Brain development under stress: Hypotheses of glucocorticoid actions revisited

Neuroscience and Biobehavioral Reviews

Volumn 34, Issue 6, 2010, Pages 853-866

  Oitzl, Melly S ^a   Champagne, Danielle L ^a   van der Veen, Rixt ^a   de Kloet, E Ronald ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Glucocorticoid receptor; Maternal care; Mineralocorticoid receptor; Resilience; Vulnerability

Indexed keywords

ADRENALIN; CORTICOSTEROID RECEPTOR; CORTICOTROPIN; ENDORPHIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MINERALOCORTICOID RECEPTOR; VASOPRESSIN;

ADAPTATION; AGING; BEHAVIOR DISORDER; CHRONIC STRESS; COGNITION; COPING BEHAVIOR; EARLY LIFE STRESS; ENVIRONMENTAL FACTOR; EPIGENETICS; FEAR; GENETIC VARIABILITY; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFORMATION PROCESSING; LIMBIC SYSTEM; MATERNAL CARE; MATERNAL DEPRIVATION; MENTAL STRESS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REVIEW; REWARD; SOCIAL BEHAVIOR;

AGING; ANIMALS; BRAIN; GLUCOCORTICOIDS; HUMANS; MODELS, NEUROLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 77950627167     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2009.07.006     Document Type: Review

References (169)

1. Ambroggi F., Turiault M., Milet A., Deroche-Gamonet V., Parnaudeau S., Balado E., Barik J., van der Veen R., Maroteaux G., Lemberger T., Schütz G., Lazar M., Marinelli M., Piazza P.V., Tronche F. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat. Neurosci. 2009, 12(3):247-249.
2. Arbel I., Kadar T., Silbermann M., Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res. 1994, 657:227-235.
3. Barker D.J. Adult consequences of fetal growth restriction. Clin. Obstet. Gynecol. 2006, 49:270-283.
4. Barker D.J. The origins of the developmental origins theory. J. Intern. Med. 2007, 261:412-417.
5. Bohus B., de Kloet E.R. Adrenal steroids and extinction behavior: antagonism by progesterone, deoxycorticosterone and dexamethasone of a specific effect of corticosterone. Life Sci. 1981, 28:433-440.
6. Bonanno G.A., Mancini A.D. The human capacity to thrive in the face of potential trauma. Pediatrics 2008, 121:369-375.
7. Borcel E., Perez-Alvarez L., Herrero A.I., Brionne T., Varea E., Berezin V., Bock E., Sandi C., Venero C. Chronic stress in adulthood followed by intermittent stress impairs spatial memory and the survival of newborn hippocampal cells in aging animals: prevention by FGL, a peptide mimetic of neural cell adhesion molecule. Behav. Pharmacol. 2008, 19:41-49.
8. Brady K.T., Verduin M.L., Tolliver B.K. Treatment of patients comorbid for addiction and other psychiatric disorders. Curr. Psychiatry Rep. 2007, 9:374-380.
9. Brinks V., de Kloet E.R., Oitzl M.S. Strain specific fear behaviour and glucocorticoid response to aversive events: modelling PTSD in mice. Prog. Brain Res. 2008, 167:257-261.
10. Brinks V., de Kloet E.R., Oitzl M.S. Corticosterone facilitates extinction of fear memory in BALB/c mice but strengthens cue related fear in C57BL/6 mice. Exp. Neurol. 2009, 216(2):375-382.
11. Brinks V., van der Mark M.H., de Kloet E.R., Oitzl M.S. Differential MR/GR activation in mice results in emotional states beneficial or impairing for cognition. Neural Plast. 2007, 2007:90163.
12. Brinks V., van der Mark M.H., de Kloet E.R., Oitzl M.S. Emotion and cognition in high and low stress sensitive mouse strains: a combined neuroendocrine and behavioral study in BALB/c and C57BL/6J mice. Front Behav. Neurosci. 2007, 1:8.
