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The Role of Oxytocin in Social Buffering: What Do Primate Studies Add?

  • Catherine CrockfordEmail author
  • Tobias Deschner
  • Roman M. Wittig
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 35)

Abstract

The ability to maintain close social bonds impacts on reproductive success, longevity, stress and health in social mammals, including humans (Silk et al., Curr Biol 20(15):1359–1361, 2010; Crockford et al., Horm Behav 53(1):254–265, 2008; Wittig et al., Horm Behav 54(1):170–177, 2008; Archie et al., Proc R Soc B 281(1793):20141261, 2014; Cameron et al., Proc Natl Acad Sci U S A 106:13850–13853, 2009; Schülke et al., Curr Biol 20:2207–2210, 2010; Silk et al., Science 302:1231–1234, 2003; Holt-Lunstad et al., PLoS Med 7(7):e1000316, 2010). Close social bonds provide an important social support system, at least in part by acting as a buffer against the deleterious effects of chronic exposure to stressors (Young et al., Proc Natl Acad Sci U S A 51:18195–18200, 2014; Heinrichs et al., Biol Psychiatry 54:1389–1398, 2003). There is accumulating evidence that individuals that provide predictable affiliation or support to others (bond partners) may moderate the perception of the stressor as well as of the physiological stress response. The neuropeptide, oxytocin, may mediate social buffering by down-regulating HPA activity and thus reducing the stress response. However, much within this process remains unclear, such as whether oxytocin is always released when exposed to a stressor, whether more oxytocin is released if there is social support, what aspect of stress or social support triggers oxytocin release and whether social support in the absence of a stressor also impacts oxytocin release and HPA activity, during everyday life. We review the literature that addresses each of these questions in an attempt to clarify where future research effort will be helpful. A better understanding of these dynamics is likely to have implications for enhancing social and health gains from human social relationships.

Keywords

Cortisol Field primate studies Social support Stress 

Notes

Acknowledgements

Funding was provided by the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 679787 and the Max Planck Society.

