Bridging the Gap Between People and Animals: The Roots of Social Behavior and Its Relationship to Pain



Pain is considered a personal experience, but it is rarely private. Individuals’ responses to pain function to communicate distress to others in the environment, eliciting emotional reactions and caregiving actions that in turn impact the sufferer’s pain experience. In animals, these behaviors are considered empathy-like and indicative of a complex social framework. Laboratory experiments on animals and humans have shown that social context can have direct effects on the expression of pain. In this review, we discuss the foundations of social behavior in animal models, how they relate to empathy, and highlight shared neural mechanisms between pain and social behaviors.


Empathy Pain Animal model Emotional contagion Human Neuroscience Oxytocin Prosocial behavior Helping behavior Familiarity 


  1. Aghajani, M., Mahdavi, M. R. V., Najafabadi, M. K., Ghazanfari, T., Azimi, A., Soleymani, S. A., & Dust, S. M. (2013). Effects of dominant/subordinate social status on formalin-induced pain and changes in serum proinflammatory cytokine concentrations in mice. PLoS One, 8, e80650.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Akther, S., Korshnova, N., Zhong, J., Liang, M. K., Cherepanov, S. M., Lopatina, O., … Higashida, H. (2013). CD38 in the nucleus accumbens and oxytocin are related to paternal behavior in mice. Molecular Brain, 6, 41.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andre, J., Zeau, B., Pohl, M., Cesselin, F., Benoliel, J. J., & Becker, C. (2005). Involvement of cholecystokininergic systems in anxiety-induced hyperalgesia in male rats: Behavioral and biochemical studies. Journal of Neuroscience, 25, 7896–7904.PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2008). Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Social Cognitive and Affective Neuroscience, 3, 128–134.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bales, K. L., & Carter, C. S. (2003). Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Hormones and Behavior, 44, 178–184.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bamshad, M., Novak, M. A., & de Vries, G. J. (1994). Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiology and Behavior, 56, 751–758.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Baron-Cohen, S., & Wheelwright, S. (2004). The empathy quotient: An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34, 163–175.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bartal, I. B., Shan, H. Z., Molasky, N. M. R., Murray, T. M., Williams, J. Z., Decety, J., & Mason, P. (2016). Anxiolytic treatment impairs helping behavior in rats. Frontiers in Psychology, 7, 850.Google Scholar
  9. Bartz, J. A., Zaki, J., Bolger, N., Hollander, E., Ludwig, N. N., Kolevzon, A., & Ochsner, K. N. (2010). Oxytocin selectively improves empathic accuracy. Psychological Science, 21, 1426–1428.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Beckes, L., Coan, J. A., & Hasselmo, K. (2013). Familiarity promotes the blurring of self and other in the neural representation of threat. Social Cognitive and Affective Neuroscience, 8, 670–677.PubMedCrossRefPubMedCentralGoogle Scholar
  11. Ben-Ami Bartal, I., Decety, J., & Mason, P. (2011). Empathy and pro-social behavior in rats. Science, 334, 1427–1430.PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bester-Meredith, J. K., Young, L. J., & Marler, C. A. (1999). Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Hormones and Behavior, 36, 25–38.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bos, P. A., Hofman, D., Hermans, E. J., Montoya, E. R., Baron-Cohen, S., & van Honk, J. (2016). Testosterone reduces functional connectivity during the ‘reading the mind in the eyes’ test. Psychoneuroendocrinology, 68, 194–201.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bosch, O. J., Meddle, S. L., Beiderbeck, D. I., Douglas, A. J., & Neumann, I. D. (2005). Brain oxytocin correlates with maternal aggression: Link to anxiety. Journal of Neuroscience, 25, 6807–6815.PubMedCrossRefPubMedCentralGoogle Scholar