13. Brinks V., Berger S., Gass P., de Kloet E.R., Oitzl M.S. Mineralocorticoid receptors in control of emotional arousal and fear memory. Horm. Behav. 2009, 56(2):232-238.
14. Cabib S., Orsini C., Le Moal M., Piazza P.V. Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science 2000, 289:463-465.
15. Campbell J., Spear L.P. Effects of early handling on amphetamine-induced locomotor activation and conditioned place preference in the adult rat. Psychopharmacology (Berl.) 1999, 143:183-189.
16. Carlier M., Roubertoux P., Cohen-Salmon C. Differences in patterns of pup care in Mus musculus domesticus: 1. Comparisons between eleven inbred strains. Behav. Neural Biol. 1982, 35:205-210.
17. Champagne D.L., Bagot R.C., van Hasselt F., Ramakers G., Meaney M.J., de Kloet E.R., Joels M., Krugers H. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 2008, 28:6037-6045.
18. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003, 79:359-371.
19. Cruz F.C., Quadros I.M., Planeta, Cda S., Miczek K.A. Maternal separation stress in male mice: long-term increases in alcohol intake. Psychopharmacology (Berl.) 2008, 201(3):459-468.
20. Dalm S., de Visser L., Spruijt B.M., Oitzl M.S. Repeated rat exposure inhibits the circadian activity patterns of C57BL/6J mice in the home cage. Behav. Brain Res. 2009, 196:84-92.
21. De Bellis M.D. Developmental traumatology: a contributory mechanism for alcohol and substance use disorders. Psychoneuroendocrinology 2002, 27:155-170.
22. de Kloet E.R., Joels M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
23. de Kloet E.R., Oitzl M.S. Who cares for a stressed brain? The mother, the kid or both?. Neurobiol. Aging 2003, 24(Suppl. 1):S61-S65.
24. de Kloet E.R., Oitzl M.S., Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci. 1999, 22:422-426.
25. de Kloet E.R., Oitzl M.S., Vermetten E. Stress hormones and PTSD: basic studies and clinical perspectives. Prog. Brain Res. 2008, 167. Elsevier, Amsterdam.
26. de Kloet E.R., Sutanto W., van den Berg D.T., Carey M.P., van Haarst A.D., Hornsby C.D., Meijer O.C., Rots N.Y., Oitzl M.S. Brain mineralocorticoid receptor diversity: functional implications. J. Steroid Biochem. Mol. Biol. 1993, 47:183-190.
27. de Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301.
28. de Quervain D.J. Glucocorticoid-induced inhibition of memory retrieval: implications for posttraumatic stress disorder. Ann. N. Y. Acad. Sci. 2006, 1071:216-220.
29. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
30. de Quervain D.J., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Front. Neuroendocrinol. 2009, (March 31). [Epub ahead of print].
31. de Rijk R.H., Wust S., Meijer O.C., Zennaro M.C., Federenko I.S., Hellhammer D.H., Giacchetti G., Vreugdenhil E., Zitman F.G., de Kloet E.R. A common polymorphism in the mineralocorticoid receptor modulates stress responsiveness. J. Clin. Endocrinol. Metab. 2006, 91:5083-5089.
32. Deroche-Gamonet V., Sillaber I., Aouizerate B., Izawa R., Jaber M., Ghozland S., Kellendonk C., Le Moal M., Spanagel R., Schütz G., Tronche F., Piazza P.V. The glucocorticoid receptor as a potential target to reduce cocaine abuse. J. Neurosci. 2003, 23(11):4785-4790.
33. Deminiere J.M., Piazza P.V., Guegan G., Abrous N., Maccari S., Le Moal M., Simon H. Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res. 1992, 586:135-139.
34. Denenberg V.H., Brumaghim J.T., Haltmeyer G.C., Zarrow M.X. Increased adrenocortical activity in the neonatal rat following handling. Endocrinology 1967, 81:1047-1052.
