Stress During Gestation Alters Postpartum Maternal Care and the Development of the Offspring in a Rodent Model

Biological Psychiatry

Volumn 59, Issue 12, 2006, Pages 1227-1235

  Champagne, Frances A ^a   Meaney, Michael J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

gestational stress; Maternal; medial preoptic area; oxytocin receptor

Indexed keywords

CORTICOSTERONE; OXYTOCIN RECEPTOR;

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; BREEDING; CHILD DEVELOPMENT; COMPARATIVE STUDY; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FEMALE; FETUS OUTCOME; GENOMICS; GROOMING; LACTATION; LICKING; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MATING; MOTHER; MOTHER CHILD RELATION; NEUROENDOCRINE SYSTEM; NEWBORN; NONHUMAN; PARENTAL BEHAVIOR; PREGNANCY; PRIORITY JOURNAL; PROGENY; PUERPERIUM; RAT; RECEPTOR BINDING; REGULATORY MECHANISM; STRESS;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CORTICOSTERONE; DISEASE MODELS, ANIMAL; FEMALE; GROOMING; MATERNAL BEHAVIOR; POSTPARTUM PERIOD; PREGNANCY; RATS; RATS, LONG-EVANS; RECEPTORS, OXYTOCIN; STRESS, PSYCHOLOGICAL;

EID: 33745476901     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2005.10.016     Document Type: Article

References (64)