  15. Bowles, S. (2009). Did warfare among ancestral hunter-gatherers affect the evolution of human social behaviors? Science, 324, 1293–1298.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Brandtzaeg, O. K., Johnsen, E., Roberg-Larsen, H., Seip, K. F., MacLean, E. L., Gesquiere, L. R., … Wilson, S. R. (2016). Proteomics tools reveal startlingly high amounts of oxytocin in plasma and serum. Scientific Reports, 6, 31693.Google Scholar
  17. Bruchey, A. K., Jones, C. E., & Monfils, M.-H. (2010). Fear conditioning by-proxy: Social transmission of fear during memory retrieval. Behavioural Brain Research, 214, 80–84.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Buchan, J. C., Alberts, S. C., Silk, J. B., & Altmann, J. (2003). True paternal care in a multi-male primate society. Nature, 425, 179–181.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B., & Young, L. J. (2016). Oxytocin-dependent consolation behavior in rodents. Science, 351, 375–378.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Byrne, R. W., & Corp, N. (2004). Neocortex size predicts deception rate in primates. Proceedings of the Royal Society B: Biological Sciences, 271, 1693.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Calcagnoli, F., Stubbendorff, C., Meyer, N., de Boer, S. F., Althaus, M., & Koolhaas, J. M. (2015). Oxytocin microinjected into the central amygdaloid nuclei exerts anti-aggressive effects in male rats. Neuropharmacology, 90, 74–81.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Caligioni, C., & Franci, C. (2002). Oxytocin secretion induced by osmotic stimulation in rats during the estrous cycle and after ovariectomy and hormone replacement therapy. Life Sciences, 71, 2821–2831.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Cantoni, D., & Brown, R. E. (1997). Paternal investment and reproductive success in the California mouse, Peromyscus californicus. Animal Behaviour, 54, 377–386.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Cassady, J. C., & Johnson, R. E. (2002). Cognitive test anxiety and academic performance. Contemporary Educational Psychology, 27(2), 270–295.CrossRefGoogle Scholar
  25. Chang, S. W., Gariepy, J. F., & Platt, M. L. (2013). Neuronal reference frames for social decisions in primate frontal cortex. Nature Neuroscience, 16, 243–250.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Chapman, E., Baron-Cohen, S., Auyeung, B., Knickmeyer, R., Taylor, K., & Hackett, G. (2006). Fetal testosterone and empathy: Evidence from the Empathy Quotient (EQ) and the “reading the mind in the eyes” test. Social Neuroscience, 1, 135–148.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Charpentier, M. J., Peignot, P., Hossaert-McKey, M., & Wickings, E. J. (2007). Kin discrimination in juvenile mandrills, Mandrillus sphinx. Animal Behaviour, 73, 37–45.CrossRefGoogle Scholar
  28. Cicirello, D. M., & Wolff, J. O. (1990). The effects of mating on infanticide and pup discrimination in white-footed mice. Behavioral Ecology and Sociobiology, 26, 275–279.CrossRefGoogle Scholar
  29. Clark, M. M., & Galef, B. G. (2000). Why some male Mongolian gerbils may help at the nest: Testosterone, asexuality and alloparenting. Animal Behaviour, 59, 801–806.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Consiglio, A. R., Borsoi, A., Pereira, G. A., & Lucion, A. B. (2005). Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiology & Behavior, 85, 354–362.CrossRefGoogle Scholar
  31. D’Amato, F. R., & Pavone, F. (1996). Reunion of separated sibling mice: Neurobiological and behavioral aspects. Neurobiology of Learning and Memory, 65, 9–16.PubMedCrossRefPubMedCentralGoogle Scholar
  32. De Felipe, C., Herrero, J. F., O'brien, J. A., Palmer, J. A., Doyle, C. A., Smith, A. J., … Hunt, S. P. (1998). Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature, 392, 394–397.PubMedCrossRefPubMedCentralGoogle Scholar
  33. De Waal, F. B. M. (2008). Putting the altruism back into altruism: The evolution of empathy. Annual Review of Psychology, 59, 279–300.PubMedCrossRefPubMedCentralGoogle Scholar