35. Dong Y., Poellinger L., Okret S., Hoog J.O., von Bahr-Lindstrom H., Jornvall H., Gustafsson J.A. Regulation of gene expression of class I alcohol dehydrogenase by glucocorticoids. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:767-771.
36. Ehlers C.L., Walker B.M., Pian J.P., Roth J.L., Slawecki C.J. Increased alcohol drinking in isolate-housed alcohol-preferring rats. Behav. Neurosci. 2007, 121:111-119.
37. Ferguson D., Sapolsky R. Mineralocorticoid receptor overexpression differentially modulates specific phases of spatial and nonspatial memory. J. Neurosci. 2007, 27:8046-8052.
38. Ferrari E., Casarotti D., Muzzoni B., Albertelli N., Cravello L., Fioravanti M., Solerte S.B., Magri F. Age-related changes of the adrenal secretory pattern: possible role in pathological brain aging. Brain Res. Brain Res. Rev. 2001, 37:294-300.
39. Gass P., Kretz O., Wolfer D.P., Berger S., Tronche F., Reichardt H.M., Kellendonk C., Lipp H.P., Schmid W., Schutz G. Genetic disruption of mineralocorticoid receptor leads to impaired neurogenesis and granule cell degeneration in the hippocampus of adult mice. EMBO Rep. 2000, 1:447-451.
40. Giordano R., Bo M., Pellegrino M., Vezzari M., Baldi M., Picu A., Balbo M., Bonelli L., Migliaretti G., Ghigo E., Arvat E. Hypothalamus-pituitary-adrenal hyperactivity in human aging is partially refractory to stimulation by mineralocorticoid receptor blockade. J. Clin. Endocrinol. Metab. 2005, 90:5656-5662.
41. Gluckman P.D., Cutfield W., Hofman P., Hanson M.A. The fetal, neonatal, and infant environments-the long-term consequences for disease risk. Early Hum. Dev. 2005, 81:51-59.
42. Gluckman P.D., Hanson M.A., Beedle A.S. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am. J. Hum. Biol. 2007, 19:1-19.
43. Grootendorst J., de Kloet E.R., Dalm S., Oitzl M.S. Reversal of cognitive deficit of apolipoprotein E knockout mice after repeated exposure to a common environmental experience. Neuroscience 2001, 108:237-247.
44. Grootendorst J., de Kloet E.R., Vossen C., Dalm S., Oitzl M.S. Repeated exposure to rats has persistent genotype-dependent effects on learning and locomotor activity of apolipoprotein E knockout and C57Bl/6 mice. Behav. Brain Res. 2001, 125:249-259.
45. Harlow H.F. The Nature of Love. Am. Psychol. 1958, 13:673-685.
46. Heijmans B.T., Tobi E.W., Stein A.D., Putter H., Blauw G.J., Susser E.S., Slagboom P.E., Lumey L.H. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17046-17049.
47. Heim C., Plotsky P.M., Nemeroff C.B. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 2004, 29:641-648.
48. Henry C., Guegant G., Cador M., Arnauld E., Arsaut J., Le Moal M., Demotes-Mainard J. Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res. 1995, 685:179-186.
49. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front. Neuroendocrinol. 2003, 24:151-180.
50. Heuser I., Deuschle M., Weber A., Kniest A., Ziegler C., Weber B., Colla M. The role of mineralocorticoid receptors in the circadian activity of the human hypothalamus-pituitary-adrenal system: effect of age. Neurobiol. Aging 2000, 21:585-589.
51. Holmes M.C., Seckl J.R. The role of 11beta-hydroxysteroid dehydrogenases in the brain. Mol. Cell. Endocrinol. 2006, 248:9-14.
52. Horton T.H. Fetal origins of developmental plasticity: animal models of induced life history variation. Am. J. Hum. Biol. 2005, 17:34-43.
