586
Views
21
CrossRef citations to date
0
Altmetric
Original Articles

Associations between early life experience, chronic HPA axis activity, and adult social rank in rhesus monkeys

, , , , , & show all
Pages 92-101 | Received 04 Dec 2015, Published online: 25 Apr 2016

References

  • Abbott, D. H., Keverne, E. B., Bercovitch, F. B., Shively, C. A., Mendoza, S. P., Saltzman, W., … Sapolsky, R. M. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior, 43(1), 67–82. doi:10.1016/S0018-506X(02)00037-5
  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3), 227–266. doi:10.1163/156853974X00534
  • Andrews, M. W., & Rosenblum, L. A. (1994). The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Development, 65(5), 1398–1404. doi:10.2307/1131506
  • Bahadori, M., Sanaeinasab, H., Ghanei, M., Tavana, A. M., Ravangard, R., & Karamali, M. (2015). The social determinants of health (SDH) in Iran: A systematic review article. Iranian Journal of Public Health, 44(6), 728.
  • Balasubramaniam, K. N., Dittmar, K., Berman, C. M., Butovskaya, M., Cooper, M. A., Majolo, B., … De Waal, F. B. M. (2012). Hierarchical steepness, counter aggression, and macaque social style scale. American Journal of Primatology, 74(10), 915–925. doi:10.1002/ajp.2012.74.issue-10
  • Bastian, M. L., Sponberg, A. C., Suomi, S. J., & Higley, J. D. (2003). Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta). Developmental Psychobiology, 42(1), 44–51. doi:10.1002/dev.10091
  • Bernstein, I. S., & Ehardt, C. (1986). The influence of kinship and socialization on aggressive behaviour in rhesus monkeys (Macaca mulatta). Animal Behaviour, 34(3), 739–747. doi:10.1016/S0003-3472(86)80057-4
  • Bernstein, I. S., & Ehardt, C. L. (1985). Age-sex differences in the expression of agonistic behavior in rhesus monkey (Macaca mulatta) groups. Journal of Comparative Psychology, 99(2), 115–132. doi:10.1037/0735-7036.99.2.115
  • Blomquist, G. E. (2009). Trade-off between age of first reproduction and survival in a female primate. Biology Letters, 5(3), 339–342. doi:10.1098/rsbl.2009.0009
  • Brotman, L. M., Gouley, K. K., Huang, K.-Y., Kamboukos, D., Fratto, C., & Pine, D. S. (2007). Effects of a psychosocial family-based preventive intervention on cortisol response to a social challenge in preschoolers at high risk for antisocial behavior. Archives of General Psychiatry, 64(10), 1172–1179. doi:10.1001/archpsyc.64.10.1172
  • Browne, D. T., & Jenkins, J. M. (2012). Health across early childhood and socioeconomic status: Examining the moderating effects of differential parenting. Social Science & Medicine, 74(10), 1622–1629. doi:10.1016/j.socscimed.2012.01.017
  • Bush, N. R., Obradović, J., Adler, N., & Boyce, W. T. (2011). Kindergarten stressors and cumulative adrenocortical activation: The “first straws” of allostatic load? Development and Psychopathology, 23(04), 1089–1106. doi:10.1017/S0954579411000514
  • Chen, E., Cohen, S., & Miller, G. E. (2010). How low socioeconomic status affects 2 year hormonal trajectories in children. Psychological Science, 21(1), 31–37. doi:10.1177/0956797609355566
  • Cohen, S., Doyle, W. J., & Baum, A. (2006). Socioeconomic status is associated with stress hormones. Psychosomatic Medicine, 68(3), 414–420. doi:10.1097/01.psy.0000221236.37158.b9
  • Conti, G., Hansman, C., Heckman, J. J., Novak, M. F., Ruggiero, A., & Suomi, S. J. (2012). Primate evidence on the late health effects of early-life adversity. Proceedings of the National Academy of Sciences, 109(23), 8866–8871. doi:10.1073/pnas.1205340109
  • Cummins, D. (2005). Dominance, status, and social hierarchies. In The handbook of evolutionary psychology (pp. 676–697). Hoboken, NJ: Wiley.
