Prior high corticosterone exposure reduces activation of immature neurons in the ventral hippocampus in response to spatial and nonspatial memory

Hippocampus

Volumn 25, Issue 3, 2015, Pages 329-344

  Workman, Joanna L ^a   Chan, Melissa Y T ^a   Galea, Liisa A M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Depression; Doublecortin; Neurogenesis; Stress; Water maze

Indexed keywords

CORTICOSTERONE; DOUBLECORTIN; ANTIINFLAMMATORY AGENT; DOUBLECORTIN PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; EGR1 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CELL MATURATION; CELL PROLIFERATION; CLIMBING; CONTROLLED STUDY; DEPRESSION; DEVELOPMENTAL STAGE; FORCED SWIM TEST; GENE EXPRESSION; GENE PRODUCT; GRANULE CELL; HIPPOCAMPUS; HORMONE ACTION; IMMEDIATE EARLY GENE; IMMOBILITY; MALE; MEMORY; MITOSIS; MORRIS WATER MAZE TEST; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPTICAL DENSITY; PHENOTYPE; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; SPATIAL MEMORY; TASK PERFORMANCE; TRAINING; ZIF268 GENE; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; CELL COUNT; CYTOLOGY; DRUG EFFECTS; MAZE TEST; METABOLISM; NERVE CELL; PSYCHOLOGY; SPATIAL ORIENTATION; SPRAGUE DAWLEY RAT; STATISTICS; SWIMMING; TIME FACTOR; TONIC IMMOBILITY;

ANALYSIS OF VARIANCE; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL COUNT; CORTICOSTERONE; EARLY GROWTH RESPONSE PROTEIN 1; HIPPOCAMPUS; IMMOBILITY RESPONSE, TONIC; MALE; MAZE LEARNING; MEMORY; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SPATIAL NAVIGATION; STATISTICS AS TOPIC; SWIMMING; TIME FACTORS;

EID: 84922660931     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22375     Document Type: Article

References (107)