53. Huot R.L., Thrivikraman K.V., Meaney M.J., 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 (Berl.) 2001, 158:366-373.
54. Jans J.E., Woodside B.C. Nest temperature: effects on maternal behavior, pup development, and interactions with handling. Dev. Psychobiol. 1990, 23:519-534.
55. Joels M., Karst H., de Rijk R.H., de Kloet E.R. The coming out of the brain mineralocorticoid receptor. Trends Neurosci. 2008, 31:1-7.
56. Joels M., Karst H., Krugers H.J., Lucassen P.J. Chronic stress: Implications for neuronal morphology, function and neurogenesis. Front. Neuroendocrinol. 2007, 28:72-96.
57. Joels M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cogn Sci. 2006, 10:152-158.
58. Jun S.S., Chen Z., Pace M.C., Shaul P.W. Glucocorticoids downregulate cyclooxygenase-1 gene expression and prostacyclin synthesis in fetal pulmonary artery endothelium. Circ. Res. 1999, 84:193-200.
59. Karst H., Berger S., Turiault M., Tronche F., Schutz G., Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19204-19207.
60. Kawakami S.E., Quadros I.M., Takahashi S., Suchecki D. Long maternal separation accelerates behavioural sensitization to ethanol in female, but not in male mice. Behav. Brain Res. 2007, 184(2):109-116.
61. Khantzian E.J. The self-medication hypothesis of addictive disorders: focus on heroin and cocaine dependence. Am. J. Psychiatry 1985, 142:1259-1264.
62. King S., Laplante D., Joober R. Understanding putative risk factors for schizophrenia: retrospective and prospective studies. J. Psychiatry Neurosci. 2005, 30:342-348.
63. Kippin T.E., Szumlinski K.K., Kapasova Z., Rezner B., See R.E. Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology 2008, 33:769-782.
64. Kosten T.A., Miserendino M.J., Kehoe P. Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience. Brain Res. 2000, 875:44-50.
65. Kosten T.A., Zhang X.Y., Kehoe P. Neurochemical and behavioral responses to cocaine in adult male rats with neonatal isolation experience. J. Pharmacol. Exp. Ther. 2005, 314:661-667.
66. Kosten T.A., Zhang X.Y., Kehoe P. Heightened cocaine and food self-administration in female rats with neonatal isolation experience. Neuropsychopharmacology 2006, 31:70-76.
67. Kuningas M., de Rijk R.H., Westendorp R.G., Jolles J., Slagboom P.E., van Heemst D. Mental performance in old age dependent on cortisol and genetic variance in the mineralocorticoid and glucocorticoid receptors. Neuropsychopharmacology 2007, 32:1295-1301.
68. Landfield P.W., Waymire J.C., Lynch G. Hippocampal aging and adrenocorticoids: quantitative correlations. Science 1978, 202:1098-1102.
69. Levine S. Infantile experience and resistance to physiological stress. Science 1957, 126:405.
70. Levine S. Stimulation in infancy. Sci. Am. 1960, 202:81-86.
71. Levine S. The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors. Ann. N. Y. Acad. Sci. 1994, 746:275-288.
72. Levine S. Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 2000, 405:149-160.
73. Levine S. Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiol. Behav. 2001, 73:255-260.
74. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 2005, 30:939-946.
75. Levine S., Huchton D.M., Wiener S.G., Rosenfeld P. Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev. Psychobiol. 1991, 24:547-558.
76. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
77. Lu L., Shepard J.D., Hall F.S., Shaham Y. Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci. Biobehav. Rev. 2003, 27:457-491.
78. Lupien S.J., Fiocco A., Wan N., Maheu F., Lord C., Schramek T., Tu M.T. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 2005, 30:225-242.
79. Lynch W.J., Mangini L.D., Taylor J.R. Neonatal isolation stress potentiates cocaine seeking behavior in adult male and female rats. Neuropsychopharmacology 2005, 30:322-329.
