Mirali S, Acland EL, Niederstrasser N, et al. Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Curr Biol 2015, 25: 326–332.

    Article  CAS  PubMed  Google Scholar 

  96. Langford DJ, Tuttle AH, Brown K, Deschenes S, Fischer DB, Mutso A, et al. Social approach to pain in laboratory mice. Soc Neurosci 2010, 5: 163–170.

    Article  PubMed  Google Scholar 

  97. Yang L, Shi LJ, Yu J, Zhang YQ. Activation of protein kinase A in the amygdala modulates anxiety-like behaviors in social defeat exposed mice. Mol Brain 2016, 9: 3.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Gioiosa L, Chiarotti F, Alleva E, Laviola G. A trouble shared is a trouble halved: social context and status affect pain in mouse dyads. PLoS One 2009, 4: e4143.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Smith ML, Hostetler CM, Heinricher MM, Ryabinin AE. Social transfer of pain in mice. Sci Adv 2016, 2: e1600855.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Baptista-de-Souza D, Nunciato AC, Pereira BC, Fachinni G, Zaniboni CR, Canto-de-Souza A. Mice undergoing neuropathic pain induce anxiogenic-like effects and hypernociception in cagemates. Behav Pharmacol 2015, 26: 664–672.

    Article  CAS  PubMed  Google Scholar 

  101. Yang H, Jung S, Seo J, Khalid A, Yoo JS, Park J, et al. Altered behavior and neural activity in conspecific cagemates co-housed with mouse models of brain disorders. Physiol Behav 2016, 163: 167–176.

    Article  CAS  PubMed  Google Scholar 

  102. Chen J, Lariviere WR. The nociceptive and anti-nociceptive effects of bee venom injection and therapy: a double-edged sword. Prog Neurobiol 2010, 92:151–183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Chen J, Guan SM. Bee venom and Pain. In: Gopalakrishnakone P. (Ed.). Toxinology: Toxins and Drug Discovery. Springer Netherlands, 2015: 1–34. DOI 10.1007/978-94-007-6726-3_1-1.

  104. Kiyokawa Y, Hiroshima S, Takeuchi Y, Mori Y. Social buffering reduces male rats’ behavioral and corticosterone responses to a conditioned stimulus. Horm Behav 2014, 65: 114–118.

    Article  CAS  PubMed  Google Scholar 

  105. Ishii A, Kiyokawa Y, Takeuchi Y, Mori Y. Social buffering ameliorates conditioned fear responses in female rats. Horm Behav 2016, 81: 53–58.

    Article  PubMed  Google Scholar 

  106. Mikami K, Kiyokawa Y, Takeuchi Y, Mori Y. Social buffering enhances extinction of conditioned fear responses in male rats. Physiol Behav 2016, 163: 123–128.

    Article  CAS  PubMed  Google Scholar 

  107. Takahashi Y, Kiyokawa Y, Kodama Y, Arata S, Takeuchi Y, Mori Y. Olfactory signals mediate social buffering of conditioned fear responses in male rats. Behav Brain Res 2013, 240: 46–51.

    Article  PubMed  Google Scholar 

  108. Kiyokawa Y, Wakabayashi Y, Takeuchi Y, Mori Y. The neural pathway underlying social buffering of conditioned fear responses in male rats. Eur J Neurosci 2012, 36: 3429–3437.

    Article  PubMed  Google Scholar 

  109. Fuzzo F, Matsumoto J, Kiyokawa Y, Takeuchi Y, Ono T, Nishijo H. Social buffering suppresses fear-associated activation of the lateral amygdala in male rats: behavioral and neurophysiological evidence. Front Neurosci 2015, 9: 99.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Popper KR, Eccles JC. The Self and Its Brain. An Argument for Interactionism. London: Taylor & Francis Group, 1977.

  111. Danziger N, Faillenot I, Peyron R. Can we share a pain we never felt? Neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 2009, 61: 203–212.

    Article  CAS  PubMed  Google Scholar 

  112. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor cortex. Brain 1996, 119: 593–609.

    Article  PubMed  Google Scholar 

  113. Gallese V, Keysers C, Rizzolatti G. A unifying view of the basis of social cognition. Trends Cogn Sci 2004, 8: 396–403.

    Article  PubMed  Google Scholar 

  114. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. Cortical mechanisms of human imitation. Science 1999, 286: 2526–2528.

    Article  CAS  PubMed  Google Scholar 

  115. Rizzolatti G. Confounding the origin and function of mirror neurons. Behav Brain Sci 2014, 37: 218–219.

    Article  PubMed  Google Scholar 

  116. Rizzolatti G, Fogassi L, Gallese V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2001, 2: 661–670.

    Article  CAS  PubMed  Google Scholar 

  117. Rizzolatti G, Cattaneo L, Fabbri-Destro M, Rozzi S. Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiol Rev 2014, 94: 655–706.