1. Ammerman R.T., Cassisi J.E., Hersen M., and van Hasselt V.B. Consequences of physical abuse and neglect in children. Clin Psychol Rev 6 (1986) 291-310
2. Bauer M.K., Harding J.E., Bassett N.S., Breier B.H., Oliver M.H., Gallaher B.H., et al. Fetal growth and placental function. Mol Cell Endocrinol 140 (1998) 115-120
3. Belzung C., and Griebel G. Measuring normal and pathological anxiety-like behavior in mice. A review. Behav Brain Res 125 (2001) 141-149
4. Berman C.M. Intergenerational transmission of maternal rejection rates among free-ranging rheus monkeys on Cayo Santiago. Anim Behav 44 (1990) 247-258
5. Bifulco A., Moran P.M., Ball C., Jacobs C., Baines R., Bunn A., et al. Childhood adversity, parental vulnerability and disorder. Examining inter-generational transmission of risk. J Child Psychol Psychiatry 43 (2002) 1075-1086
6. Brown G.R., and Anderson B. Psychiatric morbidity in adult inpatients with childhood histories of sexual and physical abuse. Am J Psychiatry 148 (1993) 55-61
7. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P., and Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 95 (1998) 5335-5340
8. Champagne F., Diorio J., Sharma S., and Meaney M.J. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98 (2001) 12736-12741
9. Champagne F., and Meaney M.J. Like mother, like daughter. evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133 (2001) 287-302
10. Champagne F.A., Francis D.D., Mar A., and Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79 (2003) 359-371
11. Chapillon P., Patin V., Roy V., Vincent A., and Caston J. Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents. a review. Dev Psychobiol 41 (2002) 373-387
12. Conger R.D., Ge X., Elder Jr. G.H., Lorenz F.O., and Simons R.L. Economic stress, coercive family process, and developmental problems of adolescents. Child Dev 65 (1994) 541-561
13. Coplan J.D., Andrews M.W., Rosenblum L.A., Owens M.J., Friedman S., Gorman J.M., et al. Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors. Implications for the pathophysiology of mood and anxiety disorders. Proc Natl Acad Sci U S A 93 (1996) 1619-1623
14. Coplan J.D., Trost R.C., Owens M.J., Cooper T.B., Gorman J.M., Nemeroff C.B., et al. Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Arch Gen Psychiatry 55 (1998) 473-477
15. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9 (1985) 37-44
16. Darnaudery M., Dutriez I., Viltart O., Morley-Fletcher S., and Maccari S. Stress during gestation induces lasting effects on emotional reactivity of the dam rat. Behav Brain Res 153 (2004) 211-216
17. De Bellis M.D. Developmental traumatology. A contributory mechanism for alcohol and substance use disorders. Psychoneuroendocrinology 27 (2002) 155-170
18. Eisenberg L., and Earls F.J. Poverty, social depreciation and child development. In: Hamburg D.A. (Ed). Handbook of Psychiatry, vol. 6 (1975), Basic Books, New York 275-291
19. Fahrbach S.E., Morrell J.I., and Pfaff D.W. Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40 (1985) 526-532
20. Fairbanks L.A. Early experience and cross-generational continuity of mother-infant contact in vervet monkeys. Dev Psychobiol 22 (1989) 669-681
21. Farrington D.P., Gallagher B., Morley L., St Ledger R.J., and West D.J. Are there any sucessful men from criminogenic backgrounds?. Psychiatry 51 (1988) 116-130
22. Feehan M., McGee R., Stanton W.R., and Silva P.A. Strict and inconsistent discipline in childhood. Consequences for adolescent mental health. Br J Clin Psychol 30 (1991) 325-331
23. Field T. Maternal depression effects on infants and early interventions. Prev Med 27 (1998) 200-203
24. Fleming A.S., and Corter C. Factors influencing maternal responsiveness in humans. Usefulness of an animal model. Psychoneuroendocrinology 13 (1988) 189-212
25. Francis D.D., Champagne F.C., and Meaney M.J. Variations in maternal behavior are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12 (2000) 1145-1148
26. Francis D.D., Diorio J., and Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286 (1999) 1155-1158
27. Fride E., and Weinstock M. The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat. Dev Psychobiol 17 (1984) 651-660
28. Haapasalo J., and Tremblay R.E. Physically aggressive boys from ages 6 to 12. Family background, parenting behavior, and prediction of delinquency. J Consult Clin Psychol 62 (1994) 1044-1052
29. Hales C.N., and Barker D.J. Type 2 (non-insulin-dependent) diabetes mellitus. The thrifty phenotype hypothesis. Diabetologia 35 (1992) 595-601
30. Heim C., Newport D.J., Heit S., Graham Y.P., Wilcox M., Bonsall R., et al. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284 (2000) 592-597
31. Hirshfeld D.R., Biederman J., Brody L., Faraone S.V., and Rosenbaum J.F. Associations between expressed emotion and child behavioral inhibition and psychopathology. A pilot study. J Am Acad Child Adolesc Psychiatry 36 (1997) 205-213