  34. De Waal, F. B. M., Aureli, F., & Judge, P. G. (2000). Coping with crowding. Scientific American, 282, 76–81.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Downey, D. B. (1994). The school performance of children from single-mother and single-father families: Economic or interpersonal deprivation? Journal of Family Issues, 15, 129–147.CrossRefGoogle Scholar
  36. Dulac, C., O’Connell, L. A., & Wu, Z. (2014). Neural control of maternal and paternal behaviors. Science, 345, 765–770.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dumais, K. M., Alonso, A. G., Bredewold, R., & Veenema, A. H. (2016). Role of the oxytocin system in amygdala subregions in the regulation of social interest in male and female rats. Neuroscience, 330, 138–149.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Dumais, K. M., Alonso, A. G., Immormino, M. A., Bredewold, R., & Veenema, A. H. (2016). Involvement of the oxytocin system in the bed nucleus of the stria terminalis in the sex-specific regulation of social recognition. Psychoneuroendocrinology, 64, 79–88.PubMedCrossRefGoogle Scholar
  39. Dunbar, R., & Bever, J. (1998). Neocortex size predicts group size in carnivores and some insectivores. Ethology, 104, 695–708.CrossRefGoogle Scholar
  40. Edgerly, J. S. (1988). Maternal behaviour of a webspinner (order Embiidina): Mother-nymph associations. Ecological Entomology, 13, 263–272.CrossRefGoogle Scholar
  41. Feldman, R., Gordon, I., & Zagoory-Sharon, O. (2011). Maternal and paternal plasma, salivary, and urinary oxytocin and parent–infant synchrony: Considering stress and affiliation components of human bonding. Developmental Science, 14, 752–761.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Feldman, R., Weller, A., Zagoory-Sharon, O., & Levine, A. (2007). Evidence for a neuroendocrinological foundation of human affiliation plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychological Science, 18, 965–970.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Felicio, L. F., Mann, P. E., & Bridges, R. S. (1991). Intracerebroventricular cholecystokinin infusions block beta-endorphin-induced disruption of maternal behavior. Pharmacology Biochemistry and Behavior, 39, 201–204.CrossRefGoogle Scholar
  44. Feng, C. L., Li, Z. H., Feng, X., Wang, L. L., Tian, T. X., & Luo, Y. J. (2016). Social hierarchy modulates neural responses of empathy for pain. Social Cognitive and Affective Neuroscience, 11, 485–495.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Francis, D. D., Young, L. J., Meaney, M. J., & Insel, T. R. (2002). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: Gender differences. Journal of Neuroendocrinology, 14, 349–353.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gioiosa, L., Chiarotti, F., Alleva, E., & Laviola, G. (2009). A trouble shared is a trouble halved: Social context and status affect pain in mouse dyads. PLoS One, 4, e4143.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Graves, J., & Whiten, A. (1980). Adoption of strange chicks by herring gulls, Larus argentatus L. Ethology, 54, 267–278.Google Scholar
  48. Gubernick, D. J., Winslow, J. T., Jensen, P., Jeanotte, L., & Bowen, J. (1995). Oxytocin changes in males over the reproductive cycle in the monogamous, biparental California mouse, Peromyscus californicus. Hormones and Behavior, 29, 59–73.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Hanelová, J., & Vilímová, J. (2013). Behaviour of the central European Acanthosomatidae (Hemiptera: Heteroptera: Pentatomoidea) during oviposition and parental care. Acta Musei Moraviae, Scientiae Biologicae, 98, 433–457.Google Scholar
  50. Hayden, S. R., Jackson, T. T., & Guydish, J. (1984). Helping behavior of females: Effects of stress and commonality of fate. The Journal of Psychology, 117, 233–237.PubMedCrossRefGoogle Scholar
  51. Hein, G., Silani, G., Preuschoff, K., Batson, C. D., & Singer, T. (2010). Neural responses to ingroup and outgroup members’ suffering predict individual differences in costly helping. Neuron, 68, 149–160.PubMedCrossRefGoogle Scholar
