Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood

Journal of Neuroscience

Volumn 30, Issue 19, 2010, Pages 6635-6645

  Oomen, Charlotte A ^a   Soeters, Heleen ^a   Audureau, Nathalie ^a   Vermunt, Lisa ^a   Van Hasselt, Felisa N ^a   Manders, Erik M M ^b   Joëls, Marian ^a,c   Lucassen, Paul J ^a   Krugers, Harm ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; DENTATE GYRUS; EMOTION; FEMALE; GRANULE CELL; HIPPOCAMPUS; LEARNING; LIFE STRESS; LONG TERM POTENTIATION; MALE; MATERNAL DEPRIVATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT;

ANIMALS; CORTICOSTERONE; DENDRITES; DENTATE GYRUS; EMOTIONS; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; RANDOM ALLOCATION; RATS; RATS, WISTAR; SPACE PERCEPTION; STRESS, PSYCHOLOGICAL; SYNAPSES;

EID: 77952341577     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0247-10.2010     Document Type: Article

References (91)

1. Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2007) Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32:256-266. (Pubitemid 46400278)
2. Aisa B, Elizalde N, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2009) Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus 19:1222-1231.
3. Akirav I, Richter-Levin G (1999) Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci 19:10530-10535. (Pubitemid 30228059)
4. Alfarez DN, De Simoni A, Velzing EH, Bracey E, Joels M, Edwards FA, Krugers HJ (2009) Corticosterone reduces dendritic complexity in developing hippocampal CA1 neurons. Hippocampus 19:828-836.
5. Altman J, Bayer SA (1990a) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325-342. (Pubitemid 20368498)
6. Altman J, Bayer SA (1990b) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365-381. (Pubitemid 20368500)
7. Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joels M (2009) Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem 92:292-300.
8. Banasr M, Soumier A, Hery M, Mocaer E, Daszuta A (2006) Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis. Biol Psychiatry 59:1087-1096. (Pubitemid 43849657)
9. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113:1170-1188.
10. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28:273-283. (Pubitemid 38844376)
11. Boekhoorn K, Terwel D, Biemans B, Borghgraef P, Wiegert O, Ramakers GJ, de Vos K, Krugers H, Tomiyama T, Mori H, Joels M, van Leuven F, Lucassen PJ (2006) Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J Neurosci 26:3514-3523.
12. Bredy TW, Grant RJ, Champagne DL, Meaney MJ (2003) Maternal care influences neuronal survival in the hippocampus of the rat. Eur J Neurosci 18:2903-2909.
13. Brunson KL, Kramar E, Lin B, Chen Y, Colgin LL, Yanagihara TK, Lynch G, Baram TZ (2005) Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci 25:9328-9338. (Pubitemid 41464745)
14. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
15. Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, Joels M, Krugers H (2008) Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 28:6037-6045.
16. Champagne DL, de Kloet ER, Joels M (2009) Fundamental aspects of the impact of glucocorticoids on the (immature) brain. Semin Fetal Neonatal Med 14:136-142.
17. Claiborne BJ, Amaral DG, Cowan WM (1990) Quantitative, threedimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206-219.
18. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213.
19. Cordero MI, Merino JJ, Sandi C (1998) Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav Neurosci 112:885-891.
20. Coulter DA, Carlson GC (2007) Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog Brain Res 163:235-243.
21. Cowansage KK, Ledoux JE, Monfils MH (2009) Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 3:12-29.
22. de Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475.
23. Fabricius K, Wortwein G, Pakkenberg B (2008) The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Struct Funct 212:403-416. (Pubitemid 351161499)
24. Fluttert M, Dalm S, Oitzl MS (2000) A refined method for sequential blood sampling by tail incision in rats. Lab Anim 34:372-378.
25. Garner B, Wood SJ, Pantelis C, van den Buuse M (2007) Early maternal deprivation reduces prepulse inhibition and impairs spatial learning ability in adulthood: no further effect of post-pubertal chronic corticosterone treatment. Behav Brain Res 176:323-332.
26. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265. (Pubitemid 30491297)
27. Greisen MH, Altar CA, Bolwig TG, Whitehead R, Wortwein G (2005) Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats. J Neurosci Res 79:772-778. (Pubitemid 40476501)
