Stress reactivity in young marmosets (Callithrix geoffroyi): Ontogeny, stability, and lack of concordance among co-twins

Hormones and Behavior

Volumn 61, Issue 2, 2012, Pages 196-203

  French, Jeffrey A ^a   Smith, Adam S ^a   Gleason, Angela M ^a   Birnie, Andrew K ^a   Mustoe, Aaryn ^a   Korgan, Austin ^a  

^a UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

Author keywords

Area under the curve; Marmoset; Stability; Stress reactivity; Trait; Urinary cortisol

Indexed keywords

HYDROCORTISONE;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; AREA UNDER THE CURVE; ARTICLE; CALLITHRIX GEOFFROYI; CALLITRICHINAE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; HYDROCORTISONE URINE LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; JUVENILE; MALE; MENTAL STRESS; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; STRESS; TWIN CONCORDANCE;

ANIMALS; AREA UNDER CURVE; CALLITHRIX; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LITTER SIZE; PITUITARY-ADRENAL SYSTEM; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 84862816782     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.12.006     Document Type: Article

References (72)

1. Baker J.V., Abbott D.H., Saltzman W. Social determinants of reproductive failure in male common marmosets housed with their natal family. Anim. Behav. 1999, 58(3):501-513.
2. Barr C.S., Newman T.K., Shannon C., Parker C., Dvoskin R.L., Becker M.L., Schwandt M., Champoux M., Lesch K.P., Goldman D., Suomi S.J., Higley J.D. Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biol. Psychiatry 2004, 55(7):733-738.
3. Benirschke K. The biology of the twinning process: how placentation influences outcome. Semin. Perinatol. 1995, 19(5):342-350.
4. Berger M., Bossert S., Krieg J.C., Dirlich G., Ettmeier W., Schreiber W., von Zerssen D. Interindividual differences in the susceptibility of the cortisol system: an important factor for the degree of hypercortisolism in stress situations?. Biol Psychiatry 1987, 22(11):1327-1339.
5. Birnie A.K., Smith A.S., Nali C., French J.A. Social and developmental influences on urinary androgen levels in young male white-faced marmosets (Callithrix geoffroyi). Am. J. Primatol. 2011, 73(4):378-385.
6. Boyce W.T., Ellis B.J. Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev. Psychopathol. 2005, 17(2):271-301.
7. Capitanio J.P., Mendoza S.P., Lerche N.W. Individual differences in peripheral blood immunological and hormonal measures in adult male rhesus macaques (Macaca mulatta): evidence for temporal and situational consistency. Am. J. Primatol. 1998, 44(1):29-41.
8. Carere C., Groothuis T., Möstl E., Daan S., Koolhaas J. Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm. Behav. 2003, 43(5):540-548.
9. Chrousos G.P., Renquist D., Brandon D., Eil C., Pugeat M., Vigersky R., Cutler G.B., Loriaux D.L., Lipsett M.B. Glucocorticoid hormone resistance during primate evolution: receptor-mediated mechanisms. Proc. Natl. Acad. Sci. U. S. A. 1982, 79(6):2036-2040.
10. Coe C.L., Savage A., Bromley L.J. Phylogenetic influences on hormone levels across the primate order. Am. J. Primatol. 1992, 28(2):81-100.
11. Cohen S., Hamrick N.M.S., Rodriguez M.S., Feldman P.J., Rabin B.S., Manuck S.B. The stability of and intercorrelations among cardiovascular, immune, endocrine, and psychological reactivity. Ann. Behav. Med. 2000, 22(3):171-179.
12. Davis E.P., Granger D.A. Developmental differences in infant salivary alpha-amylase and cortisol responses to stress. Psychoneuroendocrinology 2009, 34(6):795-804.
13. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19(3):269-301.