1. Aguilar-Valles A, Sanchez E, de Gortari P, Balderas I, Ramirez-Amaya V, Bermudez-Rattoni F, Joseph-Bravo P. 2005. Analysis of the stress response in rats trained in the water-maze: Differential expression of corticotropin-releasing hormone, CRH-R1, glucocorticoid receptors and brain-derived neurotrophic factor in limbic regions. Neuroendocrinology 82:306-319.
2. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
3. 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.
4. 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.
5. Barha CK, Galea LA. 2013. The hormone therapy, Premarin, impairs hippocampus-dependent spatial learning and memory and reduces activation of new granule neurons in response to memory in female rats. Neurobiol Aging 34:986-1004.
6. Bessa JM, Ferreira D, Melo I, Marques F, Cerqueira JJ, Palha JA, Almeida OF, Sousa N. 2009. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol Psychiatry 14:764-773, 739.
7. Bodnoff SR, Suranyi-Cadotte B, Quirion R, Meaney MJ. 1989. A comparison of the effects of diazepam versus several typical and atypical anti-depressant drugs in an animal model of anxiety. Psychopharmacology (Berl) 97:277-279.
8. Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John Mann J, Arango V. 2009. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34:2376-2389.
9. Boldrini M, Hen R, Underwood MD, Rosoklija GB, Dwork AJ, Mann JJ, Arango V. 2012. Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol Psychiatry 72:562-571.
10. Bozon B, Davis S, Laroche S. 2002. Regulated transcription of the immediate-early gene Zif268: Mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus 12:570-577.
11. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S. 2003. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B Biol Sci 358:805-814.
12. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
13. Brummelte S, Galea L. 2010a. Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm Behav 58:769-779.
14. Brummelte S, Galea L. 2010b. Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 168:680-690.
15. Brummelte S, Pawluski JL, Galea LA. 2006. High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: A model of post-partum stress and possible depression. Horm Behav 50:370-382.
16. Burns LH, Annett L, Kelley AE, Everitt BJ, Robbins TW. 1996. Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: Implication for limbic-striatal interactions. Behav Neurosci 110:60-73.
17. Cameron HA, Gould E. 1994. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
18. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
19. Campbell S, Marriott M, Nahmias C, MacQueen GM. 2004. Lower hippocampal volume in patients suffering from depression: A meta-analysis. Am J Psychiatry 161:598-607.
20. Chow C, Epp JR, Lieblich SE, Barha CK, Galea LA. 2013. Sex differences in neurogenesis and activation of new neurons in response to spatial learning and memory. Psychoneuroendocrinology 38:1236-1250.
21. Coburn-Litvak PS, Pothakos K, Tata DA, McCloskey DP, Anderson BJ. 2003. Chronic administration of corticosterone impairs spatial reference memory before spatial working memory in rats. Neurobiol Learn Mem 80:11-23.
22. Cole AJ, Saffen DW, Baraban JM, Worley PF. 1989. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
23. Conrad CD. 2006. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus? Behav Cogn Neurosci Rev 5:41-60.
24. Conrad CD. 2010. A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 34:742-755.
25. Conrad CD, LeDoux JE, Magarinos AM, McEwen BS. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113:902-913.
26. Crayton JW, Joshi I, Gulati A, Arora RC, Wolf WA. 1996. Effect of corticosterone on serotonin and catecholamine receptors and uptake sites in rat frontal cortex. Brain Res 728:260-262.
27. Cryan JF, Valentino RJ, Lucki I. 2005. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 29:547-569.
28. Czeh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M, Bartolomucci A, Fuchs E. 2001. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 98:12796-12801.
29. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I, Drew M, Craig DA, Guiard BP, Guilloux JP, Artymyshyn RP, Gardier AM, Gerald C, Antonijevic IA, Leonardo ED, Hen R . 2009. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62:479-493.
30. de Hoz L, Knox J, Morris RG. 2003. Longitudinal axis of the hippocampus: Both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol. Hippocampus 13:587-603.
31. de Villiers AS, Russell VA, Taljaard JJ. 1992. Effect of corticosterone on noradrenergic nuclei in the pons-medulla and [3H]NA release from terminals in hippocampal slices. Neurochem Res 17:273-280.
32. Degroot A, Treit D. 2004. Anxiety is functionally segregated within the septo-hippocampal system. Brain Res 1001:60-71.
33. Detke MJ, Rickels M, Lucki I. 1995. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl) 121:66-72.
34. Epp JR, Spritzer MD, Galea LA. 2007. Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience 149:273-285.
35. Epp JR, Haack AK, Galea LA. 2011a. Activation and survival of immature neurons in the dentate gyrus with spatial memory is dependent on time of exposure to spatial learning and age of cells at examination. Neurobiol Learn Mem 95:316-325.
36. Epp JR, Scott NA, Galea LA. 2011b. Strain differences in neurogenesis and activation of new neurons in the dentate gyrus in response to spatial learning. Neuroscience 172:342-354.