28. Gruss M, Braun K, Frey JU, Korz V (2008) Maternal separation during a specific postnatal time window prevents reinforcement of hippocampal long-term potentiation in adolescent rats. Neuroscience 152:1-7.
29. Guijarro JZ, Tiba PA, Ferreira TL, Kawakami SE, Oliveira MG, Suchecki D (2007) Effects of brief and long maternal separations on the HPA axis activity and the performance of rats on context and tone fear conditioning. Behav Brain Res 184:101-108.
30. 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. (Pubitemid 32595461)
31. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ (2004) Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 19:131-144. (Pubitemid 38122079)
32. Hsu D (2007) The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res 163:601-613.
33. Huang WL, Harper CG, Evans SF, Newnham JP, Dunlop SA (2001) Repeated prenatal corticosteroid administration delays myelination of the corpus callosum in fetal sheep. Int J Dev Neurosci 19:415-425. (Pubitemid 32500337)
34. Huot RL, Plotsky PM, Lenox RH, McNamara RK (2002) Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950:52-63.
35. Karst H, Karten YJ, Reichardt HM, de Kloet ER, Schutz G, Joels M (2000) Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers. Nat Neurosci 3:977-978.
36. Kikusui T, Ichikawa S, Mori Y (2009) Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology 34:762-772.
37. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453-462.
38. Kitamura T, Saitoh Y, Takashima N, Murayama A, Niibori Y, Ageta H, Sekiguchi M, Sugiyama H, Inokuchi K (2009) Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 139:814-827.
39. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci U S A 99:10825-10830.
40. Korz V, Frey JU (2005) Bidirectional modulation of hippocampal longterm potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J Neurosci 25:7393-7400. (Pubitemid 41129812)
41. Kosten TA, Lee HJ, Kim JJ (2006) Early life stress impairs fear conditioning in adult male and female rats. Brain Res 1087:142-150.
42. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G (2003) Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 467:455-463. (Pubitemid 37467122)
43. Lehmann J, Pryce CR, Bettschen D, Feldon J (1999) The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 64:705-715.
44. Lehmann J, Russig H, Feldon J, Pryce CR (2002) Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacol Biochem Behav 73:141-145. (Pubitemid 34667026)
45. Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN (2006) Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatry 59:786-792.
46. Leventopoulos M, Ruedi-Bettschen D, Knuesel I, Feldon J, Pryce CR, Opacka-Juffry J (2007) Long-term effects of early life deprivation on brain glia in Fischer rats. Brain Res 1142:119-126. (Pubitemid 46413198)
47. Levine S, Huchton DM, Wiener SG, Rosenfeld P (1991) Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev Psychobiol 24:547-558.
48. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659-1662. (Pubitemid 27446227)
49. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3:799-806. (Pubitemid 30485705)
50. Lucassen PJ, Bosch O, Jousma E, Krömer SA, Andrews R, Seckl JR, Neumann ID (2009) Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low anxiety: possible key role of lack of induction of placental 11B-hydroxysteroid dehydrogenase type 2. Eur J Neurosci 29: 97-103.
51. Lucassen PJ, Meerlo P, Naylor AS, van Dam AM, Dayer AG, Fuchs E, Oomen CA, Czeh B (2010) Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepressant action. Eur Neuropsychopharmacol 20:1-17.
52. Lyons DM, Parker KJ, Katz M, Schatzberg AF (2009) Developmental cascades linking stress inoculation, arousal regulation, and resilience. Front Behav Neurosci 3:32.
53. Maggio N, Segal M (2007) Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J Neurosci 27:5757-5765. (Pubitemid 350021083)
54. Mayer JL, Klumpers L, Maslam S, de Kloet ER, Joels M, Lucassen PJ (2006) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol 18:629-631.
55. McEwen BS (2003) Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 9:149-154.
56. McEwen BS, Magarinos AM (2001) Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16:S7-S19.
57. Meyer JS (1983) Early adrenalectomy stimulates subsequent growth and development of the rat brain. Exp Neurol 82:432-446. (Pubitemid 14239942)
58. Mirescu C, Peters JD, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841-846. (Pubitemid 38989507)
59. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
60. Oitzl MS, Workel JO, Fluttert M, Frosch F, De Kloet ER (2000) 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 12:3771-3780.