14. DeRijk R.H., de Kloet E.R., Zitman F.G., van Leeuwen N. Mineralocorticoid receptor gene variants as determinants of HPA axis regulation and behavior. Endocr. Dev. 2011, 20:137-148.
15. Dettling A.C., Feldon J., Pryce C.R. Repeated parental deprivation in the infant common marmoset (Callithrix jacchus, primates) and analysis of its effects on early development. Biol. Psychiatry 2002, 52(11):1037-1046.
16. Dettling A.C., Feldon J., Pryce C.R. Early deprivation and behavioral and physiological responses to social separation/novelty in the marmoset. Pharmacol. Biochem. Behav. 2002, 73(1):259-269.
17. Dettling A.C., Schnell C.R., Maier C., Feldon J., Pryce C.R. Behavioral and physiological effects of an infant-neglect manipulation in a bi-parental, twinning primate: impact is dependent on familial factors. Psychoneuroendocrinology 2007, 32(4):331-349.
18. DeVries A.C., Craft T.K., Glasper E.R., Neigh G.N., Alexander J.K. 2006 Curt P. Richter award winner: social influences on stress responses and health. Psychoneuroendocrinology 2007, 32(6):587-603.
19. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004, 130(3):355-391.
20. Diorio J., Meaney M.J. Maternal programming of defensive responses through sustained effects on gene expression. J. Psychiatry Neurosci. 2007, 32(4):275-284.
21. Ellis B.J., Jackson J.J., Boyce W.T. The stress response systems: universality and adaptive individual differences. Dev. Rev. 2006, 26(2):175-212.
22. Evans M.R., Roberts M.L., Buchanan K.L., Goldsmith A.R. Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. J. Evol. Biol. 2006, 19(2):343-352.
23. Federenko I.S., Nagamine M., Hellhammer D.H., Wadhwa P.D., Wüst S. The heritability of hypothalamus pituitary adrenal axis responses to psychosocial stress is context dependent. J. Clin. Endocrinol. Metab. 2004, 89(12):6244.
24. Fevolden S.E., Refstie T., Roed K.H. Selection for high and low cortisol stress response in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). Aquaculture 1991, 95(1-2):53-65.
25. Filippini, K.M., French, J.A., in preparation. Onset of reproductive function in female marmosets living in family groups.
26. Fite J.E., French J.A., Patera K.J., Hopkins E.C., Rukstalis M., Jensen H.A., Ross C.N. Nighttime wakefulness associated with infant rearing in Callithrix kuhlii. Int. J. Primatol. 2003, 24(6):1267-1280.
27. Flinn M.V. Are cortisol profiles a stable trait during child development?. Am. J. Hum. Biol. 2009, 21(6):769-771.
28. Flinn M.V., Nepomnaschy P.A., Muehlenbein M.P., Ponzi D. Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neurosci. Biobehav. Rev. 2011, 35(7):1611-1629.
29. French J.A., Brewer K.J., Schaffner C.M., Schalley J., Hightower Merritt D., Smith T.E., Bell S.M. Urinary steroid and gonadotropin excretion across the reproductive cycle in female Wied's black tufted ear marmosets (Callithrix kuhli). Am. J. Primatol. 1996, 40(3):231-245.
30. Gunnar M.R., Donzella B. Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 2002, 27(1-2):199-220.
31. Gunnar M.R., Quevedo K.M. Early care experiences and HPA axis regulation in children: a mechanism for later trauma vulnerability. Prog. Brain Res. 2008, 167:137-149.
32. Gunnar M.R., Wewerka S., Frenn K., Long J.D., Griggs C. Developmental changes in hypothalamus-pituitary-adrenal activity over the transition to adolescence: normative changes and associations with puberty. Dev. Psychopathol. 2009, 21(01):69-85.
33. Hamer M., Gibson E.L., Vuononvirta R., Williams E., Steptoe A. Inflammatory and hemostatic responses to repeated mental stress: individual stability and habituation over time. Brain Behav. Immun. 2006, 20(5):456-459.
