Hormonal and behavioral responses to stress in lactating and non-lactating female common marmosets (Callithrix jacchus)

Physiology and Behavior

Volumn 104, Issue 3, 2011, Pages 446-453

  Saltzman, Wendy ^a,b   Abbott, David H ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Adrenocorticotropic hormone; Cortisol; Lactation; Maternal care; Parental care; Stress

Indexed keywords

CORTICOTROPIN; HYDROCORTISONE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; CALLITRICHINAE; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; FEMALE; FOLLICULAR PHASE; HORMONE RESPONSE; HYDROCORTISONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; LACTATION; LUTEAL PHASE; MENSTRUAL CYCLE; NONHUMAN; OVARY CYCLE; PRIORITY JOURNAL; PUERPERIUM; REPRODUCTION; STRESS;

ADRENOCORTICOTROPIC HORMONE; ANALYSIS OF VARIANCE; ANIMALS; CALLITHRIX; FEMALE; HAWKS; HYDROCORTISONE; LACTATION; POSTPARTUM PERIOD; PREGNANCY; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 79959858590     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.05.005     Document Type: Article

References (55)

1. Ricklefs R.E., Wikelski M. The physiology/life-history nexus. Trends Ecol Evol 2002, 17:462-468.
2. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. J Neuroendocrinol 2003, 15:711-724.
3. Breuner C.W., Patterson S.H., Hahn T.P. In search of relationships between the acute adrenocortical response and fitness. Gen Comp Endocrinol 2008, 157:288-295.
4. 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, 21:55-89.
5. Bókony V., Lendvai A.Z., Liker A., Angelier F., Wingfield J.C., Chastel O. Stress response and the value of reproduction: are birds prudent parents?. Am Nat 2009, 173:589-598.
6. Lightman S.L., Windle R.J., Wood S.A., Kershaw Y.M., Shanks N., Ingram C.D. Peripartum plasticity within the hypothalamo-pituitary-adrenal axis. Prog Brain Res 2001, 133:111-129.
7. Tu M.T., Lupien S.J., Walker C.-D. Measuring stress responses in postpartum mothers: perspectives from studies in human and animal populations. Stress 2005, 8:19-34.
8. Lightman S.L., Young W.S. Lactation inhibits stress-mediated secretion of corticosterone and oxytocin and hypothalamic accumulation of corticotropin-releasing factor and enkephalin messenger ribonucleic acids. Endocrinology 1989, 124:2358-2364.
9. Walker C.-D., Tilders F.J.H., Burlet A. Increased colocalization of corticotropin-releasing factor and arginine vasopressin in paraventricular neurones of the hypothalamus in lactating rats: evidence from immunotargeted lesions and immunohistochemistry. J Neuroendocrinol 2001, 13:74-85.
10. Walker C.-D., Toufexis D.J., Burlet A. Hypothalamic and limbic expression of CRF and vasopressin during lactation: implications for the control of ACTH secretion and stress hyporesponsiveness. Prog Brain Res 2001, 133:99-110.
11. Thoman E.B., Conner R.L., Levine S. Lactation suppresses adrenal corticosteroid activity and aggressiveness in rats. J Comp Physiol Psychol 1970, 3:364-369.
12. Fleming A.S., Luebke C. Timidity prevents the virgin female rat from being a good mother: emotionality differences between nulliparous and parturient females. Physiol Behav 1981, 27:863-868.
13. Hard E., Hansen S. Reduced fearfulness in the lactating rat. Physiol Behav 1985, 35:641-643.
14. Ferreira A., Hansen S., Nielsen M., Archer T., Minor B.G. Behavior of mother rats in conflict tests sensitive to antianxiety agents. Behav Neurosci 1989, 103:193-201.
15. Kellogg C.K., Barrett K.A. Reduced progesterone metabolites are not critical for plus-maze performance of lactating female rats. Pharmacol Biochem Behav 1999, 63:441-448.