61. Oomen CA, Mayer JL, de Kloet ER, Joels M, Lucassen PJ (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 26:3395-3401. (Pubitemid 350243543)
62. Oomen CA, Girardi CE, Cahyadi R, Verbeek EC, Krugers H, Joels M, Lucassen PJ (2009) Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS One 4:e3675.
63. Paizanis E, Renoir T, Lelievre V, Saurini F, Melfort M, Gabriel C, Barden N, Mocaer E, Hamon M, Lanfumey L (2009) Behavioural and neuroplastic effects of the new-generation antidepressant agomelatine compared to fluoxetine in glucocorticoid receptor-impaired mice. Int J Neuropsychopharmacol 24:1-16.
64. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
65. 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. (Pubitemid 34626001)
66. Petersen A, Wortwein G, Gruber SH, Mathe AA (2008) Escitalopram reduces increased hippocampal cytogenesis in a genetic rat depression model. Neurosci Lett 436:305-308.
67. Pham K, McEwen BS, Ledoux JE, Nader K (2005) Fear learning transiently impairs hippocampal cell proliferation. Neuroscience 130:17-24. (Pubitemid 39550411)
68. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
69. Plotsky PM, Meaney MJ (1993) 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 18:195-200. (Pubitemid 23130604)
70. Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Romer B, Rodriguez GR, Kronenberg G, Kempermann G (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7:77.
71. Pu Z, Krugers HJ, Joels M (2007) Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn Mem 14:359-367.
72. Pugh CR, Tremblay D, Fleshner M, Rudy JW (1997) A selective role for corticosterone in contextual-fear conditioning. Behav Neurosci 111:503-511. (Pubitemid 27251320)
73. Revest JM, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza PV, Abrous DN (2009) Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 14:959-967.
74. Sahay A, Hen R (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115.
75. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia AD, Sofroniew MV, Kandel ER, Santarelli L, Hen R, Drew MR (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A 103:17501-17506. (Pubitemid 44788998)
76. Schaaf MJ, Workel JO, Lesscher HM, Vreugdenhil E, Oitzl MS, de Kloet ER (2001) Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res 915:227-233. (Pubitemid 32947038)
77. Schmidt M, Enthoven L, van Woezik JH, Levine S, de Kloet ER, Oitzl MS (2004) The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J Neuroendocrinol 16:52-57. (Pubitemid 38159393)
78. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187. (Pubitemid 38656194)
79. Snyder JS, Radik R, Wojtowicz JM, Cameron HA (2009) Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19:360-370.
80. Stevenson CW, Spicer CH, Mason R, Marsden CA (2009) Early life programming of fear conditioning and extinction in adult male rats. Behav Brain Res 205:505-510.
81. Uysal N, Ozdemir D, Dayi A, Yalaz G, Baltaci AK, Bediz CS (2005) Effects of maternal deprivation on melatonin production and cognition in adolescent male and female rats. Neuro Endocrinol Lett 26:555-560. (Pubitemid 43013731)
82. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270. (Pubitemid 30491298)
83. Walker TL, Yasuda T, Adams DJ, Bartlett PF (2007) The doublecortin expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27: 3734-3742. (Pubitemid 46557670)
84. Wang S, Scott BW, Wojtowicz JM (2000) Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257. (Pubitemid 30055890)
85. Wearne SL, Rodriguez A, Ehlenberger DB, Rocher AB, Henderson SC, Hof PR (2005) New techniques for imaging, digitization and analysis of three-dimensional neural morphology on multiple scales. Neuroscience 136:661-680. (Pubitemid 41774717)
86. Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427-451.
87. Welberg LA, Seckl JR (2001) Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13:113-128. (Pubitemid 32058738)
88. A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
89. Workel JO, Oitzl MS, Fluttert M, Lesscher H, Karssen A, de Kloet ER (2001) Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of Brown Norway rats from youth to senescence. J Neuroendocrinol 13:569-580. (Pubitemid 32591045)
90. Wossink J, Karst H, Mayboroda O, Joels M (2001) Morphological and functional properties of rat dentate granule cells after adrenalectomy. Neuroscience 108:263-272. (Pubitemid 33152967)
91. Zhou M, Conboy L, Sandi C, Joels M, Krugers HJ (2009) Fear conditioning enhances spontaneous AMPA receptor-mediated synaptic transmission in mouse hippocampal CA1 area. Eur J Neurosci 30:1559-1564.