  52. Higham, J. P., Barr, C. S., Hoffman, C. L., Mandalaywala, T. M., Parker, K. J., & Maestripieri, D. (2011). Mu-opioid receptor (OPRM1) variation, oxytocin levels and maternal attachment in free-ranging rhesus macaques Macaca mulatta. Behavioral Neuroscience, 125, 131–136.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hild, S., Andersen, I. L., & Zanella, A. J. (2010). The relationship between thermal nociceptive threshold in lambs and ewe–lamb interactions. Small Ruminant Research, 90, 142–145.CrossRefGoogle Scholar
  54. Holman, S., & Goy, R. (1980). Behavioral and mammary responses of adult female rhesus to strange infants. Hormones and Behavior, 14, 348–357.PubMedCrossRefGoogle Scholar
  55. Holman, S., & Goy, R. W. (1995). Experiential and hormonal correlates of care-giving in rhesus macaques. In Motherhood in human and nonhuman primates: Biosocial determinants (pp. 87–93). Basel, Switzerland: Karger Publishers.Google Scholar
  56. Howells, E. M., Reif, J. S., Bechdel, S. E., Murdoch, M. E., Bossart, G. D., McCulloch, S. D., & Mazzoil, M. S. (2009). A novel case of non-offspring adoption in a free-ranging Atlantic bottlenose dolphin (Tursiops truncatus) inhabiting the Indian River Lagoon, Florida. Aquatic Mammals, 35, 43–47.CrossRefGoogle Scholar
  57. Huchard, E., Charpentier, M. J., Marshall, H., King, A. J., Knapp, L. A., & Cowlishaw, G. (2012). Paternal effects on access to resources in a promiscuous primate society. Behavioral Ecology, 24, 229–236.CrossRefGoogle Scholar
  58. Insel, T. R., & Hulihan, T. J. (1995). A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles. Behavioral Neuroscience, 109, 782.PubMedCrossRefGoogle Scholar
  59. Izar, P., Verderane, M. P., Visalberghi, E., Ottoni, E. B., Gomes De Oliveira, M., Shirley, J., & Fragaszy, D. (2006). Cross-genus adoption of a marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus): Case report. American Journal of Primatology, 68, 692–700.PubMedCrossRefGoogle Scholar
  60. Jenkins, E. V., Morris, C., & Blackman, S. (2000). Delayed benefits of paternal care in the burying beetle Nicrophorus vespilloides. Animal Behaviour, 60, 443–451.PubMedCrossRefGoogle Scholar
  61. Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., … Shin, H.-S. (2010). Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nature Neuroscience, 13, 482–488.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Jouventin, P., Barbraud, C., & Rubin, M. (1995). Adoption in the emperor penguin, Aptenodytes forsteri. Animal Behaviour, 50, 1023–1029.CrossRefGoogle Scholar
  63. Kavaliers, M., Colwell, D. D., & Choleris, E. (2005). Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behavioral Ecology and Sociobiology, 58, 60–71.CrossRefGoogle Scholar
  64. Kendrick, K., Keverne, E., & Baldwin, B. (1987). Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology, 46, 56–61.PubMedCrossRefGoogle Scholar
  65. Kim, B. S., Lee, J., Bang, M., Am Seo, B., Khalid, A., Jung, M. W., & Jeon, D. (2014). Differential regulation of observational fear and neural oscillations by serotonin and dopamine in the mouse anterior cingulate cortex. Psychopharmacology, 231, 4371–4381.PubMedCrossRefGoogle Scholar
  66. Kim, S., Mátyás, F., Lee, S., Acsády, L., & Shin, H.-S. (2012). Lateralization of observational fear learning at the cortical but not thalamic level in mice. Proceedings of the National Academy of Sciences U S A, 109, 15497–15501.CrossRefGoogle Scholar
  67. Knickmeyer, R., Baron-Cohen, S., Raggatt, P., & Taylor, K. (2005). Foetal testosterone, social relationships, and restricted interests in children. Journal of Child Psychology and Psychiatry, 46, 198–210.PubMedCrossRefGoogle Scholar
  68. Konig, M., Zimmer, A. M., Steiner, H., & Holmes, P. V. (1996). Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature, 383, 535.PubMedCrossRefGoogle Scholar
  69. Kuczaj, S. A., Frick, E. E., Jones, B. L., Lea, J. S. E., Beecham, D., & Schnoller, F. (2015). Underwater observations of dolphin reactions to a distressed conspecific. Learning and Behavior, 43, 289–300.PubMedCrossRefGoogle Scholar
  70. Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000). Long-term behavioral and neuroendocrine adaptations to adverse early experience. Progress in Brain Research, 122, 81–103.PubMedCrossRefPubMedCentralGoogle Scholar