References

  1. Archie EA, Tung J, Clark M, Altmann J, Alberts SC, Archie EA (2014) Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proc R Soc B 281(1793):20141261CrossRefPubMedGoogle Scholar
  2. Babygirija R, Bulbul M, Yoshimoto S, Ludwig K, Takahashi T (2012) Central and peripheral release of oxytocin following chronic homotypic stress in rats. Auton Neurosci 167:56–60CrossRefPubMedGoogle Scholar
  3. Beehner JC, Bergman TJ (2017) The next step for stress research in primates: to identify relationships between glucocorticoid secretion and fitness. Horm Behav 91:68–83CrossRefGoogle Scholar
  4. Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL (2005) The effect of new alpha males on female stress in free-ranging baboons. Anim Behav 69:1211–1221CrossRefGoogle Scholar
  5. Bosch OJ, Dabrowska J, Modi ME, Johnson ZV, Keebaugh AC, Barrett CE et al (2016) Oxytocin in the nucleus accumbens shell reverses CRFR2-evoked passive stress-coping after partner loss in monogamous male prairie voles. Psychoneuroendocrinology 64:66–78CrossRefPubMedGoogle Scholar
  6. Brown CA, Cardoso C, Ellenbogen MA (2016) A meta-analytic review of the correlation between peripheral oxytocin and cortisol concentrations. Front Neuroendocrinol 43:19–27CrossRefPubMedGoogle Scholar
  7. Burkett JP, Andari E, Curry DC, de Waal FBM, Young LJ (2016) Oxytocin-dependent consolation behavior in rodents. Science 351:375–378CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci U S A 106:13850–13853CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cavanaugh J, Carp SB, Rock CM, French JA (2016) Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys. Psychoneuroendocrinology 66:22–30CrossRefPubMedGoogle Scholar
  10. Cohen S, Wills TA (1985) Stress, social support, and the buffering hypothesis. Psychol Bull 98(2):310CrossRefPubMedGoogle Scholar
  11. Crockford C, Wittig RM, Whitten PL, Seyfarth RM, Cheney DL (2008) Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm Behav 53(1):254–265CrossRefPubMedGoogle Scholar
  12. Crockford C, Wittig RM, Langergraber K, Ziegler TE, Zuberbühler K, Deschner T (2013) Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proc R Soc B Biol Sci 280(1755):20122765CrossRefGoogle Scholar
  13. Crockford C, Deschner T, Ziegler TE, Wittig RM (2014) Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review. Front Behav Neurosci 8:68. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3949137&tool=pmcentrez&rendertype=abstractCrossRefPubMedPubMedCentralGoogle Scholar
  14. De Dreu CKW (2012) Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda. Horm Behav 61:419–428CrossRefPubMedGoogle Scholar
  15. Eckstein M, Scheele D, Weber K, Stoffel-Wagner B, Maier W, Hurlemann R (2014) Oxytocin facilitates the sensation of social stress. Hum Brain Mapp 35(9):4741–4750CrossRefPubMedGoogle Scholar
  16. Engelmann M, Ebner K, Landgraf R, Holsboer F, Wotjak CT (1999) Emotional stress triggers intrahypothalamic but not peripheral release of oxytocin in male rats. J Neuroendocrinol 11(11):867–872CrossRefPubMedGoogle Scholar
  17. Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM et al (2006) Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc Biol Sci 273:707–712CrossRefPubMedGoogle Scholar
  18. Field T, Diego M, Delgado J, Medina L (2013) Yoga and social support reduce prenatal depression, anxiety and cortisol. J Bodyw Mov Ther 17(4):397–403. doi: 10.1016/j.jbmt.2013.03.010CrossRefPubMedGoogle Scholar
  19. Fraser ON, Bugnyar T (2011) Ravens reconcile after aggressive conflicts with valuable partners. PLoS One 6(3):1–5CrossRefGoogle Scholar
  20. Grewen KM, Girdler SS, Amico J, Light KC (2005) Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact. Psychosom Med 67:531–538CrossRefPubMedGoogle Scholar
  21. Heinrichs M, Neumann I, Ehlert U (2002) Lactation and stress: protective effects of breast-feeding in humans. Stress 5(3):195–203CrossRefPubMedGoogle Scholar
  22. Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U (2003) Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 54:1389–1398CrossRefPubMedGoogle Scholar
  23. Hennessy MB, Kaiser S, Sachser N (2009) Social buffering of the stress response: diversity, mechanisms, and functions. Front Neuroendocrinol 30(4):470–482. doi: 10.1016/j.yfrne.2009.06.001CrossRefPubMedGoogle Scholar