  • Daubenmier, J., Kristeller, J., Hecht, F. M., Maninger, N., Kuwata, M., Jhaveri, K., … Epel, E. (2011). Mindfulness intervention for stress eating to reduce cortisol and abdominal fat among overweight and obese women: An exploratory randomized controlled study. Journal of Obesity, 2011, 1–13. doi:10.1155/2011/651936
  • Dettmer, A. M. (2015). Age at first reproduction in female rhesus monkeys at the LCE field station. Unpublished raw data.
  • Dettmer, A. M., Kaburu, S. S., Byers, K. L., Murphy, A. M., Soneson, E., Wooddell, L. J., & Suomi, S. J. (2015). First-time rhesus monkey mothers, and mothers of sons, preferentially engage in face-to-face interactions with their infants. American Journal of Primatology. doi:10.1002/ajp.22503
  • Dettmer, A. M., Novak, M. A., Meyer, J. S., & Suomi, S. J. (2014). Population density dependent hair cortisol concentrations in rhesus monkeys (Macaca mulatta). Psychoneuroendocrinology, 42, 59–67. doi:10.1016/j.psyneuen.2014.01.002
  • Dettmer, A. M., Novak, M. A., Suomi, S. J., & Meyer, J. S. (2012). Physiological and behavioral adaptation to relocation stress in differentially reared rhesus monkeys: Hair cortisol as a biomarker for anxiety-related responses. Psychoneuroendocrinology, 37(2), 191–199. doi:10.1016/j.psyneuen.2011.06.003
  • Dettmer, A. M., Rosenberg, K. L., Suomi, S. J., Meyer, J. S., & Novak, M. A. (2015). Associations between parity, hair hormone profiles during pregnancy and lactation, and infant development in rhesus monkeys (Macaca mulatta). Plos One, 10(7), e0131692. doi:10.1371/journal.pone.0131692
  • Dettmer, A. M., Ruggiero, A. M., Novak, M. A., Meyer, J. S., & Suomi, S. J. (2008). Surrogate mobility and orientation affect the early neurobehavioral development of infant rhesus macaques (Macaca mulatta). Developmental Psychobiology, 50(4), 418–422. doi:10.1002/(ISSN)1098-2302
  • Dettmer, A. M., & Suomi, S. J. (2014). Nonhuman primate models of neuropsychiatric disorders: Influences of early rearing, genetics, and epigenetics. ILAR Journal, 55(2), 361–370. doi:10.1093/ilar/ilu025
  • DeVries, A. C., Glasper, E. R., & Detillion, C. E. (2003). Social modulation of stress responses. Physiology & Behavior, 79(3), 399–407. doi:10.1016/S0031-9384(03)00152-5
  • Dozier, M., Peloso, E., Lewis, E., Laurenceau, J.-P., & Levine, S. (2008). Effects of an attachment-based intervention on the cortisol production of infants and toddlers in foster care. Development and Psychopathology, 20(3), 845–859. doi:10.1017/S0954579408000400
  • Ebrecht, M., Hextall, J., Kirtley, L.-G., Taylor, A., Dyson, M., & Weinman, J. (2004). Perceived stress and cortisol levels predict speed of wound healing in healthy male adults. Psychoneuroendocrinology, 29(6), 798–809. doi:10.1016/S0306-4530(03)00144-6
  • Elo, A. (1978). The rating of chess players, past and present. New York, NY: Arco.
