Psychoneuroendocrinology
Volume 37, Issue 2 , Pages 191-199 , February 2012

Physiological and behavioral adaptation to relocation stress in differentially reared rhesus monkeys: Hair cortisol as a biomarker for anxiety-related responses

  • Amanda M. Dettmer

      Affiliations

    • Department of Psychiatry, University of Pittsburgh, 3811 O’Hara Street, Pittsburgh, PA, 15213, United States
    • Corresponding Author InformationCorresponding author. Tel.: +1 412 648 1266; fax: +1 412 648 1465.
  • ,
  • Melinda A. Novak

      Affiliations

    • Department of Psychology, University of Massachusetts Amherst, Amherst, MA, United States
  • ,
  • Stephen J. Suomi

      Affiliations

    • Laboratory of Comparative Ethology, Eunice Kennedy Shriver National Institute of Child Health & Human Development, NIH, Bethesda, MD, United States
  • ,
  • Jerrold S. Meyer

      Affiliations

    • Department of Psychology, University of Massachusetts Amherst, Amherst, MA, United States

Received 6 August 2010 ,Revised 19 April 2011 ,Accepted 1 June 2011.

References 

  1. Barrett CE, Noble P, Hanson E, Pine DS, Winslow JT, Nelson EE. Early adverse rearing experiences alter sleep-wake patterns and plasma cortisol levels in juvenile rhesus monkeys. Psychoneuroendocrinology. 2009;34:1029–1040
  2. Blumstein, D.T., Daniel, J.C., Evans, C.S., 2006. JWatcher (Version 1.0) [Software]. Available from http://www.jwatcher.ucla.edu.
  3. Capitanio JP, Mendoza SP, Mason WA, Maninger N. Rearing environment and hypothalamic–pituitary–adrenal regulations in young rhesus monkeys (Macaca mulatta). Dev. Psychobiol. 2005;46:318–330
  4. Clarke AS. Social rearing effects on HPA axis activity over early development and in response to stress in rhesus monkeys. Dev. Psychobiol. 1993;26:433–446
  5. Coplan JD, Andrews MW, Rosenblum LA, Owens MJ, Friedman S, Gorman JM, et al. Persistent elevations of cerebrospinal fluid concentrations of corticotrophin releasing hormone in adult nonhuman primates exposed to early life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc. Natl. Acad. Sci. 1996;93:1619–1623
  6. Davenport MD, Novak MA, Meyer JS, Tiefenbacher S, Higley JD, Lindell SG, et al. Continuity and change in emotional reactivity in rhesus monkeys throughout the prepubertal period. Motiv. Emotion. 2003;27:57–76
  7. Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS. Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen. Comp. Endocrinol. 2006;147:255–261
  8. Davenport MD, Lutz CK, Tiefenbacher S, Novak MA, Meyer JS. A rhesus monkey model of self-injury: effects of relocation stress on behavior and neuroendocrine function. Biol. Psychiatry. 2008;63:990–996
  9. Dettenborn L, Tietze A, Bruckner F, Kirschbaum C. Higher cortisol content in hair among long-term unemployed individuals compared to controls. Psychoneuroendocrinology. 2010;35:1404–1409
  10. Dettmer AM, Novak MFSX, Novak MA, Meyer JS, Suomi SJ. Hair cortisol predicts object permanence performance in infant rhesus macaques (Macaca mulatta). Dev. Psychobiol. 2009;51:706–713
  11. Erickson K, Gabry KE, Lindell S, Champoux M, Schulkin J, Gold P, et al. Social withdrawal behaviors in nonhuman primates and changes in neuroendocrine and monoamine concentrations during a separation paradigm. Dev. Psychobiol. 2005;46:331–339
  12. Fahlke C, Lorenz JG, Long J, Champoux M, Suomi S, Higley JD. Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcohol Clin. Exp. Res. 2000;24:644–650
  13. Francis DD, Caldji C, Champagne F, Plotsky PM, Meaney MJ. The role of corticotrophin-releasing factor—norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biol. Psychiatry. 1999;46:1153–1166
  14. Guazzo EP, Kirkpatrick PJ, Goodyer IM, Shiers HM, Herbert J. Cortisol, dehydroepiandrosterone (DHEA), and DHEA sulfate in the cerebrospinal fluid of man: relation to blood levels and the effects of age. J. Clin. Endocrinol. Metab. 1996;81:3951–3960
  15. Hansen EW. The development of maternal and infant behavior in the rhesus monkey. Behaviour. 1966;27:107–149
  16. Harlow HF. Age-mate or peer affectional system. Adv. Study Behav. 1969;2:333–353
  17. Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry. 2001;49:1023–1039
  18. Higley JD, Suomi SJ. Temperamental reactivity in non-human primates. In:  Kohnstamm G,  Bates JE,  Rothbart MK editor. Temperament in Childhood. New York: Wiley & Sons; 1989;p. 153–167
  19. Higley JD, Suomi SJ, Linnoila M. Serotonin in nonhuman primates: gender, rearing and developmental correlates with behavioral timidity and affective psychopathology. In:  Coccaro EF,  Murphy DL editor. Serotonin in Major Psychiatric Disorders. Washington, DC: American Psychiatric Press, Inc.; 1990;p. 27–46