16. Toufexis D.J., Rochford J., Walker C.D. Lactation-induced reduction in rats' acoustic startle is associated with changes in noradrenergic neurotransmission. Behav Neurosci 1999, 113:176-184.
17. Neumann I.D. Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depress Anxiety 2003, 17:111-121.
18. Lonstein J.S. Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones. Horm Behav 2005, 47:241-255.
19. Deschamps S., Woodside B., Walker C.-D. Pups presence eliminates the stress hyporesponsiveness of early lactating females to a psychological stress representing a threat to the pups. J Neuroendocrinol 2003, 15:486-497.
20. Slattery D.A., Neumann I.D. No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 2008, 586:377-385.
21. Hubbs A.H., Millar J.S., Wiebe J.P. Effect of brief exposure to a potential predator on cortisol concentrations in female Columbian ground squirrels (Spermophilus columbianus). Can J Zool 2000, 78:578-587.
22. Hill P.D., Chatterton R.T., Aldag J.C. Neuroendocrine responses to stressors in lactating and nonlactating mammals: a literature review. Biol Res Nurs 2003, 5:79-86.
23. Reeder D.M., Kunz T.H., Widmaier E.P. Baseline and stress-induced glucocorticoids during reproduction in the variable flying fox, Pteropus hypomelanus (Chiroptera: Pteropodidae). J Exp Zool A Comp Exp Biol 2004, 301:682-690.
24. Tilbrook A.J., Turner A.I., Ibbott M.D., Clarke I.J. Activation of the hypothalamo-pituitary-adrenal axis by isolation and restraint stress during lactation in ewes: effect of the presence of the lamb and suckling. Endocrinology 2006, 147:3501-3509.
25. Brunton P.J., Russell J.A., Douglas A.J. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 2008, 20:764-766.
26. Douglas A.J., Brunton P.J., Bosch O.J., Russell J.A., Neumann I.D. Neuroendocrine responses to stress in mice: hyporesponsiveness in pregnancy and parturition. Endocrinology 2003, 144:5268-5276.
27. Maestripieri D., Hoffman C.L., Fulks R., Gerald M.S. Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Horm Behav 2008, 53:170-176.
28. Hoffman C.L., Ayala J.E., Mas-Rivera A., Maestripieri D. Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free-ranging female rhesus macaques. Am J Primatol 2010, 72:559-565.
29. Tardif S.D., Smucny D.A., Abbott D.H., Mansfield K., Schultz-Darken N., Yamamoto M.E. Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 2003, 53:364-368.
30. Arruda M.F., Araújo A., Sousa M.B.C., Albuquerque F.S., Albuquerque A.C.S.R., Yamamoto M.E. Two breeding females in free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatol 2005, 76:10-20.
31. Digby LJ, Ferrari SF, Saltzman W. Callitrichines: the role of competition in cooperatively breeding species. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger M, Bearder SK, editors. Primates in perspective, New York: Oxford University Press; 2007, p. 85-106.
32. McNeilly A.S., Abbott D.H., Lunn S.F., Chambers P.C., Hearn J.P. Plasma prolactin concentrations during the ovarian cycle and lactation and their relationship to return of fertility post partum in the common marmoset (Callithrix jacchus). J Reprod Fertil 1981, 62:353-360.
33. Tardif S.D., Jaquish C.E. Number of ovulations in the marmoset monkey (Callithrix jacchus): relation to body weight, age and repeatability. Am J Primatol 1997, 42:323-329.
34. Tardif S.D., Carson R.L., Gangaware B.L. Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus). Am J Primatol 1986, 11:103-110.
35. Ximenes M.F.F.M., Sousa M.B.C. Family composition and the characteristics of parental care during the nursing phase of captive common marmosets (Callithrix jacchus). Primates 1996, 37:175-183.
