Maternal care and development of stress responses in baboons

American Journal of Primatology

Volumn 66, Issue 3, 2005, Pages 263-278

  Bardi, Massimo ^a   Bode, Anne E ^a   Ramirez, Stephanie M ^a   Brent, Linda Y ^a  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Cortisol; HPA axis; Maternal behavior; Papio hamadryas; Stress response

Indexed keywords

HYDROCORTISONE;

BEHAVIORAL RESPONSE; ENDOCRINE SYSTEM; MATERNAL CARE; PRIMATE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BLOOD; COMPARATIVE STUDY; FEMALE; MALE; MATERNAL BEHAVIOR; OBSERVATION; PAPIO; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; RADIOIMMUNOASSAY; REGRESSION ANALYSIS; SOCIAL DOMINANCE; STRESS;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; HIERARCHY, SOCIAL; HYDROCORTISONE; MALE; MATERNAL BEHAVIOR; OBSERVATION; PAPIO; RADIOIMMUNOASSAY; REGRESSION ANALYSIS; STRESS;

PAPIO; PAPIO HAMADRYAS;

EID: 24944476082     PISSN: 02752565     EISSN: None     Source Type: Journal    
DOI: 10.1002/ajp.20143     Document Type: Article

References (75)

1. Amico JA, Mantella RC, Vollmer RR, Li X. 2004. Anxiety and stress responses in female oxytocin deficient mice. J Neuroendocrinol 16:319-324.
2. Avitsur R, Stark JL, Dhabhar FS, Kramer KA, Sheridan JF. 2003. Social experience alters the response to social stress in mice. Brain Behav Immunol 17:426-437.
3. Bardi M, Shimizu K, Fujita S, Borgognini-Tarli S, Huffman MA. 2001. Hormonal correlates of maternal style in captive macaques (Macaca fuscata and M. mulatta). Int J Primatol 22:647-662.
4. Bardi M, Huffman MA. 2002. Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata). Dev Psychobiol 41:364-372.
5. Bardi M, Shimizu K, Barrett GM, Borgognini-Tarli SM, Huffman MA. 2003a. Peripartum cortisol levels and mother-infant interactions in Japanese macaques. Am J Phys Anthropol 120:298-304.
6. Bardi M, Shimizu K, Barrett GM, Borgognini-Tarli SM, Huffman MA. 2003b. Peripartum sex steroid changes and maternal style in rhesus and Japanese macaques. Gen Comp Endocrinol 133:323-331.
7. Bardi M, French JA, Ramirez SR, Brent L. 2004. The role of the endocrine system in baboon maternal behavior. Biol Psychiatry 55:724-732.
8. Barnett SA, Burn J. 1967. Early stimulation and maternal behaviour. Nature 213:150-152.
9. Barr CS, Newman TK, Becker ML, Parker CC, Champoux M, Lesch KP, Goldman D, Suomi SJ, Higley JD. 2003. The utility of the non-human primate; model for studying gene by environment interactions in behavioral research. Genes Brain Behav 2:336-340.
10. Barr CS, Newman TK, Schwandt M, Shannon C, Dvoskin RL, Lindell SG, Taubman J, Thompson B, Champoux M, Lesch KP, Goldman D, Suomi SJ, Higley JD. 2004. Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proc Natl Acad Sci USA 101:12358-12363.
11. Bethea CL, Streicher JM, Coleman K, Pau FK, Moessner R, Cameron JL. 2004. Anxious behavior and fenfluramine-induced prolactin secretion in young rhesus macaques with different alleles of the serotonin reuptake transporter polymorphism (5HTTLPR). Behav Genet 34:295-307.
12. Bhatnagar S, Meaney MJ. 1995. Hypothalamic-pituitary-adrenal function in chronic intermittently cold-stressed neonatally handled and non handled rats. J Neuroendocrinol 7:97-108.
13. Boccia ML, Laudenslager ML, Reite ML. 1994. Intrinsic and extrinsic factors affect infant responses to maternal separation. Psychiatry 57:43-50.
14. Boccia ML, Roberts JE. 2000. Behavior and autonomic nervous system function assessed via heart period measures: the case of hyperarousal in boys with fragile X syndrome. Behav Res Methods Instrum Comput 32:5-10.
15. Bremner JD, Vermetten E. 2001. Stress and development: behavioral and biological consequences. Dev Psychopathol 13:473-489.
16. Brent L, Koban T, Ramirez S. 2002. Abnormal, abusive, and stress-related behaviors in baboon mothers. Biol Psychiatry 52:1046-1056.
17. Brent L, Koban T, Evans S. 2003. The influence of temperature on the behavior of captive mother-infant baboons. Behaviour 140:209-224.
18. Cannon WB. 1929. Bodily changes in pain, hunger, fear, and rage. New York: Appleton. 404 p.
19. Champagne FA, Francis DD, Mar A, Meaney MJ. 2003a. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359-371.
20. Champagne FA, Weaver IC, Diorio J, Sharma S, Meaney MJ. 2003b. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144:4720-4724.
21. Champoux M, Bennett A, Shannon C, Higley JD, Lesch KP, Suomi SJ. 2002. Serotonin transporter genetic polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol Psychiatry 7:1058-1063.