  20. Higley JD, Suomi SJ, Linnoila M. CSF monamine metabolite concentrations vary according to age, rearing, and sex, and are influenced by the stressor of social separation in rhesus monkeys. Psychopharmacology. 1991;103:551–556
  21. Higley JD, Suomi SJ, Linnoila M. A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol. Psychiatry. 1992;32:127–145
  22. Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology. 2001;158:366–373
  23. Kalra S, Einarson A, Karaskov T, Van Uum S, Koren G. The relationship between stress and hair cortisol in healthy pregnant women. Clin. Invest. Med. 2007;30:E103–E107
  24. Karere GM, Kinnally EL, Sanchez JN, Famula TR, Lyons LA, Capitanio JP. What is an “adverse” environment? Interactions of rearing experiences and MAOA genotype in rhesus monkeys. Biol. Psychiatry. 2009;65:770–777
  25. Kirschbaum C, Tietze A, Skoluda N, Dettenborn L. Hair as a retrospective calendar of cortisol production—increased cortisol incorporation into hair in the third trimester of pregnancy. Psychoneuroendocrinology. 2009;34:32–37
  26. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experiences. Prog. Brain Res. 2000;122:81–103
  27. Lewis M, Ramsay DS. Developmental change in infants’ responses to stress. Child Dev. 1995;66:50–59
  28. Maestripieri D, Martel FL, Nevison CM, Simpson MJA, Keverne EB. Anxiety in rhesus monkey infants in relation to interactions with their mother and other social companions. Dev. Psychobiol. 1991;24:571–581
  29. Meyer JS, Novak MA, Bowman RE, Harlow HF. Behavioral and hormonal effects of attachment object separation in surrogate-peer-reared and mother-reared infant rhesus monkeys. Dev. Psychobiol. 1975;8:425–435
  30. Nelson EE, Herman KN, Barrett CE, Noble PL, Wojteczko K, Chisholm K, et al. Adverse rearing experiences enhance responding to both aversive and rewarding stimuli in juvenile rhesus monkeys. Biol. Psychiatry. 2009;66:702–704
  31. Novak MA, O’Neill P, Suomi SJ. Adjustments and adaptations to indoor and outdoor environments: continuity and change in young adult rhesus monkeys. Am. J. Primatol. 1992;28:125–138
  32. Parr LA, Winslow JT, Davis M. Rearing experience differentially affects somatic and cardiac startle responses in rhesus monkeys (Macaca mulatta). Behav. Neurosci. 2002;116:378–386
  33. Ruppenthal GC. Survey of protocols for nursery rearing infant macaques. In:  Ruppenthal GC,  Reese DJ editor. Nursery Care of Nonhuman Primates. New York: Plenum Press; 1979;p. 165–185
  34. Ruppenthal GC, Walker CG, Sackett GP. Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages. Am. J. Primatol. 1991;25:103–113
  35. Sackett GP. Can single processes explain effects of postnatal influences on primate development?. In:  Emde RN,  Harmon R J editor. The Development of Attachment and Affiliative Systems. New York: Plenum Press; 1982;p. 3–12
  36. Sackett GP, Ruppenthal GC, Davis AE. Survival, growth, health, and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina). Am. J. Primatol. 2002;56:165–183
  37. Sauvé B, Koren G, Walsh G, Tokmakejian S, Van Uum SHM. Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin. Invest. Med. 2007;30:E183–E191
  38. Shannon C, Champoux M, Suomi SJ. Rearing condition and plasma cortisol in rhesus monkey infants. Am. J. Primatol. 1998;46:311–321
  39. Stevens H, Leckman JF, Coplan JD, Suomi SJ. Risk and resilience: early manipulation of macaque social experience and persistent behavioral and neurophysiological outcomes. J. Am. Acad. Child Adolesc. Psychiatry. 2009;48:114–127
  40. Strand SC, Novak MA. Examination of behavior in differently reared monkeys housed together. Am. J. Primatol. 2005;66(S1):120–121
  41. Suomi SJ. Genetic, maternal and environmental influences on social development in rhesus monkeys. In:  Chiarelli AB,  Corruccini RS editor. Primate Behavior and Sociobiology. New York: Springer-Verlag; 1981;p. 81–87
  42. Suomi SJ. Early stress and adult emotional reactivity in rhesus monkeys. Ciba Found. Symp. 1991;156:171–183
  43. Suomi SJ. Early determinants of behaviour: evidence from primate studies. Br. Med. Bull. 1997;53:170–184
  44. Thomson S, Koren G, Fraser L-A, Rieder M, Friedman TC, Van Uum SHM. Hair analysis provides a historical record of cortisol levels in Cushing's syndrome. Exper. Clin. Endocr. Diab. 2010;118:133–138
  45. Tukey JW. Exploratory Data Analysis. Behavioral Science-Quantitative Methods. MA: Addison-Wesley, Reading; 1977;
  46. Winslow JT, Noble PL, Lyons CK, Sterk SM, Insel TR. Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology. 2003;28:910–918
  47. Yamada J, Stevens B, de Silva N, Gibbins S, Beyene J, Taddio A, et al. Hair cortisol as a potential biologic marker of chronic stress in hospitalized neonates. Neonatology. 2007;92:42–49

PII: S0306-4530(11)00172-7

doi: 10.1016/j.psyneuen.2011.06.003

Psychoneuroendocrinology
Volume 37, Issue 2 , Pages 191-199 , February 2012