Developmental plasticity of HPA and fear responses in rats: A critical review of the maternal mediation hypothesis

Hormones and Behavior

Volumn 50, Issue 5, 2006, Pages 667-680

  Macrì, Simone ^a   Würbel, Hanno ^b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

ACTH; Corticosterone; Developmental plasticity; Early handling; HPA axis; Maternal behavior; Maternal care; Maternal separation; Phenotypic plasticity; Postnatal manipulations

Indexed keywords

GLUCOCORTICOID;

ANIMAL EXPERIMENT; BRAIN REGION; DIET RESTRICTION; DOWN REGULATION; FEAR; FEMALE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MATERNAL BEHAVIOR; MATERNAL CARE; MATERNAL DEPRIVATION; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; REVIEW; STRESS;

ANIMALS; ANIMALS, NEWBORN; ENVIRONMENT; FEAR; FEMALE; HANDLING (PSYCHOLOGY); HOUSING, ANIMAL; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MATERNAL BEHAVIOR; MATERNAL DEPRIVATION; MODELS, PSYCHOLOGICAL; NEURONAL PLASTICITY; PHENOTYPE; PITUITARY-ADRENAL SYSTEM; RATS; STRESS;

EID: 33750954402     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2006.06.015     Document Type: Review

References (93)

1. Barnett S.A., and Burn J. Early stimulation and maternal behaviour. Nature 213 (1967) 150-152
2. Bateson P., Barker D., Clutton-Brock T., Deb D., D'Udine B., Foley R.A., Gluckman P., Godfrey K., Kirkwood T., Lahr M.M., McNamara J., Metcalfe N.B., Monaghan P., Spencer H.G., and Sultan S.E. Developmental plasticity and human health. Nature 430 (2004) 419-421
3. Bell R.W., Nitschke W., Bell N.J., and Zachman T.A. Early experience, ultrasonic vocalizations, and maternal responsiveness in rats. Dev. Psychobiol. 7 (1974) 235-242
4. Bredy T.W., Humpartzoomian R.A., Cain D.P., and Meaney M.J. Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience 118 (2003) 571-576
5. Bredy T.W., Zhang T.Y., Grant R.J., Diorio J., and Meaney M.J. Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression. Eur. J. Neurosci. 20 (2004) 1355-1362
6. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., 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
7. Caldji C., Francis D., Sharma S., Plotsky P.M., and Meaney M.J. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22 (2000) 219-229
8. Calhoun J.B. Population density and social pathology. Sci. Am. 206 (1962) 139-148
9. Cameron N.M., Champagne F.A., Parent C., Fish E.W., Ozaki-Kuroda K., and Meaney M.J. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci. Biobehav. Rev. 29 (2005) 843-865
10. Catalani A., Marinelli M., Scaccianoce S., Nicolai R., Muscolo L.A., Porcu A., Koranyi L., Piazza P.V., and Angelucci L. Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance. Brain Res. 624 (1993) 209-215
11. Catalani A., Casolini P., Scaccianoce S., Patacchioli F.R., Spinozzi P., and Angelucci L. Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience 100 (2000) 319-325
12. 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
13. 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
14. De Kloet E.R., Oitzl M.S., and Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci. 22 (1999) 422-426
15. Denenberg V.H., Hudgens G.A., and Zarrow M.X. Mice reared with rats: modification of behavior by early experience with another species. Science 143 (1964) 380-381
16. Denenberg V.H., Rosenberg K.M., Paschke R., and Zarrow M.X. Mice reared with rat aunts: effects on plasma corticosterone and open field activity. Nature 221 (1969) 73-74
17. Dobzhansky T. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teach. 35 (1973) 127-129
18. Dufty Jr. A.M., Clobert J., and Moller A.P. Hormones, developmental plasticity and adaptation. Trends Ecol. Evol. 17 (2002) 190-196
19. Farrington D.P., Gallagher B., Morley L., St Ledger R.J., and West D.J. Are there any successful men from criminogenic backgrounds?. Psychiatry 51 (1988) 116-130
20. Fish E.W., Shahrokh D., Bagot R., Caldji C., Bredy T., Szyf M., and Meaney M.J. Epigenetic programming of stress responses through variations in maternal care. Ann. N. Y. Acad. Sci. 1036 (2004) 167-180
21. Francis D.D., and Meaney M.J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 9 (1999) 128-134
22. Francis D., Diorio J., Liu D., and Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286 (1999) 1155-1158
23. Francis D.D., Champagne F.C., and Meaney M.J. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J. Neuroendocrinol. 12 (2000) 1145-1148
24. Francis D.D., Diorio J., Plotsky P.M., and Meaney M.J. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 22 (2002) 7840-7843
25. Gluckman P.D., Hanson M.A., Spencer H.G., and Bateson P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc. Biol. Sci. 272 (2005) 671-677
26. Graham Y.P., Heim C., Goodman S.H., Miller A.H., and Nemeroff C.B. The effects of neonatal stress on brain development: implications for psychopathology. Dev. Psychopathol. 11 (1999) 545-565