37. Epp JR, Beasley CL, Galea LA. 2013a. Increased hippocampal neurogenesis and p21 expression in depression: Dependent on antidepressants, sex, age, and antipsychotic exposure. Neuropsychopharmacology 38:2297-2306.
38. Epp JR, Chow C, Galea LA. 2013b. Hippocampus-dependent learning influences hippocampal neurogenesis. Front Neurosci 7:57.
39. Fan Y, Chen P, Li Y, Cui K, Noel DM, Cummins ED, Peterson DJ, Brown RW, Zhu MY. 2014. Corticosterone administration up-regulated expression of norepinephrine transporter and dopamine beta-hydroxylase in rat locus coeruleus and its terminal regions. J Neurochem 128:445-458.
40. Fanselow MS, Dong HW. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
41. Ferbinteanu J, Ray C, McDonald RJ. 2003. Both dorsal and ventral hippocampus contribute to spatial learning in Long-Evans rats. Neurosci Lett 345:131-135.
42. Galea LA, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS. 1997. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81:689-697.
43. Galea LA, Wide JK, Barr AM. 2001. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav Brain Res 122:1-9.
44. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-3650.
45. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
46. Gregus A, Wintink AJ, Davis AC, Kalynchuk LE. 2005. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav Brain Res 156:105-114.
47. Guzowski JF. 2002. Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus 12:86-104.
48. Guzowski JF, Setlow B, Wagner EK, McGaugh JL. 2001. Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21:5089-5098.
49. Hamson DK, Wainwright SR, Taylor JR, Jones BA, Watson NV, Galea LA. 2013. Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology 154:3294-3304.
50. Hastings NB, Gould E. 1999. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146-154.
51. Heimovics SA, Prior NH, Maddison CJ, Soma KK. 2012. Rapid and widespread effects of 17beta-estradiol on intracellular signaling in the male songbird brain: A seasonal comparison. Endocrinology 153:1364-1376.
52. Hoffman AN, Krigbaum A, Ortiz JB, Mika A, Hutchinson KM, Bimonte-Nelson HA, Conrad CD. 2011. Recovery after chronic stress within spatial reference and working memory domains: Correspondence with hippocampal morphology. Eur J Neurosci 34:1023-1030.
53. Hunsaker MR, Kesner RP. 2008. Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol Learn Mem 89:61-69.
54. Ising M, Horstmann S, Kloiber S, Lucae S, Binder EB, Kern N, Kunzel HE, Pfennig A, Uhr M, Holsboer F. 2007. Combined dexamethasone/corticotropin releasing hormone test predicts treatment response in major depression - a potential biomarker? Biol Psychiatry 62:47-54.
55. Jakubs K, Nanobashvili A, Bonde S, Ekdahl CT, Kokaia Z, Kokaia M, Lindvall O. 2006. Environment matters: Synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 52:1047-1059.
56. Jessberger S, Nakashima K, Clemenson GD Jr, Mejia E, Mathews E, Ure K, Ogawa S, Sinton CM, Gage FH, Hsieh J. 2007. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27:5967-5975.
57. Johnson SA, Fournier NM, Kalynchuk LE. 2006. Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav Brain Res 168:280-288.
58. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S. 2001. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289-296.
59. Kalynchuk LE, Gregus A, Boudreau D, Perrot-Sinal TS. 2004. Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats. Behav Neurosci 118:1365-1377.
60. Karten YJ, Nair SM, van Essen L, Sibug R, Joels M. 1999. Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc Natl Acad Sci USA 96:13456-13461.
61. Kheirbek MA, Hen R. 2011. Dorsal vs ventral hippocampal neurogenesis: Implications for cognition and mood. Neuropsychopharmacology 36:373-374.
62. Kirby ED, Muroy SE, Sun WG, Covarrubias D, Leong MJ, Barchas LA, Kaufer D. 2013. Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. Elife 2:e00362.
63. 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 USA 99:10825-10830.
64. Loureiro M, Lecourtier L, Engeln M, Lopez J, Cosquer B, Geiger K, Kelche C, Cassel JC, Pereira de Vasconcelos A. 2012. The ventral hippocampus is necessary for expressing a spatial memory. Brain Struct Funct 217:93-106.
65. Luine V, Villegas M, Martinez C, McEwen BS. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167-170.
66. Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS. 1996. Restraint stress reversibly enhances spatial memory performance. Physiol Behav 59:27-32.
67. Lussier AL, Lebedeva K, Fenton EY, Guskjolen A, Caruncho HJ, Kalynchuk LE. 2013. The progressive development of depression-like behavior in corticosterone-treated rats is paralleled by slowed granule cell maturation and decreased reelin expression in the adult dentate gyrus. Neuropharmacology 71:174-183.
68. Magarinos AM, Orchinik M, McEwen BS. 1998. Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: A paradox. Brain Res 809:314-318.
69. Malberg JE, Eisch AJ, Nestler EJ, Duman RS. 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110.
70. Maren S, Holt WG. 2004. Hippocampus and Pavlovian fear conditioning in rats: Muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. Behav Neurosci 118:97-110.