22. Drolet G, Dumont EC, Gosselin I, Kinkead R, Laforest S, Trottier JF. 2001. Role of endogenous opioid system in the regulation of the stress response. Prog Neuropsychopharmacol Biol Psychiatry 25:729-741.
23. Fairbanks LA, McGuire MT. 1988. Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev Psychobiol 21:711-724.
24. Fairbanks LA. 1996. Individual differences in maternal style, causes and consequences for mothers and offspring. Adv Stud Behav 25:579-611.
25. Francis DD, Meaney MJ. 1999. Maternal care and the development of stress responses. Curr Opin Neurobiol 9:128-134.
26. Franz C. 1999. Allogrooming behavior and grooming site preferences in captive bonobos (Pan paniscus): association with female dominance. Int J Primatol 20:525-546.
27. French JA, Brewer KJ, Shaffner CM, Schaliey J, Hightower-Merritt DL, et al. 1996. Urinary steroid and gonadotropin excretion across the reproductive cycle in females Wied's black tufted-ear marmosets (Callithrix kuhili). Am J Primatol 40:231-245.
28. French JA, Koban T, Rukstalis M, Ramirez SM, Bardi M, Brent L. 2004. Excretion of urinary steroids in pre- and postpartum female baboons (Papio hamadryas anubis sp.). Gen Comp Endocrinol 137:69-77.
29. Gerra G, Monti D, Panerai AE, Sacerdote P, Anderlini R, Avanzini P, Zaimovic A, Brambilla F, Franceschi C. 2003. Long-term immune-endocrine effects of bereavement: relationships with anxiety levels and mood. Psychiatry Res 121:145-158.
30. Gilmer WS, McKinney WT. 2003. Early experience and depressive disorders: human and non-human primate studies. J Affect Disord 75:97-113.
31. Gue M, Bravard A, Meunier J, Veyrier R, Gaillet S, Recasens M, Maurice T. 2004. Sex differences in learning deficits induced by prenatal stress in juvenile rats. Behav Brain Res 150:149-157.
32. Heim C, Nemeroff CB. 2001. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023-1039.
33. Hendrickx AG. 1965. The menstrual cycle of the baboon as determined by the vaginal smear, vaginal biopsy, and perineal swelling. In: Vagtborg H, editor. The baboon in medical research. Vol. II. Austin, TX: University of Texas Press. p 70-83.
34. Huffman LC, Bryan YE, del Carmen R, Pedersen FA, Doussard-Roosevelt JA, Porges SW. 1998. Infant temperament and cardiac vagal tone: assessments at twelve weeks of age. Child Dev 69:624-635.
35. Insel TR, O'Brien DJ, Leckman JF. 2002. Oxytocin, vasopressin, and autism: is there a connection? In: Cacioppo JT, Benton GG, Adolphs R, Carter CS, Davidson RJ, McClintock MK, McEwen BS, Meaney MJ, Schacter DJ, Sternberg EM, Suomi SS, Taylor SE, editors. Foundation in social neuroscience. Cambridge: MIT Press. p 695-711.
36. Jansen A, Nguyen XV, Karpitskiy V, Mettenleiter T, Loewy AD. 1995. Central command neurons of the sympathetic nervous system: basis of the fight-or-flight response. Science 270:644-646.
37. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. 2000. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122:81-103.
38. Levine S, Mody T. 2003. The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey. Neurosci Biobehav Rev 27:83-89.
39. Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ. 2000. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12:5-12.
40. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. 2002. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. In: Cacioppo JT, Benton GG, Adolphs R, Carter CS, Davidson RJ, McClintock MK, McEwen BS, Meaney MJ, Schacter DJ, Sternberg EM, Suomi SS, Taylor SE, editors. Foundation in social neuroscience. Cambridge: MIT Press. p 755-761.
41. Maestripieri D, Martel FL, Nevison CM, Simpson MJ, Keverne EB. 1991. Anxiety in rhesus monkey infants in relation to interactions with their mother and other social companions. Dev Psychobiol 24:571-581.
42. Maestripieri D. 1999. The biology of human parenting: insights from nonhuman primates. Neurosci Biobehav Rev 23:411-422.
43. Manly BFJ. 1994. Multivariate statistical methods. London: Chapman & Hall. 159 p.
44. Martel FL, Nevison CM, Simpson MJ, Keverne EB. 1995. Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. Dev Psychobiol 28:71-84.
45. Mason J. 1975. A historical view of the stress field. J Hum Stress 1:6-21.
46. McEwen BS. 2003. Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 9:149-154.
47. Meaney MJ, Aitken DH. 1985. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res 354:301-304.