27. 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
28. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 12 (1998) 129-162
29. Heim C., and Nemeroff C.B. The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biol. Psychiatry 46 (1999) 1509-1522
30. Heim C., and Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49 (2001) 1023-1039
31. Heim C., Owens M.J., Plotsky P.M., and Nemeroff C.B. Persistent changes in corticotropin-releasing factor systems due to early life stress: relationship to the pathophysiology of major depression and post-traumatic stress disorder. Psychopharmacol. Bull. 33 (1997) 185-192
32. Heim C., Newport D.J., Bonsall R., Miller A.H., and Nemeroff C.B. Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. Am. J. Psychiatry 158 (2001) 575-581
33. Henderson N.D. Genetic influences on the behavior of mice can be obscured by laboratory rearing. J. Comp. Physiol. Psychol. 72 (1970) 505-511
34. Hofer M.A. Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology 21 (1996) 203-217
35. Houston A.I., and McNamara J.M. Phenotypic plasticity as a state-dependent life-history decision. Evol. Ecol. 6 (1992) 243-253
36. Huot R.L., Thrivikraman K.V., Meaney M.J., and Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berlin) 158 (2001) 366-373
37. Jans J.E., and Woodside B.C. Nest temperature: effects on maternal behavior, pup development, and interactions with handling. Dev. Psychobiol. 23 (1990) 519-534
38. Lee M.H., and Williams D.I. Long term changes in nest condition and pup grouping following handling of rat litters. Dev. Psychobiol. 8 (1975) 91-95
39. Lee M.H., and Williams D.I. A longitudinal study of mother-young teraction in the rat: the effects of infantile stimulation, diurnal rhythms, and pup maturation. Behaviour 63 (1977) 241-261
40. Lehmann J., and Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev. Neurosci. 11 (2000) 383-408
41. Levine S. Infantile experience and resistance to physiological stress. Science 126 (1957) 405
42. Levine S. Plasma-free corticosterone response to electric shock in rats stimulated in infancy. Science 135 (1962) 795-796
43. Levine S. Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 405 (2000) 149-160
44. Levine S. Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiol. Behav. 73 (2001) 255-260
45. Levine S., and Lewis G.W. Critical period for effects of infantile experience on maturation of stress response. Science 129 (1959) 42-43
46. Levine S., Chevalier J.A., and Korchin S.J. The effects of early shock and handling on later avoidance learning. J. Pers. 24 (1956) 475-493
47. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., and Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1659-1662
48. Liu D., Caldji C., Sharma S., Plotsky P.M., and Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J. Neuroendocrinol. 12 (2000) 5-12
49. Macri, S., 2005. Effects of environmental modulation of rat maternal care on the expression of stress and fear responses in adult offspring. PhD Thesis, ETH Collection, Number 16131, p. 1-133. Available online at http://e-collection.ethbib.ethz.ch/ecol-pool/diss/fulltext/eth16131.pdf.
50. Macri, S., Würbel, H., in press. Effects of variation in postnatal maternal environment on maternal behaviour and fear and stress responses in rats. Anim. Behav.
51. Macri S., Mason G.J., and Würbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur. J. Neurosci. 20 (2004) 1017-1024
52. McCormick C.M., Kehoe P., and Kovacs S. Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int. J. Dev. Neurosci. 16 (1998) 175-185
53. McEwen B.S. Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840 (1998) 33-44
54. 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
55. Meaney M.J., and Szyf M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin. Neurosci. 7 (2005) 103-123
56. Meaney M.J., Aitken D.H., van Berkel C., Bhatnagar S., and Sapolsky R.M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239 (1988) 766-768
57. Meier G.W., and Schutzman L.H. Mother-infant interactions and experimental manipulation: confounding or misidentification?. Dev. Psychobiol. 1 (1968) 141-145
58. Mirescu C., Peters J.D., and Gould E. Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci. 7 (2004) 841-846
59. Moles A., Rizzi R., and D'Amato F.R. Postnatal stress in mice: does "stressing" the mother have the same effect as "stressing" the pups?. Dev. Psychobiol. 44 (2004) 230-237
60. Nemeroff C.B. The corticotropin-releasing factor (CRF) hypothesis of depression: new findings and new directions. Mol. Psychiatry 1 (1996) 336-342
61. Ohta H., Honma S., Abe H., and Honma K. Periodic absence of nursing mothers phase-shifts circadian rhythms of clock genes in the suprachiasmatic nucleus of rat pups. Eur. J. Neurosci. 17 (2003) 1628-1634