36. Saltzman W., Abbott D.H. Effects of elevated circulating cortisol concentrations on maternal behavor in common marmost monkeys (Callithrix jacchus). Psychoneuroendocrinology 2009, 34:1222-1234.
37. Saltzman W, Boettcher CA, Post JL, Abbott DH. Inhibition of maternal behaviour by central infusion of corticotrophin-releasing hormone in marmoset monkeys (Callithrix jacchus). J Neuroendocrinol in press.
38. Hearn J.P. Restraining device for small monkeys. Lab Anim 1977, 11:261-262.
39. Saltzman W., Schultz-Darken N.J., Scheffler G., Wegner F.H., Abbott D.H. Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiol Behav 1994, 56:801-810.
40. Orth D.N. Adrenocorticotropic hormone (ACTH). Methods of hormone radioimmunoassay 1979, 245-278. Academic Press, New York. 2nd edition. B.M. Jaffe, H.R. Behrman (Eds.).
41. Blumstein D.T., Daniel J.C. Quantifying behavior the JWatcher way 2007, Sinauer, Sunderland, MA.
42. Baker J.V., Abbott D.H., Saltzman W. Social determinants of reproductive failure in malecommon marmosets housed with their natal family. Anim Behav 1999, 58:501-513.
43. Saltzman W., Prudom S.L., Schultz-Darken N.J., Wittwer D.J., Abbott D.H. Social suppression of cortisol in female marmoset monkeys: role of circulating ACTH levels and glucocorticoid negative feedback. Psychoneuroendocrinology 2004, 29:141-161.
44. Harlow C.R., Gems S., Hodges J.K., Hearn J.P. The relationship between plasma progesterone and the timing of ovulation and early embryonic development in the marmoset monkey (Callithrix jacchus). J Zool 1983, 201:273-282.
45. Summers P.M., Wennink C.J., Hodges J.K. Cloprostenol-induced luteolysis in the marmoset monkey (Callithrix jacchus). J Reprod Fertil 1985, 73:133-138.
46. Saltzman W., Schultz-Darken N.J., Wegner F.H., Wittwer D.J., Abbott D.H. Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Horm Behav 1998, 33:58-74.
47. Heinrichs M., Meinlschmidt G., Neumann I., Wagner S., Kirschbaum C., Ehlert U., et al. Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J Clin Endocrinol Metab 2001, 86:4798-4804.
48. Kaye J., Soothill P., Hunt M., Lightman S. Responses to the 35% CO2 challenge in postpartum women. Clin Endocrinol 2004, 61:582-588.
49. Walker C.D., Trottier G., Rochford J., Lavallée D. Dissociation between behavioral and hormonal responses to the forced swim stress in lactating rats. J Neuroendocrinol 1995, 7:615-622.
50. Chiodera P., Salvarani C., Bacchi-Modena A., Spallanzani R., Cigarini C., Alboni A., et al. Relationship between plasma profiles of oxytocin and adrenocorticotropic hormone during suckling or breast stimulation in women. Horm Res 1991, 35:119-123.
51. Amico J.A., Johnston J.M., Vagnucci A.H. Suckling-induced attenuation of plasma cortisol concentrations in postpartum lactating women. Endocr Res 1994, 20:79-87.
52. Atkinson H.C., Waddell B.J. The hypothalamic-pituitary-adrenal axis in rat pregnancy and lactation: circadian variation and interrelationship of plasma adrenocorticotropin and corticosterone. Endocrinology 1995, 136:512-520.
53. Rima B.N., Bardi M., Friedenberg J.M., Christon L.M., Karelina K.E., Lambert K.G., et al. Reproductive experience and the response of female Sprague-Dawley rats to fear and stress. Comp Med 2009, 59:437-443.
54. Lankarani-Fard A., Kritz-Silverstein D., Barrett-Connor E., Goodman-Gruen D. Cumulative duration of breast-feeding influences cortisol levels in postmenopausal women. J Womens Health Gend Based Med 2001, 10:681-687.
55. Federenko I.S., Wolf J.M., Wüst S., Schlotz W., Hellhammer J., Kudielka B.M., et al. Parity does not alter baseline or stimulated activity of the hypothalamus-pituitary-adrenal axis in women. Dev Psychobiol 2006, 48:703-711.