  • Fernald, L. C. H., & Gunnar, M. R. (2009). Poverty-alleviation program participation and salivary cortisol in very low-income children. Social Science & Medicine, 68(12), 2180–2189. doi:10.1016/j.socscimed.2009.03.032
  • Gunnar, M. R. (2000). Early adversity and the development of stress reactivity and regulation. The Effects of Early Adversity on Neurobehavioral Development, 31, 163–200.
  • Gunnar, M. R. (2003). Integrating neuroscience and psychological approaches in the study of early experiences. Proceedings of the National Academy of Sciences, 1008, 238–247. doi:10.1196/annals.1301.024
  • Gust, D. A., Gordon, T. P., Hambright, M. K., & Wilson, M. E. (1993). Relationship between social factors and pituitary-adrenocortical activity in female rhesus monkeys (Macaca mulatta). Hormones and Behavior, 27(3), 318–331. doi:10.1006/hbeh.1993.1024
  • Hackman, D. A., Betancourt, L. M., Brodsky, N. L., Hurt, H., & Farah, M. J. (2012). Neighborhood disadvantage and adolescent stress reactivity. Frontiers in Human Neuroscience, 6. doi:10.3389/fnhum.2012.00277
  • Hackman, D. A., Farah, M. J., & Meaney, M. J. (2010). Socioeconomic status and the brain: Mechanistic insights from human and animal research. Nature Reviews Neuroscience, 11(9), 651–659. doi:10.1038/nrn2897
  • Hennessy, M. B., Kaiser, S., & Sachser, N. (2009). Social buffering of the stress response: Diversity, mechanisms, and functions. Frontiers in Neuroendocrinology, 30(4), 470–482.
  • Hol, T., Van den Berg, C. L., Van Ree, J. M., & Spruijt, B. M. (1999). Isolation during the play period in infancy decreases adult social interactions in rats. Behavioural Brain Research, 100(1–2), 91–97. doi:10.1016/S0166-4328(98)00116-8
  • Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the HPA axis: A review of animal models and human studies across development. Psychological Bulletin, 140(1), 256–282. doi:10.1037/a0032671
  • Hunter, A. L., Minnis, H., & Wilson, P. (2011). Altered stress responses in children exposed to early adversity: A systematic review of salivary cortisol studies. Stress, 14(6), 614–626.
  • Kaplan, J. R., Manuck, S. B., Clarkson, T. B., Lusso, F. M., & Taub, D. M. (1982). Social status, environment, and atherosclerosis in cynomolgus monkeys. Arteriosclerosis, Thrombosis, and Vascular Biology, 2(5), 359–368. doi:10.1161/01.ATV.2.5.359
  • Langlois, É. V., Miszkurka, M., Zunzunegui, M. V., Ghaffar, A., Ziegler, D., & Karp, I. (2015). Inequities in postnatal care in low-and middle-income countries: A systematic review and meta-analysis. Bulletin of the World Health Organization, 93(4), 259–270G. doi:10.2471/BLT.14.140996
  • Li, L., Power, C., Kelly, S., Kirschbaum, C., & Hertzman, C. (2007). Life-time socio economic position and cortisol patterns in mid-life. Psychoneuroendocrinology, 32(7), 824–833. doi:10.1016/j.psyneuen.2007.05.014
  • Lovallo, W. R. (2013). Early life adversity reduces stress reactivity and enhances impulsive behavior: Implications for health behaviors. International Journal of Psychophysiology, 90(1), 8–16. doi:10.1016/j.ijpsycho.2012.10.006
  • Luecken, L. J., & Appelhans, B. M. (2006). Early parental loss and salivary cortisol in young adulthood: The moderating role of family environment. Development and Psychopathology, 18(01), 295–308. doi:10.1017/S0954579406060160
  • Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2001). Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status. Development and Psychopathology, 13(3), 653–676. doi:10.1017/S0954579401003133
  • 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 & Behavior, 96(4–5), 613–619. doi:10.1016/j.physbeh.2008.12.016