62. Parfitt D.B., Levin J.K., Saltstein K.P., Klayman A.S., Greer L.M., and Helmreich D.L. Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res. 1016 (2004) 111-118
63. Parker K.J., Buckmaster C.L., Sundlass K., Schatzberg A.F., and Lyons D.M. Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 3000-3005
64. Penza K.M., Heim C., and Nemeroff C.B. Neurobiological effects of childhood abuse: implications for the pathophysiology of depression and anxiety. Arch. Women Ment. Health 6 (2003) 15-22
65. Plotsky P.M., and Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 18 (1993) 195-200
66. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., and Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30 (2005) 2192-2204
67. Pryce C.R., and Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 27 (2003) 57-71
68. Pryce C.R., Bettschen D., and Feldon J. Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev. Psychobiol. 38 (2001) 239-251
69. Rampon C., Tang Y.P., Goodhouse J., Shimizu E., Kyin M., and Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3 (2000) 238-244
70. Richards M.P.M. Infantile handling in rodents: a reassessment in the light of recent studies of maternal behaviour. Anim. Behav. 14 (1966) 582
71. Rosenblatt J.S. Psychobiology of maternal behavior: contribution to the clinical understanding of maternal behavior among humans. Acta Paediatr. Suppl. 397 (1994) 3-8
72. Ruedi-Bettschen D., Feldon J., and Pryce C.R. Circadian- and temperature-specific effects of early deprivation on rat maternal care and pup development: short-term markers for long-term effects?. Dev. Psychobiol. 45 (2004) 59-71
73. Sapolsky R.M. Why Zebras Don't Get Ulcers (2004), Henry Holt and Company
74. Schaefer Jr. T., Weingarten F.S., and Towne J.C. Temperature change: the basic variable in the early handling phenomenon?. Science 135 (1962) 41-42
75. Schmidt M.V., Levine S., Oitzl M.S., van der Mark M., Muller M.B., Holsboer F., and de Kloet E.R. Glucocorticoid receptor blockade disinhibits pituitary-adrenal activity during the stress hyporesponsive period of the mouse. Endocrinology 146 (2005) 1458-1464
76. Seckl J.R., and Meaney M.J. Early life events and later development of ischaemic heart disease. Lancet 342 (1993) 1236
77. Sih A. Prey uncertainty and the balancing of antipredator and feeding needs. Am. Nat. 139 (1992) 1052-1069
78. Sih A. A behavioral ecological view of phenotypic plasticity. In: Scheiner S.M., and DeWitt T.J. (Eds). Phenotypic Plasticity: Functional and Conceptual Approaches (2004), Oxford Univ. Press, Oxford 112-125
79. Sih A., Bell A.M., Johnson J.C., and Ziemba R.E. Behavioral syndromes: an intergrative overiew. Q. Rev. Biol. 79 (2004) 241-277
80. Smith J., and Prior M. Temperament and stress resilience in school-age children: a within-families study. J. Am. Acad. Child Adolesc. Psych. 34 (1995) 168-179
81. Smotherman W.P., and Bell R.W. Maternal mediation of early experience. In: Bell R.W., and Smotherman W.P. (Eds). Maternal Influences and Early Behavior (1980), Spectrum, New York 201-210
82. Smotherman W.P., Brown C.P., and Levine S. Maternal responsiveness following differential pup treatment and mother-pup interactions. Horm. Behav. 8 (1977) 242-253
83. Smotherman W.P., Wiener S.G., Mendoza S.P., and Levine S. Maternal pituitary-adrenal responsiveness as a function of differential treatment of rat pups. Dev. Psychobiol. 10 (1977) 113-122
84. Stern J.M., and Johnson S.K. Ventral somatosensory determinants of nursing behavior in Norway rats: I. Effects of variations in the quality and quantity of pup stimuli. Physiol. Behav. 47 (1990) 993-1011
85. Tufto J. The evolution of plasticity and nonplastic spatial and temporal adaptations in the presence of imperfect environmental cues. Am. Nat. 156 (2000) 121-130
86. Villescas R., Bell R.W., Wright L., and Kufner M. Effect of handling on maternal behavior following return of pups to the nest. Dev. Psychobiol. 10 (1977) 323-329
87. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., and Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 7 (2004) 847-854
88. Weininger O. Physiological damage under emotional stress as a function of early experience. Science 119 (1954) 285-286
89. Würbel H. Behaviour and the standardization fallacy. Nat. Genet. 26 (2000) 263
90. Würbel H. Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci. 24 (2001) 207-211
91. Würbel H. Behavioral phenotyping enhanced-Beyond (environmental) standardization. Genes Brain Behav. 1 (2002) 3-8
92. Zhang T.Y., Parent C., Weaver I., and Meaney M.J. Maternal programming of individual differences in defensive responses in the rat. Ann. N. Y. Acad. Sci. 1032 (2004) 85-103
93. Zimmerberg B., Kim J.H., Davidson A.N., and Rosenthal A.J. Early deprivation alters the vocalization behavior of neonates directing maternal attention in a rat model of child neglect. Ann. N. Y. Acad. Sci. 1008 (2003) 308-313