80. Maccari S., Piazza P.V., Kabbaj M., Barbazanges A., Simon H., Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neurosci. 1995, 15:110-116.
81. Marinelli M., Aouizerate B., Barrot M., Le Moal M., Piazza P.V. Dopamine-dependent responses to morphine depend on glucocorticoid receptors. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(13):7742-7747.
82. Marissal-Arvy N., Lombes M., Petterson J., Moisan M.P., Mormede P. Gain of function mutation in the mineralocorticoid receptor of the Brown Norway rat. J. Biol. Chem. 2004, 279:39232-39239.
83. Marquardt A.R., Ortiz-Lemos L., Lucion A.B., Barros H.M. Influence of handling or aversive stimulation during rats' neonatal or adolescence periods on oral cocaine self-administration and cocaine withdrawal. Behav. Pharmacol. 2004, 15:403-412.
84. Matthews K., Robbins T.W., Everitt B.J., Caine S.B. Repeated neonatal maternal separation alters intravenous cocaine self-administration in adult rats. Psychopharmacology (Berl.) 1999, 141:123-134.
85. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 1999, 22:105-122.
86. McEwen B.S. Mood disorders and allostatic load. Biol. Psychiatry 2003, 54:200-207.
87. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 2007, 87:873-904.
88. McEwen B.S., Seeman T. Protective and damaging effects of mediators of stress. Elaborating and testing the concepts of allostasis and allostatic load. Ann. N. Y. Acad. Sci. 1999, 896:30-47.
89. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 2004, 27:1-28.
90. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonté B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12(3):342-348.
91. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res. 2007, 1161:56-64.
92. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
93. Meaney M.J., Aitken D.H., van B.C., Bhatnagar S., Sapolsky R.M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 1988, 239:766-768.
94. Meaney M.J., Brake W., Gratton A. Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse?. Psychoneuroendocrinology 2002, 27:127-138.
95. Meaney M.J., Szyf M., Seckl J.R. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol. Med. 2007, 13:269-277.
96. Meijer O.C., van der L.S., Lachize S., Steenbergen P.J., de Kloet E.R. Steroid receptor coregulator diversity: what can it mean for the stressed brain?. Neuroscience 2006, 138:891-899.
97. Mikics E., Kruk M.R., Haller J. Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats. Psychoneuroendocrinology 2004, 29:618-635.
98. Moffett M.C., Vicentic A., Kozel M., Plotsky P., Francis D.D., Kuhar M.J. Maternal separation alters drug intake patterns in adulthood in rats. Biochem. Pharmacol. 2007, 73:321-330.
99. Morano M.I., Vazquez D.M., Akil H. The role of the hippocampal mineralocorticoid and glucocorticoid receptors in the hypothalamo-pituitary-adrenal axis of the aged Fisher rat. Mol. Cell. Neurosci. 1994, 5:400-412.
100. Moriceau S., Roth T.L., Okotoghaide T., Sullivan R.M. Corticosterone controls the developmental emergence of fear and amygdala function to predator odors in infant rat pups. Int. J. Dev. Neurosci. 2004, 22(5-6):415-422.
101. Morsink M.C., Joels M., Sarabdjitsingh R.A., Meijer O.C., de Kloet E.R., Datson N.A. The dynamic pattern of glucocorticoid receptor-mediated transcriptional responses in neuronal PC12 cells. J. Neurochem. 2006, 99:1282-1298.
102. Morsink M.C., Steenbergen P.J., Vos J.B., Karst H., Joels M., de Kloet E.R., Datson N.A. Acute activation of hippocampal glucocorticoid receptors results in different waves of gene expression throughout time. J. Neuroendocrinol. 2006, 18:239-252.