  • Marshall, I. J., Wang, Y., Crichton, S., McKevitt, C., Rudd, A. G., & Wolfe, C. D. (2015). The effects of socioeconomic status on stroke risk and outcomes. The Lancet Neurology, 14(12), 1206–1218. doi:10.1016/S1474-4422(15)00200-8
  • McCormack, K., Sanchez, M. M., Bardi, M., & Maestripieri, D. (2006). Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Developmental Psychobiology, 48(7), 537–550. doi:10.1002/(ISSN)1098-2302
  • McEwen, B. S. (2003). Early life influences on life-long patterns of behavior and health. Mental Retardation and Developmental Disabilities Research Reviews, 9(3), 149–154. doi:10.1002/(ISSN)1098-2779
  • McEwen, B. S. (2008). Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. European Journal of Pharmacology, 583(2–3), 174–185. doi:10.1016/j.ejphar.2007.11.071
  • McKinney, C. H., Antoni, M. H., Kumar, M., Tims, F. C., & McCabe, P. M. (1997). Effects of guided imagery and music (GIM) therapy on mood and cortisol in healthy adults. Health Psychology, 16(4), 390–400. doi:10.1037/0278-6133.16.4.390
  • McLaughlin, K. A., Breslau, J., Green, J. G., Lakoma, M. D., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2011). Childhood socio-economic status and the onset, persistence, and severity of DSM-IV mental disorders in a US national sample. Social Science & Medicine, 73(7), 1088–1096. doi:10.1016/j.socscimed.2011.06.011
  • Meaney, M. J., & Szyf, M. (2005). Environmental programming of stress responses through DNA methylation: Life at the interface between a dynamic environment and a fixed genome. Dialogues in Clinical Neuroscience, 7(2), 103–123.
  • Meyer, J. S., & Novak, M. A. (2012). Minireview: Hair cortisol: A novel biomarker of hypothalamic-pituitary-adrenocortical activity. Endocrinology, 153(9), 4120–4127. doi:10.1210/en.2012-1226
  • Miller, G. E., Chen, E., & Parker, K. J. (2011). Psychological stress in childhood and susceptibility to the chronic diseases of aging: Moving toward a model of behavioral and biological mechanisms. Psychological Bulletin, 137(6), 959–997. doi:10.1037/a0024768
  • Montez, J. K., & Hayward, M. D. (2014). Cumulative childhood adversity, educational attainment, and active life expectancy among US adults. Demography, 51(2), 413–435. doi:10.1007/s13524-013-0261-x
  • National Center for Health Statistics (US). (2012). Health, United States, 2011: With special feature on socioeconomic status and health. Hyattsville, MD: Author.
  • Neumann, C., Duboscq, J., Dubuc, C., Ginting, A., Irwan, A. M., Agil, M., … Engelhardt, A. (2011). Assessing dominance hierarchies: Validation and advantages of progressive evaluation with Elo-rating. Animal Behaviour, 82(4), 911–921. doi:10.1016/j.anbehav.2011.07.016
  • Novak, M. A., Hamel, A. F., Kelly, B. J., Dettmer, A. M., & Meyer, J. S. (2013). Stress the HPA axis, and nonhuman primate well-being: A review. Applied Animal Behaviour Science, 143(2–4), 135–149. doi:10.1016/j.applanim.2012.10.012
  • Oitzl, M. S., Champagne, D. L., van der Veen, R., & de Kloet, E. R. (2010). Brain development under stress: Hypotheses of glucocorticoid actions revisited. Neuroscience & Biobehavioral Reviews, 34(6), 853–866. doi:10.1016/j.neubiorev.2009.07.006
  • Palmer, F. B., Anand, K. J., Graff, J. C., Murphy, L. E., Qu, Y., Völgyi, E., … Tylavsky, F. A. (2013). Early adversity, socioemotional development, and stress in urban 1-year-old children. The Journal of Pediatrics, 163(6), 1733–1739. doi:10.1016/j.jpeds.2013.08.030
  • Power, C., & Hertzman, C. (1997). Social and biological pathways linking early life and adult disease. British Medical Bulletin, 53(1), 210–221. doi:10.1093/oxfordjournals.bmb.a011601
  • Rawlins, R. G., & Kessler, M. J. (1986). The Cayo Santiago macaques: History, behavior, and biology. Albany, NY: SUNY Press.