    Article  PubMed  Google Scholar 

  118. Rizzolatti G, Craighero L. The mirror-neuron system. Annu Rev Neurosci 2004, 27: 169–192.

    Article  CAS  PubMed  Google Scholar 

  119. Rizzolatti G, Fabbri–Destro M. The mirror system and its role in social cognition. Curr Opin Neurobiol 2008, 18: 179–184.

    Article  CAS  PubMed  Google Scholar 

  120. Rizzolatti G, Sinigaglia C. The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 2010, 11: 264–274.

    Article  CAS  PubMed  Google Scholar 

  121. De Dreu CK, Kret ME. Oxytocin conditions intergroup relations through upregulated in-Group empathy, cooperation, conformity, and defense. Biol Psychiatry 2016, 79: 165–173.

    Article  PubMed  CAS  Google Scholar 

  122. Beetz A, Uvnäs-Moberg K, Julius H, Kotrschal K. Psychosocial and psychophysiological effects of human-animal interactions: the possible role of oxytocin. Front Psychol 2012, 3: 234.

    PubMed  PubMed Central  Google Scholar 

  123. Marlin BJ, Mitre M, D’amour JA, Chao MV, Froemke RC. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 2015, 520: 499–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Burkett JP, Andari E, Johnson ZV, Curry DC, de Waal FB, Young LJ. Oxytocin-dependent consolation behavior in rodents. Science 2016, 351: 375–378.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, et al. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 2012, 73: 553–566.

    Article  CAS  PubMed  Google Scholar 

  126. Mitchell IJ, Gillespie SM, Abu-Akel A. Similar effects of intranasal oxytocin administration and acute alcohol consumption on socio-cognitions, emotions and behaviour: Implications for the mechanisms of action. Neurosci Biobehav Rev 2015, 55: 98–106.

    Article  CAS  PubMed  Google Scholar 

  127. Smith A. Cognitive empathy and emotional empathy in human behavior and evolution. Psychol Rec 2006, 56: 3–21.

    Article  Google Scholar 

  128. Smith A. The empathy imbalance hypothesis of autism: a theoretical approach to cognitive and emotional empathy in autistic development. Psychol Rec 2009, 59: 489–510.

    Article  Google Scholar 

  129. Hovey D, Lindstedt M, Zettergren A, Jonsson L, Johansson A, Melke J, et al. Antisocial behavior and polymorphisms in the oxytocin receptor gene: findings in two independent samples. Mol Psychiatry 2016, 21: 983–988.

    Article  CAS  PubMed  Google Scholar 

  130. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 2001, 42: 241–251.

    Article  CAS  PubMed  Google Scholar 

  131. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. Oxytocin improves “mind-reading” in humans. Biol Psychiatry 2007, 61: 731–733.

    Article  CAS  PubMed  Google Scholar 

  132. Guastella AJ, Einfeld SL, Gray KM, Rinehart NJ, Tonge BJ, Lambert TJ, et al. Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry 2010, 67: 692–694.

    Article  CAS  PubMed  Google Scholar 

  133. American Psychiatric Association, 1994. Diagnostic and statistical manual of mental disorders (DSM-IV). Washington DC: American Psychiatric Association, 1994.

  134. Wöhr M, Scattoni ML. Behavioural methods used in rodent models of autism spectrum disorders: current standards and new developments. Behav Brain Res 2013, 251: 5–17.

    Article  PubMed  Google Scholar 

  135. Lukas M, Neumann ID. Oxytocin and vasopressin in rodent behaviors related to social dysfunctions in autism spectrum disorders. Behav Brain Res 2013, 251: 85–94.

    Article  CAS  PubMed  Google Scholar 

  136. Caldwell HK, Aulino EA, Freeman AR, Miller TV, Witchey SK. Oxytocin and behavior: Lessons from knockout mice. Dev Neurobiol 2017, 77: 190–201.

    Article  CAS  PubMed  Google Scholar 

  137. Marlin BJ, Froemke RC. Oxytocin modulation of neural circuits for social behavior. Dev Neurobiol 2017, 77: 169–189.

    Article  CAS  PubMed  Google Scholar 

  138. Peñagarikano O. Oxytocin in animal models of autism spectrum disorder. Dev Neurobiol 2017, 77: 202–213.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the National Basic Research Development Program of China (2013CB835100) and the Natural Science Foundation of China (81571072) to JC.

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Authors and Affiliations

  1. Institute for Biomedical Sciences of Pain, Tangdu Hospital, Fourth Military Medical University, Xi’an, 710038, China

    Jun Chen

  2. Key Laboratory of Brain Stress and Behavior, PLA, Xi’an, 710038, China

    Jun Chen

  3. Beijing Institute for Brain Disorders, Beijing, 100069, China

    Jun Chen

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  1. Jun Chen
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Correspondence to Jun Chen.

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Chen, J. Empathy for Distress in Humans and Rodents. Neurosci. Bull. 34, 216–236 (2018). https://doi.org/10.1007/s12264-017-0135-0

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  • DOI: https://doi.org/10.1007/s12264-017-0135-0

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