  71. Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt, J. S., … Mogil, J. S. (2006). Social modulation of pain as evidence for empathy in mice. Science, 312, 1967–1970.CrossRefGoogle Scholar
  72. Langford, D. J., Tuttle, A. H., Briscoe, C., Harvey-Lewis, C., Baran, I., Gleeson, P., … Mogil, J. S. (2011). Varying perceived social threat modulates pain behavior in male mice. The Journal of Pain, 12, 125–132.CrossRefGoogle Scholar
  73. Langford, D. J., Tuttle, A. H., Brown, K., Deschenes, S., Fischer, D. B., Mutso, A., … Sternberg, W. F. (2010). Social approach to pain in laboratory mice. Social Neuroscience, 5, 163–170.PubMedCrossRefPubMedCentralGoogle Scholar
  74. Lidhar, N. K., Insel, N., Dong, J. Y., & Takehara-Nishiuchi, K. (2017). Observational fear learning in degus is correlated with temporal vocalization patterns. Behavioural Brain Research, 332, 362–371.PubMedCrossRefPubMedCentralGoogle Scholar
  75. Lloyd, D., Di Pellegrino, G., & Roberts, N. (2004). Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue? Cognitive, Affective, & Behavioral Neuroscience, 4, 270–278.CrossRefGoogle Scholar
  76. Loggia, M. L., Mogil, J. S., & Bushnell, M. C. (2008). Empathy hurts: Compassion for another increases both sensory and affective components of pain perception. Pain, 136, 168–176.CrossRefGoogle Scholar
  77. Lubin, D. A., Elliot, J. C., Black, M. C., & Johns, J. M. (2003). An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behavioral Neuroscience, 117, 195.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lutchmaya, S., Baron-Cohen, S., & Raggatt, P. (2002). Foetal testosterone and eye contact in 12-month-old human infants. Infant Behavior and Development, 25, 327–335.CrossRefGoogle Scholar
  79. Maestripieri, D. (1993). Infant kidnapping among group-living rhesus macaques: Why don’t mothers rescue their infants? Primates, 34, 211–216.CrossRefGoogle Scholar
  80. Maestripieri, D., Hoffman, C. L., Anderson, G. M., Carter, C. S., & Higley, J. D. (2009). Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioral variables. Physiology and Behavior, 96, 613–619.PubMedCrossRefPubMedCentralGoogle Scholar
  81. Mann, P., Kinsley, C., & Bridges, R. (1991). Opioid receptor subtype involvement in maternal behavior in lactating rats. Neuroendocrinology, 53, 487–492.PubMedCrossRefPubMedCentralGoogle Scholar
  82. Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C. (2015). Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature, 520, 499–504.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Martin, L. J., Hathaway, G., Isbester, K., Mirali, S., Acland, E. L., Niederstrasser, N., … Sapolsky, R. M. (2015). Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Current Biology, 25, 326–332.PubMedCrossRefPubMedCentralGoogle Scholar
  84. McCarthy, M. M. (1990). Oxytocin inhibits infanticide in female house mice (Mus domesticus). Hormones and Behavior, 24, 365–375.PubMedCrossRefPubMedCentralGoogle Scholar
  85. McNutt, J. W. (1996). Adoption in African wild dogs, Lycaon pictus. Journal of Zoology, 240, 163–173.CrossRefGoogle Scholar
  86. Mikosz, M., Nowak, A., Werka, T., & Knapska, E. (2015). Sex differences in social modulation of learning in rats. Scientific Reports, 5, 18114.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Mogil, J. S. (2009). Animal models of pain: Progress and challenges. Nature Reviews Neuroscience, 10, 283–294.PubMedCrossRefPubMedCentralGoogle Scholar
  88. Monassi, C. R., Bandler, R., & Keay, K. A. (2003). A subpopulation of rats show social and sleep-waking changes typical of chronic neuropathic pain following peripheral nerve injury. European Journal of Neuroscience, 17, 1907–1920.PubMedCrossRefPubMedCentralGoogle Scholar
  89. Nagasawa, M., Okabe, S., Mogi, K., & Kikusui, T. (2012). Oxytocin and mutual communication in mother-infant bonding. Frontiers in Human Neuroscience, 6, 31.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Olazabal, D., & Young, L. (2006). Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles. Neuroscience, 141, 559–568.PubMedCrossRefPubMedCentralGoogle Scholar