  • Russell, E., Koren, G., Rieder, M., & Van Uum, S. (2012). Hair cortisol as a biological marker of chronic stress: Current status, future directions and unanswered questions. Psychoneuroendocrinology, 37(5), 589–601. doi:10.1016/j.psyneuen.2011.09.009
  • Sapolsky, R. M. (2004). Social status and health in humans and other animals. Annual Review of Anthropology, 33, 393–418. doi:10.1146/annurev.anthro.33.070203.144000
  • Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308(5722), 648–652. doi:10.1126/science.1106477
  • Sapolsky, R. M., Alberts, S. C., & Altmann, J. (1997). Hypercortisolism associated with social subordinance or social isolation among wild baboons. Archives of General Psychiatry, 54(12), 1137–1143. doi:10.1001/archpsyc.1997.01830240097014
  • Schwartz, J. E., Friedman, H. S., Tucker, J. S., Tomlinson-Keasey, C., Wingard, D. L., & Criqui, M. H. (1995). Sociodemographic and psychosocial factors in childhood as predictors of adult mortality. American Journal of Public Health, 85(9), 1237–1245. doi:10.2105/AJPH.85.9.1237
  • Shannon, C., Champoux, M., & Suomi, S. J. (1998). Rearing condition and plasma cortisol in rhesus monkey infants. American Journal of Primatology, 46(4), 311–321. doi:10.1002/(ISSN)1098-2345
  • Shively, C. A., Laber-Laird, K., & Anton, R. F. (1997). Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biological Psychiatry, 41(8), 871–882. doi:10.1016/S0006-3223(96)00185-0
  • Smith, G. D. (1996). Down at heart–the meaning and implications of social inequalities in cardiovascular disease. Journal of the Royal College of Physicians of London, 31(4), 414–424.
  • Smith, G. D., Hart, C., Blane, D., Gillis, C., & Hawthorne, V. (1997). Lifetime socioeconomic position and mortality: Prospective observational study. Bmj, 314(7080), 547. doi:10.1136/bmj.314.7080.547
  • Smotherman, W. P., Hunt, L. E., McGinnis, L. M., & Levine, S. (1979). Mother-infant separation in group-living rhesus macaques: A hormonal analysis. Developmental Psychobiology, 12(3), 211–217.
  • Stevens, H. E., Leckman, J. F., Coplan, J. D., & Suomi, S. J. (2009). Risk and resilience: Early manipulation of macaque social experience and persistent behavioral and neurophysiological outcomes. Journal of the American Academy of Child & Adolescent Psychiatry, 48(2), 114–127. doi:10.1097/CHI.0b013e318193064c
  • Suomi, S. J. (1997). Early determinants of behaviour: Evidence from primate studies. British Medical Bulletin, 53(1), 170–184. doi:10.1093/oxfordjournals.bmb.a011598
  • Wiener, S. G., Johnson, D. F., & Levine, S. (1987). Influence of postnatal rearing conditions on the response of squirrel monkey infants to brief perturbations in mother-infant relationships. Physiology & Behavior, 39(1), 21–26.
  • Winslow, J. T., Noble, P. L., Lyons, C. K., Sterk, S. M., & Insel, T. R. (2003). Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology, 28(5), 910–918.
  • Wooddell, L. J., Kaburu, S. K., Dettmer, A. M., & Suomi, S. J. (2015, November). Elo rating as a tool to measure rank changes and dominance stability in semi free ranging rhesus macaques. American Journal of Primatology, 77(S1), 80.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.