34. Hellhammer J., Fries E., Schweisthal O., Schlotz W., Stone A., Hagemann D. Several daily measurements are necessary to reliably assess the cortisol rise after awakening: state-and trait components. Psychoneuroendocrinology 2007, 32(1):80-86.
35. Higley J.D., Suomi S.J., Linnoila M. A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol. Psychiatry 1992, 32(2):127-145.
36. Jabbi M., Korf J., Kema I., Hartman C., Van der Pompe G., Minderaa R., Ormel J., Den Boer J. Convergent genetic modulation of the endocrine stress response involves polymorphic variations of 5-HTT, COMT and MAOA. Mol. Psychiatry 2007, 12(5):483-490.
37. Johnson E.O., Kamilaris T.C., Carter S., Gold P.W., Chrousos G.P. Environmental stress and reproductive success in the common marmoset (Callithrix jacchus jacchus). Am. J. Primatol. 1991, 25(3):191-201.
38. Johnson E.O., Kamilaris T.C., Carter C.S., Calogero A.E., Gold P.W., Chrousos G.P. The biobehavioral consequences of psychogenic stress in a small, social primate (Callithrix jacchus jacchus). Biol. Psychiatry 1996, 40(5):317-337.
39. Kirschbaum C., Steyer R., Eid M., Patalla U., Schwenkmezger P., Hellhammer D. Cortisol and behavior: 2. Application of a latent state-trait model to salivary cortisol. Psychoneuroendocrinology 1990, 15(4):297-307.
40. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 2005, 69(1):113.
41. Law A.J., Pei Q., Walker M., Gordon-Andrews H., Weickert C.S., Feldon J., Pryce C.R., Harrison P.J. Early parental deprivation in the marmoset monkey produces long-term changes in hippocampal expression of genes involved in synaptic plasticity and implicated in mood disorder. Neuropsychopharmacology 2008, 34(6):1381-1394.
42. Leung E., Tasker S.L., Atkinson L., Vaillancourt T., Schulkin J., Schmidt L.A. Perceived maternal stress during pregnancy and its relation to infant stress reactivity at 2 days and 10 months of postnatal life. Clin. Pediatr. (Phila) 2010, 49(2):158.
43. Lilly A.A., Mehlman P.T., Higley J.D. Trait like immunological and hematological measures in female rhesus across varied environmental conditions. Am. J. Primatol. 1999, 48(3):197-223.
44. McCormack K., Newman T.K., Higley J.D., Maestripieri D., Sanchez M.M. Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Horm. Behav. 2009, 55(4):538-547.
45. Modell S., Lauer C.J., Schreiber W., Huber J., Krieg J.C., Holsboer F. Hormonal response pattern in the combined DEX-CRH test is stable over time in subjects at high familial risk for affective disorders. Neuropsychopharmacology 1998, 18(4):253-262.
46. Ouellet-Morin I., Boivin M., Dionne G., Lupien S.J., Arsenault L., Barr R.G., Pèrusse D., Tremblay R.E. Variations in heritability of cortisol reactivity to stress as a function of early familial adversity among 19-month-old twins. Arch. Gen. Psychiatry 2008, 65(2):211.
47. Overli O., Winberg S., Pottinger T.G. Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout - a review. Integr. Comp. Biol. 2005, 45(3):463-474.
48. Parker K.J., Maestripieri D. Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates. Neurosci. Biobehav. Rev. 2011, 35(7):1466-1483.
49. Préville M., Zarit S., Susman E., Boulenger P., Lehoux R. Response variability of salivary cortisol among older adults under psychological stress. Aging Ment. Health 2008, 12:249-257.
50. Pruessner J.C., Kirschbaum C., Meinlschmid G., Hellhammer D.H. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 2003, 28(7):916-931.
51. Pryce C.R., Palme R., Feldon J. Development of pituitary-adrenal endocrine function in the marmoset monkey: infant hypercortisolism is the norm. J. Clin. Endocrinol. Metab. 2002, 87(2):691.