  91. Owen, S. F., Tuncdemir, S. N., Bader, P. L., Tirko, N. N., Fishell, G., & Tsien, R. W. (2013). Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature, 500, 458–462.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Parker, K. J., & Lee, T. M. (2001). Central vasopressin administration regulates the onset of facultative paternal behavior in Microtus pennsylvanicus (meadow voles). Hormones and Behavior, 39, 285–294.PubMedCrossRefPubMedCentralGoogle Scholar
  93. Parr, L. A., & de Waal, F. B. M. (1999). Visual kin recognition in chimpanzees. Nature, 399, 647–648.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Pedersen, C. A., Ascher, J. A., Monroe, Y. L., & Prange, A. J. (1982). Oxytocin induces maternal behavior in virgin female rats. Science, 216, 648–650.PubMedCrossRefPubMedCentralGoogle Scholar
  95. Pillay, N. (2000). Fostering in the African striped mouse: Implications for kin recognition and dominance. Acta Theriologica, 45, 193–200.CrossRefGoogle Scholar
  96. Plotnik, J. M., & de Waal, F. B. M. (2014). Asian elephants (Elephas maximus) reassure others in distress. PeerJ, 2, e278.PubMedPubMedCentralCrossRefGoogle Scholar
  97. Queller, D. C., Zacchi, F., Cervo, R., Turillazzi, S., Henshaw, M. T., Santorelli, L. A., & Strassmann, J. E. (2000). Unrelated helpers in a social insect. Nature, 405, 784–787.PubMedCrossRefPubMedCentralGoogle Scholar
  98. Radford, A. N. (2008). Duration and outcome of intergroup conflict influences intragroup affiliative behaviour. Proceedings of the Royal Society of London B: Biological Sciences, 275, 2787–2791.CrossRefGoogle Scholar
  99. Rash, J. A., Aguirre-Camacho, A., & Campbell, T. S. (2014). Oxytocin and pain: A systematic review and synthesis of findings. The Clinical Journal of Pain, 30, 453–462.PubMedPubMedCentralGoogle Scholar
  100. Rice, G. E., & Gainer, P. (1962). Altruism in albino rat. Journal of Comparative and Physiological Psychology, 55, 123–125.PubMedCrossRefPubMedCentralGoogle Scholar
  101. Richards, M. (1966). Maternal behaviour in the golden hamster: Responsiveness to young in virgin, pregnant, and lactating females. Animal Behaviour, 14, 310–313.PubMedCrossRefPubMedCentralGoogle Scholar
  102. Riedman, M. L., & Le Boeuf, B. J. (1982). Mother-pup separation and adoption in northern elephant seals. Behavioral Ecology and Sociobiology, 11, 203–215.CrossRefGoogle Scholar
  103. Sato, N., Tan, L., Tate, K., & Okada, M. (2015). Rats demonstrate helping behavior toward a soaked conspecific. Animal Cognition, 18, 1039–1047.PubMedCrossRefPubMedCentralGoogle Scholar
  104. Schino, G., Aureli, F., D'Amato, F. R., D'Antoni, M., Pandolfi, N., & Troisi, A. (1993). Infant kidnapping and co-mothering in Japanese macaques. American Journal of Primatology, 30, 257–262.CrossRefGoogle Scholar
  105. Schneeberger, K., Dietz, M., & Taborsky, M. (2012). Reciprocal cooperation between unrelated rats depends on cost to donor and benefit to recipient. BMC Evolutionary Biology, 12, 41.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Schorscher-Petcu, A., Sotocinal, S., Ciura, S., Dupre, A., Ritchie, J., Sorge, R. E., … Mogil, J. S. (2010). Oxytocin-induced analgesia and scratching are mediated by the vasopressin-1A receptor in the mouse. Journal of Neuroscience, 30, 8274–8284.PubMedCrossRefPubMedCentralGoogle Scholar
  107. Schulte, B. A. (2000). Social structure and helping behavior in captive elephants. Zoo Biology, 19, 447–459.CrossRefGoogle Scholar
  108. Silberberg, A., Allouch, C., Sandfort, S., Kearns, D., Karpel, H., & Slotnick, B. (2014). Desire for social contact, not empathy, may explain “rescue” behavior in rats. Animal Cognition, 17, 609–618.PubMedCrossRefPubMedCentralGoogle Scholar
  109. Silk, J. B. (1980). Kidnapping and female competition among captive bonnet macaques. Primates, 21, 100–110.CrossRefGoogle Scholar
  110. Silva, R. B., Vieira, E. M., & Izar, P. (2008). Social monogamy and biparental care of the neotropical southern bamboo rat (Kannabateomys amblyonyx). Journal of Mammalogy, 89, 1464–1472.CrossRefGoogle Scholar
  111. Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303, 1157–1162.PubMedCrossRefPubMedCentralGoogle Scholar