71. Marks W, Fournier NM, Kalynchuk LE. 2009. Repeated exposure to corticosterone increases depression-like behavior in two different versions of the forced swim test without altering nonspecific locomotor activity or muscle strength. Physiol Behav 98:67-72.
72. McClure RE, Barha CK, Galea LA. 2013. 17beta-Estradiol, but not estrone, increases the survival and activation of new neurons in the hippocampus in response to spatial memory in adult female rats. Horm Behav 63:144-157.
73. McHugh SB, Deacon RM, Rawlins JN, Bannerman DM. 2004. Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav Neurosci 118:63-78.
74. McKinnon MC, Yucel K, Nazarov A, MacQueen GM. 2009. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci 34:41-54.
75. Meltzer LA, Yabaluri R, Deisseroth K. 2005. A role for circuit homeostasis in adult neurogenesis. Trends Neurosci 28:653-660.
76. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
77. Parker KJ, Schatzberg AF, Lyons DM. 2003. Neuroendocrine aspects of hypercortisolism in major depression. Horm Behav 43:60-66.
78. 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.
79. Porsolt RD, Le Pichon M, Jalfre M. 1977. Depression: A new animal model sensitive to antidepressant treatments. Nature 266:730-732.
80. Porsolt RD, Anton G, Blavet N, Jalfre M. 1978. Behavioural despair in rats: A new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379-391.
81. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA. 2006. Integration of new neurons into functional neural networks. J Neurosci 26:12237-12241.
82. Ruediger S, Spirig D, Donato F, Caroni P. 2012. Goal-oriented searching mediated by ventral hippocampus early in trial-and-error learning. Nat Neurosci 15:1563-1571.
83. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R . 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
84. Sapolsky RM, McEwen BS, Rainbow TC. 1983. Quantitative autoradiography of [3H]corticosterone receptors in rat brain. Brain Res 271:331-334.
85. Sapolsky RM, Krey LC, McEwen BS. 1984. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci 81:6174-6177.
86. Schoenfeld TJ, Rada P, Pieruzzini PR, Hsueh B, Gould E. 2013. Physical exercise prevents stress-induced activation of granule neurons and enhances local inhibitory mechanisms in the dentate gyrus. J Neurosci 33:7770-7777.
87. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. 1996. Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci 93:3908-3913.
88. Sheline YI, Sanghavi M, Mintun MA, Gado MH. 1999. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 19:5034-5043.
89. Sheline YI, Gado MH, Kraemer HC. 2003. Untreated depression and hippocampal volume loss. Am J Psychiatry 160:1516-1518.
90. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA. 2009a. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29:14484-14495.
91. Snyder JS, Radik R, Wojtowicz JM, Cameron HA. 2009b. Anatomical gradients of adult neurogenesis and activity: Young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19:360-370.
92. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. 2011. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476:458-461.
93. Snyder JS, Clifford MA, Jeurling SI, Cameron HA. 2012a. Complementary activation of hippocampal-cortical subregions and immature neurons following chronic training in single and multiple context versions of the water maze. Behav Brain Res 227:330-339.
94. Snyder JS, Ferrante SC, Cameron HA. 2012b. Late maturation of adult-born neurons in the temporal dentate gyrus. PLoS One 7:e48757.
95. Sunanda, Rao MS, Raju TR. 1995. Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons-a quantitative study. Brain Res 694:312-317.
96. Tanti A, Belzung C. 2013. Neurogenesis along the septo-temporal axis of the hippocampus: Are depression and the action of antidepressants region-specific? Neuroscience 252:234-252.
97. Tashiro A, Makino H, Gage FH. 2007. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: A critical period during an immature stage. J Neurosci 27:3252-3259.
98. Trivedi MA, Coover GD. 2004. Lesions of the ventral hippocampus, but not the dorsal hippocampus, impair conditioned fear expression and inhibitory avoidance on the elevated T-maze. Neurobiol Learn Mem 81:172-184.
99. Vorhees CV, Williams MT. 2006. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1:848-858.
100. Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS. 1992a. Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2:431-435.
101. Watanabe Y, Gould E, McEwen BS. 1992b. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341-345.
102. Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, Evan G, Bliss TV, Hunt SP. 1990. Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4:603-614.
103. Wong EY, Herbert J. 2004. The corticoid environment: A determining factor for neural progenitors' survival in the adult hippocampus. Eur J Neurosci 20:2491-2498.
104. Wong EY, Herbert J. 2006. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137:83-92.
105. Wood GE, Beylin AV, Shors TJ. 2001. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav Neurosci 115:175-187.
106. Workman JL, Brummelte S, Galea LA. 2013. Postpartum corticosterone administration reduces dendritic complexity and increases the density of mushroom spines of hippocampal CA3 arbors in dams. J Neuroendocrinol.
107. Wright RL, Lightner EN, Harman JS, Meijer OC, Conrad CD. 2006. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur J Neurosci 24:595-605.