52. Pryce C.R., Feldon J., Fuchs E., Knuesel I., Oertle T., Sengstag C., Spengler M., Weber E., Weston A., Jongen-Relo A. Postnatal ontogeny of hippocampal expression of the mineralocorticoid and glucocorticoid receptors in the common marmoset monkey. Eur. J. Neurosci. 2005, 21(6):1521-1535.
53. Roman O., Seres J., Pometlova M., Jurcovicova J. Neuroendocrine or behavioral effects of acute or chronic emotional stress in Wistar Kyoto (WKY) and spontaneously hypertensive (SHR) rats. Endocr. Regul. 2004, 38(4):151-155.
54. Rukstalis M., French J.A. Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Horm. Behav. 2005, 47(1):1-7.
55. Saltzman W., Schultz Darken N.J., Abbott D.H. Familial influences on ovulatory function in common marmosets (Callithrix jacchus). Am. J. Primatol. 1997, 41(3):159-177.
56. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. Rev. 1986, 11(1):65-76.
57. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21(1):55-89.
58. Schaffner C.M., Shepherd R.E., Santos C.V., French J.A. Development of heterosexual relationships in Wied's black tufted ear marmosets (Callithrix kuhli). Am. J. Primatol. 1995, 36(3):185-200.
59. Smith T.E., French J.A. Social and reproductive conditions modulate urinary cortisol excretion in black tufted ear marmosets (Callithrix kuhli). Am. J. Primatol. 1997, 42(4):253-267.
60. Smith T.E., French J.A. Psychosocial stress and urinary cortisol excretion in marmoset monkeys. Physiol. Behav. 1997, 62(2):225-232.
61. Smith T.E., Schaffner C.M., French J.A. Social and developmental influences on reproductive function in female Wied's black tufted-ear marmosets (Callithrix kuhli). Horm. Behav. 1997, 31(2):159-168.
62. Smith T.E., McGreer-Whitworth B., French J.A. Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (Callithrix kuhli). Horm. Behav. 1998, 34(3):211-222.
63. Smith A.S., Birnie A.K., French J.A. Social isolation affects partner-directed social behavior and cortisol during pair formation in marmosets, Callithrix geoffroyi. Physiol. Behav. 2011, 104:955-961.
64. Steptoe A., van Jaarsveld C.H.M., Semmler C., Plomin R., Wardle J. Heritability of daytime cortisol levels and cortisol reactivity in children. Psychoneuroendocrinology 2009, 34(2):273-280.
65. Tasker J.G. Rapid glucocorticoid actions in the hypothalamus as a mechanism of homeostatic integration. Obesity (Silver Spring) 2006, 14(Suppl. 5):259S-265S.
66. Thorn L., Hucklebridge F., Evans P., Clow A. The cortisol awakening response, seasonality, stress and arousal: a study of trait and state influences. Psychoneuroendocrinology 2009, 34(3):299-306.
67. Touma C., Bunck M., Glasl L., Nussbaumer M., Palme R., Stein H., Wolferstatter M., Zeh R., Zimbelmann M., Holsboer F., Landgraf R. Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology 2008, 33(6):839-862.
68. Uhart M., McCaul M., Oswald L., Choi L., Wand G. GABRA6 gene polymorphism and an attenuated stress response. Mol. Psychiatry 2004, 9(11):998-1006.
69. Walker C.D., Perrin M., Vale W., Rivier C. Ontogeny of the stress response in the rat: role of the pituitary and the hypothalamus. Endocrinology 1986, 118(4):1445.
70. Watson S., Thompson J.M., Malik N., Nicol Ferrier I., Young A.H. Temporal stability of the dex/CRH test in patients with rapid cycling bipolar I disorder: a pilot study. Aust. N. Z. J. Psychiatry 2005, 39(4):244-248.
71. Wust S., Federenko I., Hellhammer D.H., Kirschbaum C. Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrinology 2000, 25(7):707-720.
72. Yamamoto M.E. From dependence to sexual maturity: the behavioural ontogeny of Callitrichidae. Marmosets and Tamarins: Systematics, Behaviour and Ecology 2003, 235-250. Oxford University Press, Oxford. A.B. Rylands (Ed.).