  112. Sivaselvachandran, S., Acland, E. L., Abdallah, S., & Martin, L. J. (2016). Behavioral and mechanistic insight into rodent empathy. Neuroscience and Biobehavioral Reviews.Google Scholar
  113. Stürmer, S., Snyder, M., Kropp, A., & Siem, B. (2006). Empathy-motivated helping: The moderating role of group membership. Personality and Social Psychology Bulletin, 32, 943–956.PubMedCrossRefPubMedCentralGoogle Scholar
  114. Tajfel, H., Billig, M. G., Bundy, R. P., & Flament, C. (1971). Social categorization and intergroup behaviour. European Journal of Social Psychology, 1, 149–178.CrossRefGoogle Scholar
  115. Takayanagi, Y., Yoshida, M., Bielsky, I. F., Ross, H. E., Kawamata, M., Onaka, T., … Nishimon, K. (2005). Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proceedings of the National Academy of Sciences U S A, 102, 16096–16101.CrossRefGoogle Scholar
  116. Tallamy, D. W. (1984). Insect parental care. Bioscience, 34, 20–24.CrossRefGoogle Scholar
  117. Tan, J., & Hare, B. (2013). Bonobos share with strangers. PLoS One, 8, e51922.PubMedPubMedCentralCrossRefGoogle Scholar
  118. Taylor, S. E. (2006). Tend and befriend biobehavioral bases of affiliation under stress. Current Directions in Psychological Science, 15, 273–277.CrossRefGoogle Scholar
  119. Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A., & Updegraff, J. A. (2000). Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight. Psychological Review, 107, 411–429.PubMedCrossRefPubMedCentralGoogle Scholar
  120. Uvnasmoberg, K., Bruzelius, G., Alster, P., & Lundeberg, T. (1993). The antinociceptive effect of nonnoxious sensory stimulation is mediated partly through oxytocinergic mechanisms. Acta Physiologica Scandinavica, 149, 199–204.CrossRefGoogle Scholar
  121. Van Honk, J., Schutter, D. J., Bos, P. A., Kruijt, A.-W., Lentjes, E. G., & Baron-Cohen, S. (2011). Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proceedings of the National Academy of Sciences U S A, 108, 3448–3452.CrossRefGoogle Scholar
  122. von Dawans, B., Fischbacher, U., Kirschbaum, C., Fehr, E., & Heinrichs, M. (2012). The social dimension of stress reactivity acute stress increases prosocial behavior in humans. Psychological Science, 23, 651–660.CrossRefGoogle Scholar
  123. Wang, Z., Ferris, C. F., & De Vries, G. J. (1994). Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proceedings of the National Academy of Sciences U S A, 91, 400–404.CrossRefGoogle Scholar
  124. Watanabe, S. (2014). The dominant/subordinate relationship between mice modifies the approach behavior toward a cage mate experiencing pain. Behavioural Processes, 103, 1–4.PubMedCrossRefPubMedCentralGoogle Scholar
  125. Way, B. M., Taylor, S. E., & Eisenberger, N. I. (2009). Variation in the μ-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proceedings of the National Academy of Sciences U S A, 106, 15079–15084.CrossRefGoogle Scholar
  126. Weitoft, G. R., Hjern, A., Haglund, B., & Rosén, M. (2003). Mortality, severe morbidity, and injury in children living with single parents in Sweden: A population-based study. The Lancet, 361, 289–295.CrossRefGoogle Scholar
  127. Williams, A. C. d. C., Gallagher, E., Fidalgo, A. R., & Bentley, P. J. (2016). Pain expressiveness and altruistic behavior: An exploration using agent-based modeling. Pain, 157, 759.CrossRefGoogle Scholar
  128. Wilson, M. L., & Wrangham, R. W. (2003). Intergroup relations in chimpanzees. Annual Review of Anthropology, 32, 363–392.CrossRefGoogle Scholar
  129. Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993). A role for central vasopressin in pair bonding in monogamous prairie voles. Nature, 365, 545.PubMedCrossRefPubMedCentralGoogle Scholar
  130. Xu, X., Zuo, X., Wang, X., & Han, S. (2009). Do you feel my pain? Racial group membership modulates empathic neural responses. Journal of Neuroscience, 29, 8525–8529.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of Toronto MississaugaMississaugaCanada
  2. 2.Department of Cell Systems and BiologyUniversity of Toronto MississaugaMississaugaCanada

Personalised recommendations