48. Miller GM, Bendor J, Tiefenbacher S, Yang H, Novak MA, Madras BK. 2004. A muopioid receptor single nucleotide polymorphism in rhesus monkey: association with stress response and aggression. Mol Psychiatry 9:99-108.
49. Mormede P, Courvoisier H, Ramos A, Marissal-Arvy N, Ousova O, Desautes C, Duclos M, Chaouloff F, Moisan MP. 2002. Molecular genetic approaches to investigate individual variations in behavioral and neuroendocrine stress responses. Psychoneuroendocrinology 27:563-583.
50. National Research Council. 1996. Guide for the care and use of laboratory animals. Washington DC: National Academic Press. 125 p.
51. Newport DJ, Stowe ZN, Nemeroff CB. 2002. Parental depression: animal models of an adverse life event. Am J Psychiatry 159:1265-1283.
52. Penke Z, Felszeghy K, Fernette B, Sage D, Nyakas C, Burlet A. 2001. Postnatal maternal deprivation produces long-lasting modifications of the stress response, feeding and stress-related behaviour in the rat. Eur J Neurosci 14:747-755.
53. Porges SW. 2003. The polyvagal theory: phylogenetic contributions to social behavior. Physiol Behav 79:503-513.
54. Pryce CR. 1996. Socialization, hormones, and the regulation of maternal behavior in nonhuman simian primates. Adv Stud Behav 25:423-473.
55. Pryce CR, Palme R, Feldon J. 2002. Development of pituitary-adrenal endocrine function in the marmoset monkey: infant hypercortisolism is the norm. J Clin Endocrinol Metab 87:691-699.
56. Rendall D, Cheney DL, Seyfarth RM. 2000. Proximate factors mediating "contact" calls in adult female baboons (Papio cynocephalus ursinus) and their infants. J Comp Psychol 114:36-46.
57. Roske I, Baeger I, Frenzel R, Oehme P. 1994. Does a relationship exist between the quality of stress and the motivation to ingest alcohol? Alcohol 11:113-124.
58. Sanchez MM, Ladd CO, Plotsky PM. 2001. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13:419-449.
59. Sapolsky RM. 1998. Why zebras don't get ulcers: a guide to stress. New York: W.H. Freeman. 434 p.
60. Sapolsky RM. 2002. The endocrinology of the stress-response. In: Becker B, Breedlove MS, Crews D, McCarthy MM, editors. Behavioral endocrinology. Cambridge: MIT Press. p 409-450.
61. Schmidt M, Okimoto DK, Dent GW, Gordon MK, Levine S. 2002. Maternal regulation of the hypothalamic-pituitary-adrenal axis in the 20-day-old rat: consequences of laboratory weaning. J Neuroendocrinol 14:450-457.
62. Schwartz CE, Wright CI, Shin LM, Kagan J, Rauch SL. 2003. Inhibited and uninhibited infants "grown up": adult amygdalar response to novelty. Science 300:1952-1953.
63. Selye H. 1976. The stress of life. New York: McGraw-Hill. 515 p.
64. Simpson MJA. 1985. Effects of early experience on the behaviour of yearling rhesus monkey (Macaca mulatta) in the presence of a strange object: classification and correlation approaches. Primates 26:57-72.
65. Simpson MJA. 1988. How rhesus monkey mothers and infants keep in touch when infants are at risk from social companions. Int J Primatol 9:257-274.
66. Statsoft Inc. 1998. STATISTICA for Windows [computer program manual]. Tulsa, OK: Statsoft Inc. 140 p.
67. Sumova A, Jakoubek B. 1989. Analgesia and impact induced by anticipation stress: involvement of the endogenous opioid peptide system. Brain Res 503:273-280.
68. Vallee M, Mayo W, Maccari S, Le Moal M, Simon H. 1996. Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res 712:287-292.
69. Virgolini MB, Volosin M, Fulginiti AS, Cancela LM. 2004. Amphetamine and stress responses in developmentally lead-exposed rats. Neurotoxicol Teratol 26:291-303.
70. Weaver A, de Waal F. 2002. An index of relationship quality based on attachment theory. J Comp Psychol 116:93-106.
71. Weaver A, de Waal F. 2003. The mother-offspring relationship as a template in social development: reconciliation in captive brown capuchins (Cebus apella). J Comp Psychol 117:101-110.
72. Weaver ICG, Grant RJ, Meaney MJ. 2002. Maternal behavior regulates long-term hippocampal expression of BAX and apoptosis in the offspring. J Neurochem 82:998-1002.
73. Weiner H. 1992. Perturbing the organism: the biology of stressful experience. Chicago: University of Chicago Press. 357 p.
74. Williamson DE, Coleman K, Bacanu SA, Devlin BJ, Rogers J, Ryan ND, Cameron JL. 2003. Heritability of fearful-anxious endophenotypes in infant rhesus macaques: a preliminary report. Biol Psychiatry 53:284-291.
75. Zucker EL, Clarke MR. 1998. Agonistic and affiliative relationships of adult female howlers (Alouatta palliata) in Costa Rica over a 4-year period. Int J Primatol 19:433-449.