103. Muller M.J., Greverus D., Dellani P.R., Weibrich C., Wille P.R., Scheurich A., Stoeter P., Fellgiebel A. Functional implications of hippocampal volume and diffusivity in mild cognitive impairment. Neuroimage 2005, 28:1033-1042.
104. Munck A., Guyre P.M., Holbrook N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 1984, 5(1):25-44.
105. Nair S.M., Karst H., Dumas T., Phillips R., Sapolsky R.M., Rumpff van Essen L., Maslam S., Lucassen P.J., Joels M. Gene expression profiles associated with survival of individual rat dentate cells after endogenous corticosteroid deprivation. Eur. J. Neurosci. 2004, 20:3233-3243.
106. Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
107. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 1992, 106:62-71.
108. Oitzl M.S., de Kloet E.R., Joels M., Schmid W., Cole T.J. Spatial learning deficits in mice with a targeted glucocorticoid receptor gene disruption. Eur. J. Neurosci. 1997, 9:2284-2296.
109. Oitzl M.S., Fluttert M., Sutanto W., de Kloet E.R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur. J. Neurosci. 1998, 10:3759-3766.
110. Oitzl M.S., Reichardt H.M., Joels M., de Kloet E.R. Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:12790-12795.
111. Oitzl M.S., Workel J.O., Fluttert M., Frosch F., de Kloet E.R. Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur. J. Neurosci. 2000, 12:3771-3780.
112. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
113. Piazza P.V., Deminiere J.M., Le Moal M., Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989, 245:1511-1513.
114. Ploj K., Roman E., Nylander I. Long-term effects of maternal separation on ethanol intake and brain opioid and dopamine receptors in male Wistar rats. Neuroscience 2003, 121:787-799.
115. Ploj K., Roman E., Nylander I. Long-term effects of short and long periods of maternal separation on brain opioid peptide levels in male Wistar rats. Neuropeptides 2003, 37:149-156.
116. Power C., Li L., Hertzman C. Cognitive development and cortisol patterns in mid-life: findings from a British birth cohort. Psychoneuroendocrinology 2008, 33:530-539.
117. Pryce C.R., Ruedi-Bettschen D., Dettling A.C., Weston A., Russig H., Ferger B., Feldon J. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci. Biobehav. Rev. 2005, 29:649-674.
118. Pu Z., Krugers H.J., Joels M. Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn. Mem. 2007, 14:359-367.
119. Quirk G.J., Beer J.S. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. 2006, 16:723-727.
120. Reichardt H.M., Kaestner K.H., Tuckermann J., Kretz O., Wessely O., Bock R., Gass P., Schmid W., Herrlich P., Angel P., Schutz G. DNA binding of the glucocorticoid receptor is not essential for survival. Cell 1998, 93:531-541.
121. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
122. Reul J.M., Rothuizen J., de Kloet E.R. Age-related changes in the dog hypothalamic-pituitary-adrenocortical system: neuroendocrine activity and corticosteroid receptors. J. Steroid Biochem. Mol. Biol. 1991, 40:63-69.
123. Revsin Y., Rekers N.V., Louwe M.C., Saravia F.E., De Nicola A.F., de Kloet E.R., Oitzl M.S. Glucocorticoid receptor blockade normalizes hippocampal alterations and cognitive impairment in streptozotocin-induced Type 1 Diabetes mice. Neuropsychopharmacology 2009, 34(3):747-758.
124. Roman E., Gustafsson L., Hyytia P., Nylander I. Short and prolonged periods of maternal separation and voluntary ethanol intake in male and female ethanol-preferring AA and ethanol-avoiding ANA rats. Alcohol Clin. Exp. Res. 2005, 29:591-601.
125. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol. Learn. Mem. 1997, 67:176-179.
126. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10(6):423-433.
127. Rosenfeld P., Suchecki D., Levine S. Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neurosci. Biobehav. Rev. 1992, 16:553-568.
128. Rots N.Y., de J.J., Workel J.O., Levine S., Cools A.R., de Kloet E.R. Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J. Neuroendocrinol. 1996, 8:501-506.