32. Hirshfeld D.R., Biederman J., Brody L., Faraone S.V., and Rosenbaum J.F. Expressed emotion toward chidren with behavioral inhibition. Associations with maternal anxiety disorder. J Am Acad Child Adolesc Psychiatry 36 (1997) 910-917
33. Holmes S.J., and Robins L.N. The role of parental disciplinary practices in the development of depression and alcoholism. Psychiatry 51 (1988) 24-36
34. Ijzendoorn M.H. Intergenerational transmission of parenting. A review of studies in nonclinical populations. Dev Rev 12 (1991) 76-99
35. Insel T.R., and Shapiro L.E. Oxytocin receptors and maternal behavior. Ann N Y Acad Sci 652 (1992) 122-141
36. Krey L.C., Lu K.H., Bulter W.R., Hotchkiss J., Piva F., and Knobil E. Surgical disconnection of the medial basal hypothalamus and pituitary function in the rhesus monkey. II. GH and cortisol secretion. Endocrinology 96 (1975) 1088-1093
37. Kuhn C.M., and Schanberg S.M. Responses to maternal separation. Mechanisms and mediators. Int J Dev Neurosci 16 (1998) 261-270
38. Levine S. Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiol Behav 73 (2001) 255-260
39. Liberzon I., and Young E.A. Effects of stress and glucocorticoids on CNS oxytocin receptor binding. Psychoneuroendocrinology 22 (1997) 411-422
40. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1659-1662
41. Lyons D.M., Kim S., Schatzberg A.F., and Levine S. Postnatal foraging demands alter adrenocortical activity and psychosocial development. Dev Psychobiol 32 (1998) 285-291
42. Maxfield M.G., and Widom C.S. The cycle of violence. Revisited 6 years later. Arch Pediatr Adolesc Med 150 (1996) 390-395
43. McLoyd V.C. The impact of economic hardship on black families and children. Psychological distress, parenting, and socioemotional development. Child Dev 61 (1990) 311-346
44. McLoyd V.C. Socioeconomic disadvantage and child development. Am Psychol 53 (1998) 185-204
45. McLoyd V.C., and Wilson L. Maternal behavior, social support, and economic conditions as predictors of distress in children. New Dir Child Dev 46 (1990) 49-69
46. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24 (2001) 1161-1192
47. Miller L., Kramer R., Warner V., Wickramaratne P., and Weissman M. Intergenerational transmission of parental bonding among women. J Am Acad Child Adolesc Psychiatry 36 (1997) 1134-1139
48. Moore C.L., and Power K.L. Prenatal stress affects mother-infant interaction in Norway rats. Dev Psychobiol 19 (1986) 235-245
49. Myers M.M., Brunelli S.A., Squire J.M., Shindeldecker R.D., and Hoffer M.A. Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 22 (1989) 29-53
50. Neel J.V. Diabetes mellitus. A "thrifty" genotype rendered detrimental by "progress" ?. Bull World Health Organ 77 (1999) 694-703
51. Neumann I.D. Alterations in behavioural and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. Prog Brain Res 133 (2001) 143-152
52. Numan M., and Callahan E.C. The connections of the medial preoptic region and maternal behavior in the rat. Physiol Behav 25 (1980) 653-665
53. Patchev V.K., Schlosser S.F., Hassan A.H., and Almeida O.F. Oxytocin binding sites in rat limbic and hypothalamic structures. Site-specific modulation by adrenal and gonadal steroids. Neuroscience 57 (1993) 537-543
54. Pedersen C.A., and Boccia M.L. Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress 5 (2002) 259-267
55. Quirce C.M., Odio M., and Solano J.M. The effects of predictable and unpredictable schedules of physical restraint upon rats. Life Sci 28 (1981) 1897-1902
56. Rosenblatt J.S. Psychobiology of maternal behavior. Contribution to the clinical understanding of maternal behavior among humans. Acta Paediatr Suppl 397 (1994) 3-8
57. Rosenblum L.A., and Andrews M.W. Influences of environmental demand on maternal behavior and infant development. Acta Paediatr Suppl 397 (1994) 57-63
58. Seckl J.R., Nyirenda M.J., Walker B.R., and Chapman K.E. Glucocorticoids and fetal programming. Biochem Soc Trans 27 (1999) 74-78
59. Swanson L.W. Brain Maps. Structure of the Rat Brain (1992), Elsevier, Amsterdam
60. Trickett P.K., and McBride-Chang C. The developmental impact of different forms of child abuse and neglect. Dev Rev 15 (1995) 311-337
61. Unvas-Moberg K., Johansson B., Lupoli B., and Svennersten-Sjaunja K. Oxytocin facilitates behavioral, metabolic and physiological adaptations during lactation. Appl Anim Behav Sci 72 (2001) 225-234
62. Weinstock M., Fride E., and Hertzberg R. Prenatal stress effects on functional development of the offspring. Prog Brain Res 73 (1988) 319-331
63. West M.J., and King A.P. Setting nature and nurture into an ontogenetic niche. Dev Psychobiol 20 (1987) 549-562
64. Whipple E.E., and Webster-Stratton C. The role of parental stress in physically abusive families. Child Abuse Negl 15 (1991) 279-291