  24. Hew-Butler T, Noakes TD, Soldin SJ, Verbalis JG (2008) Acute changes in endocrine and fluid balance markers during high-intensity, steady-state, and prolonged endurance running: unexpected increases in oxytocin and brain natriuretic peptide during exercise. Eur J Endocrinol 159(6):729–737CrossRefPubMedGoogle Scholar
  25. Holt-Lunstad J, Birmingham WA, Light KC (2008) Influence of a “warm touch” support enhancement intervention among married couples on ambulatory blood pressure, oxytocin, alpha amylase, and cortisol. Psychosom Med 70:976–985CrossRefPubMedGoogle Scholar
  26. Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7(7):e1000316CrossRefPubMedPubMedCentralGoogle Scholar
  27. Horvat-Gordon M, Granger DA, Schwartz EB, Nelson VJ, Kivlighan KT (2005) Oxytocin is not a valid biomarker when measured in saliva by immunoassay. Physiol Behav 84(3):445–448CrossRefPubMedGoogle Scholar
  28. Hostinar CE, Gunnar MR (2015) Social support can buffer against stress and shape brain activity. AJOB Neurosci 6(3):34–42CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hostinar CE, Sullivan RM, Gunnar MR (2014) Psychobiological mechanisms underlying the social buffering of the HPA axis: a review of animal models and human studies across development. Psychol Bull 140(1):997–1003CrossRefGoogle Scholar
  30. House JS, Landis KR, Umberson D (1988) Social relationships and health. Science 241(4865):540CrossRefPubMedGoogle Scholar
  31. Jezová D, Michajlovskij N, Kvetnanský R, Makara GB (1993) Paraventricular and supraoptic nuclei of the hypothalamus are not equally important for oxytocin release during stress. Neuroendocrinology 57:776–781CrossRefPubMedGoogle Scholar
  32. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci 361:2215–2228. doi: 10.1098/rstb.2006.1941CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2004) Partner’s stress status influences social buffering effects in rats. Behav Neurosci 118(4):798CrossRefPubMedGoogle Scholar
  34. Kornienko O, Clemans KH, Out D, Granger DA (2013) Friendship network position and salivary cortisol levels. Soc Neurosci 8:385–396CrossRefPubMedGoogle Scholar
  35. Lakey B, Orehek E (2011) Relational regulation theory: a new approach to explain the link between perceived social support and mental health. Psychol Rev 118:482–495CrossRefPubMedGoogle Scholar
  36. Leng G, Sabatier N (2016) Measuring oxytocin and vasopressin: bioassays, immunoassays and random numbers. J Neuroendocrinol 28(10). doi: 10.1111/jne.12413
  37. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445CrossRefGoogle Scholar
  38. McQuaid RJ, McInnis OA, Paric A, Al-Yawer F, Matheson K, Anisman H (2016) Relations between plasma oxytocin and cortisol: the stress buffering role of social support. Neurobiol Stress 3:52–60. doi: 10.1016/j.ynstr.2016.01.001CrossRefPubMedPubMedCentralGoogle Scholar
  39. Neumann ID (2008) Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 20:858–865CrossRefPubMedGoogle Scholar
  40. Olff M, Frijling JL, Kubzansky LD, Bradley B, Ellenbogen MA, Cardoso C et al (2013) The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38(9):1883–1894. doi: 10.1016/j.psyneuen.2013.06.019CrossRefPubMedGoogle Scholar
  41. Over H (2016) The origins of belonging: social motivation in infants and young children. Philos Trans R Soc Lond B Biol Sci 371(1686):20150072. doi: 10.1098/rstb.2015.0072CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ponzi D, Muehlenbein MP, Geary DC, Flinn MV (2016) Cortisol, salivary alpha-amylase and children’s perceptions of their social networks. Soc Neurosci 11(2):164–174. doi: 10.1080/17470919.2015.1045988CrossRefPubMedGoogle Scholar
  43. Radford AN (2008) Duration and outcome of intergroup conflict influences intragroup affiliative behaviour. Proc R Soc B Biol Sci 275(1653):2787–2791. doi: 10.1098/rspb.2008.0787CrossRefGoogle Scholar
  44. Radford AN (2011) Preparing for battle? Potential intergroup conflict promotes current intragroup affiliation. Biol Lett 7:26–29CrossRefPubMedGoogle Scholar
  45. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19(5):249–255CrossRefPubMedGoogle Scholar
  46. Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model – a new model integrating homeostasis, allostasis, and stress. Horm Behav 55(3):375–389CrossRefPubMedGoogle Scholar
  47. Rukstalis M, French JA (2005) Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Horm Behav 47(1):1–7CrossRefPubMedPubMedCentralGoogle Scholar