129. Sanders M.J., Wiltgen B.J., Fanselow M.S. The place of the hippocampus in fear conditioning. Eur. J. Pharmacol. 2003, 463:217-223.
130. Sandi C., Merino J.J., Cordero M.I., Touyarot K., Venero C. Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 2001, 102:329-339.
131. Sandi C., Venero C., Guaza C. Novelty-related rapid locomotor effects of corticosterone in rats. Eur. J. Neurosci. 1996, 8:794-800.
132. Sandstrom A., Rhodin I.N., Lundberg M., Olsson T., Nyberg L. Impaired cognitive performance in patients with chronic burnout syndrome. Biol. Psychol. 2005, 69:271-279.
133. Sapolsky R. Stress, the Aging Brain and the Mechanism of Neuron Death 1992, MIT Press, Cambridge, MA.
134. Sapolsky R.M. Do glucocorticoid concentrations rise with age in the rat?. Neurobiol. Aging 1992, 13:171-174.
135. Sapolsky R.M., Krey L.C., McEwen B.S. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 1986, 7:284-301.
136. 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.
137. Schaaf M.J., Workel J.O., Lesscher H.M., Vreugdenhil E., Oitzl M.S., de Kloet E.R. Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res. 2001, 915:227-233.
138. Schmidt M., Enthoven L., van Woezik J.H., Levine S., de Kloet E.R., Oitzl M.S. The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J. Neuroendocrinol. 2004, 16:52-57.
139. Schmidt M.V., Enthoven L., van der Mark M.H., Levine S., de Kloet E.R., Oitzl M.S. The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int. J. Dev. Neurosci. 2003, 21:125-132.
140. Schmidt M.V., Oitzl M.S., Levine S., de Kloet E.R. The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Brain Res. Dev. Brain Res. 2002, 139:39-49.
141. Schroff K.C., Cowen M.S., Koch S., Spanagel R. Strain-specific responses of inbred mice to ethanol following food shortage. Addict. Biol. 2004, 9:265-271.
142. Schwabe L., Dalm S., Schachinger H., Oitzl M.S. Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol. Learn. Mem. 2008, 90:495-503.
143. Schwabe L., Schächinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as switch between memory systems. J. Cogn. Neurosci. 2009, (May 15).
144. Seckl J.R., Holmes M.C. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3:479-488.
145. Sluyter F., Hof M., Ellenbroek B.A., Degen S.B., Cools A.R. Genetic, sex, and early environmental effects on the voluntary alcohol intake in Wistar rats. Pharmacol. Biochem. Behav. 2000, 67:801-808.
146. Stanton M.E., Gutierrez Y.R., Levine S. Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. Behav. Neurosci. 1988, 102:692-700.
147. Starkman M.N., Giordani B., Gebarski S.S., Berent S., Schork M.A., Schteingart D.E. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol. Psychiatry 1999, 46:1595-1602.
148. Starkman M.N., Giordani B., Gebarski S.S., Schteingart D.E. Improvement in learning associated with increase in hippocampal formation volume. Biol. Psychiatry 2003, 53:233-238.
149. Stienstra C.M., van der Graaf F., Bosma A., Karten Y.J., Hesen W., Joels M. Synaptic transmission in the rat dentate gyrus after adrenalectomy. Neuroscience 1998, 85:1061-1071.
150. Szyf M., McGowan P., Meaney M.J. The social environment and the epigenome. Environ. Mol. Mutagen. 2008, 49:46-60.
151. Tasker J.G., Di S., Malcher-Lopes R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 2006, 147:5549-5556.
152. Tirard M., Almeida O.F., Hutzler P., Melchior F., Michaelidis T.M. Sumoylation and proteasomal activity determine the transactivation properties of the mineralocorticoid receptor. Mol. Cell. Endocrinol. 2007, 268:20-29.
153. Touyarot K., Venero C., Sandi C. Spatial learning impairment induced by chronic stress is related to individual differences in novelty reactivity: search for neurobiological correlates. Psychoneuroendocrinology 2004, 29:290-305.
154. van der Veen R., Abrous D.N., de Kloet E.R., Piazza P.V., Koehl M. Impact of intra- and interstrain cross-fostering on mouse maternal care. Genes Brain Behav. 2008, 7:184-192.
155. van der Veen R., Koehl M., Abrous D.N., de Kloet E.R., Piazza P.V., Deroche-Gamonet V. Maternal environment influences cocaine intake in adulthood in a genotype-dependent manner. PLoS ONE 2008, 3:e2245.
156. van der Veen R., Piazza P.V., Deroche-Gamonet V. Gene-environment interactions in vulnerability to cocaine intravenous self-administration: a brief social experience affects intake in DBA/2J but not in C57BL/6J mice. Psychopharmacology (Berl.) 2007, 193:179-186.
157. van Eekelen J.A., Oitzl M.S., de Kloet E.R. Adrenocortical hyporesponsiveness and glucocorticoid feedback resistance in old male brown Norway rats. J. Gerontol. A Biol. Sci. Med. Sci. 1995, 50:B83-B89.
158. van Eekelen J.A., Rots N.Y., Sutanto W., de Kloet E.R. The effect of aging on stress responsiveness and central corticosteroid receptors in the brown Norway rat. Neurobiol. Aging 1992, 13:159-170.
159. van Oers H.J., de Kloet E.R., Whelan T., Levine S. Maternal deprivation effect on the infant's neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone. J. Neurosci. 1998, 18(23):10171-10179.
160. van Rossum E.F., Russcher H., Lamberts S.W. Genetic polymorphisms and multifactorial diseases: facts and fallacies revealed by the glucocorticoid receptor gene. Trends Endocrinol. Metab. 2005, 16:445-450.
161. Vazquez D.M., Eskandari R., Zimmer C.A., Levine S., Lopez J.F. Brain 5-HT receptor system in the stressed infant rat: implications for vulnerability to substance abuse. Psychoneuroendocrinology 2002, 27:245-272.
162. Vazquez V., Penit-Soria J., Durand C., Besson M.J., Giros B., Dauge V. Maternal deprivation increases vulnerability to morphine dependence and disturbs the enkephalinergic system in adulthood. J. Neurosci. 2005, 25:4453-4462.
163. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7(8):847-854.
164. Weaver I.C., D'Alessio A.C., Brown S.E., Hellstrom I.C., Dymov S., Sharma S., Szyf M., Meaney M.J. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J. Neurosci. 2007, 27(7):1756-1768.
165. Wiegert O., Joels M., Krugers H. Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learn. Mem. 2006, 13:110-113.
166. Windle R.J., Wood S.A., Lightman S.L., Ingram C.D. The pulsatile characteristics of hypothalamo-pituitary-adrenal activity in female Lewis and Fischer 344 rats and its relationship to differential stress responses. Endocrinology 1998, 139:4044-4052.
167. Workel J.O., Oitzl M.S., Fluttert M., Lesscher H., Karssen A., de Kloet E.R. Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of brown norway rats from youth to senescence. J. Neuroendocrinol. 2001, 13:569-580.
168. Workel J.O., Oitzl M.S., Ledeboer A., de Kloet E.R. The Brown Norway rat displays enhanced stress-induced ACTH reactivity at day 18 after 24-h maternal deprivation at day 3. Brain Res. Dev. Brain Res. 1997, 103:199-203.
169. Yau J.L., Noble J., Hibberd C., Rowe W.B., Meaney M.J., Morris R.G., Seckl J.R. Chronic treatment with the antidepressant amitriptyline prevents impairments in water maze learning in aging rats. J. Neurosci. 2002, 22:1436-1442.