  48. Samuni L, Preis A, Mundry R, Deschner T, Crockford C, Wittig RM (2017) Oxytocin reactivity during intergroup conflict in wild chimpanzees. Proc Natl Acad Sci U S A 114(2):268–273CrossRefPubMedGoogle Scholar
  49. Sanchez MM, McCormack KM, Howell BR (2015) Social buffering of stress responses in nonhuman primates: maternal regulation of the development of emotional regulatory brain circuits. Soc Neurosci 10(5):512–526CrossRefPubMedPubMedCentralGoogle Scholar
  50. Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210CrossRefPubMedGoogle Scholar
  51. Seltzer LJ, Ziegler TE, Pollak SD (2010) Social vocalizations can release oxytocin in humans. Proc Biol Sci 277:2661–2666CrossRefPubMedPubMedCentralGoogle Scholar
  52. Silk JB (2007) Social components of fitness in primate groups. Science 317:1347–1351CrossRefPubMedGoogle Scholar
  53. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234CrossRefPubMedGoogle Scholar
  54. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR et al (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20(15):1359–1361CrossRefPubMedGoogle Scholar
  55. Smith AS, Wang Z (2012) Salubrious effects of oxytocin on social stress-induced deficits. Horm Behav 61(3):320–330. doi: 10.1016/j.yhbeh.2011.11.010CrossRefPubMedPubMedCentralGoogle Scholar
  56. Smith AS, Wang Z (2014) Hypothalamic oxytocin mediates social buffering of the stress response. Biol Psychiatry 76:281–288. doi: 10.1016/j.biopsych.2013.09.017CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sobolewski ME (2012) The hormonal correlates of male chimpanzee social behavior. PhD thesis, Harvard UniversityGoogle Scholar
  58. Taylor SE, Burklund LJ, Eisenberger NI, Lehman BJ, Hilmert CJ, Lieberman MD (2008) Neural bases of moderation of cortisol stress responses by psychosocial resources. J Pers Soc Psychol 95(1):197CrossRefPubMedGoogle Scholar
  59. Thoits PA (2011) Mechanisms linking social ties and support to physical and mental health. J Health Soc Behav 52(2):145–161. doi: 10.1177/0022146510395592CrossRefPubMedGoogle Scholar
  60. Torner L, Plotsky PM, Neumann ID, de Jong TR (2017) Forced swimming-induced oxytocin release into blood and brain: effects of adrenalectomy and corticosterone treatment. Psychoneuroendocrinology 77:165–174CrossRefPubMedGoogle Scholar
  61. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10(6):397–409. doi: 10.1038/nrn2647CrossRefPubMedPubMedCentralGoogle Scholar
  62. WHO (2010) WHO guidelines on drawing blood: best practices in phlebotomy. World Health Organization, Geneva, pp 1–105Google Scholar
  63. Wittig RM, Boesch C (2005) How to repair relationships – reconciliation in wild chimpanzees (Pan troglodytes). Ethology 111:736–763CrossRefGoogle Scholar
  64. Wittig RM, Crockford C, Lehmann J, Whitten PL, Seyfarth RM, Cheney DL (2008) Focused grooming networks and stress alleviation in wild female baboons. Horm Behav 54(1):170–177CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wittig RM, Crockford C, Weltring A, Deschner T, Zuberbühler K (2015) Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees. PLoS One 10(2):e0118695CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wittig RM, Crockford C, Weltring A, Langergraber KE, Deschner T, Zuberbühler K (2016) Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations. Nat Commun 13361. http://www.nature.com/doifinder/10.1038/ncomms13361CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wrangham RW, Glowacki L (2012) Intergroup aggression in chimpanzees and war in nomadic hunter-gatherers: evaluating the chimpanzee model. Hum Nat 23(1):5–29CrossRefPubMedGoogle Scholar
  68. Young C, Majolo B, Heistermann M, Schülke O, Ostner J (2014) Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. Proc Natl Acad Sci U S A 51:18195–18200CrossRefGoogle Scholar
  69. Ziegler TE, Crockford C (2017) Neuroendocrine control in social relationships in non-human primates: field based evidence. Horm Behav. http://linkinghub.elsevier.com/retrieve/pii/S0018506X16301064CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Catherine Crockford
    • 1
    Email author
  • Tobias Deschner
    • 1
  • Roman M. Wittig
    • 1
  1. 1.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany

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