Chronic stress: Implications for neuronal morphology, function and neurogenesis

Frontiers in Neuroendocrinology

Volumn 28, Issue 2-3, 2007, Pages 72-96

  Joëls, Marian ^a   Karst, Henk ^a   Krugers, Harmen J ^a   Lucassen, Paul J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Amygdala; Brainstem; Catecholamines; Chronic stress; Excitability; Glucocorticoid; Hippocampus; Long term potentiation; Memory; Morphology; Neurogenesis; Prefrontal cortex

Indexed keywords

AMPA RECEPTOR; ANTIDEPRESSANT AGENT; BENZODIAZEPINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL L TYPE; CATECHOLAMINE; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CYANOKETONE; FLUOXETINE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOID RECEPTOR ANTAGONIST; MIFEPRISTONE; MINERALOCORTICOID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PHENYTOIN; SUBSTANCE P ANTAGONIST; TIANEPTINE; VASOPRESSIN ANTAGONIST;

AMYGDALOID NUCLEUS; BEHAVIOR CHANGE; BRAIN STEM; CALCIUM CURRENT; CELL ACTIVITY; CHRONIC STRESS; DENTATE GYRUS; DEPRESSION; ELECTROCONVULSIVE THERAPY; ELECTROENCEPHALOGRAM; EXCITABILITY; FOOTSHOCK; FUNCTIONAL MORPHOLOGY; HIPPOCAMPUS; HUMAN; LONG TERM POTENTIATION; MEMORY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; TRANSCRANIAL MAGNETIC STIMULATION;

ADAPTATION, BIOLOGICAL; ADRENAL CORTEX HORMONES; ANIMALS; BRAIN; CELL SHAPE; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; HUMANS; LONG-TERM POTENTIATION; NEURONS; STRESS;

EID: 34447103169     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2007.04.001     Document Type: Review

References (304)

1. Abrous D.N., Koehl M., and Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85 (2005) 523-569
2. Ahmed T., Frey J.U., and Korz V. Long-term effects of brief acute stress on cellular signaling and hippocampal LTP. J. Neurosci. 15 (2006) 3951-3958
3. Akirav I., and Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J. Neurosci. 19 (1999) 10530-10535
4. Akirav I., and Richter-Levin G. Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 22 (2002) 9912-9921
5. Alfarez D.N., Joëls M., and Krugers H.J. Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur. J. Neurosci. 17 (2003) 1928-1934
6. Alfarez D.N., Wiegert O., Joëls M., and Krugers H.J. Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience 115 (2002) 1119-1126
7. Alfonso J., Fernandez M.E., Cooper B., Flugge G., and Frash A.C. The stress-regulated protein M6a is a key modulator for neurite outgrowth and filopodium/spine formation. Proc. Natl. Acad. Sci. USA 102 (2005) 17196-17201
8. Alfonso J., Frick L.R., Silberman D.M., Palumbo M.L., Genaro A.M., and Frash A.C. Regulation of hippocampal gene expression is conserved in two species subjected to different stressors and antidepressant treatments. Biol. Psychiatry 59 (2006) 244-251
9. Alfonso J., Pollevick G.D., van Der Hart M.G., Flugge G., Fuchs E., and Frasch A.C. Identification of genes regulated by chronic psychosocial stress and antidepressant treatment in the hippocampus. Eur. J. Neurosci. 19 (2004) 659-666
10. Alonso R., Griebel G., Pavone G., Stemmelin J., le Fur G., and Soubrie P. Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol. Psychiatry 9 (2004) 278-286
11. Anderson M.F., Aberg M.A., Nilsson M., and Eriksson P.S. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res. Dev. Brain Res. 134 (2002) 115-122
12. Anstrom K.K., and Woodward D.J. Restraint increase dopaminergic burst firing in awake rats. Neuropsychopharmacology 30 (2005) 1832-1840
13. Bachman C.G., Linthorst A.C.E., Holsboer F., and Reul J.M.H.M. Effect of chronic administration of selective glucocorticoid receptor antagonists on the rat hypothalamic-pituitary-adrenocortical axis. Neuropsychopharmacology 28 (2003) 1056-1067
14. Bain M.J., Dwyer S.M., and Rusak B. Restraint stress affects hippocampal cell proliferation differently in rats and mice. Neurosci. Lett. 368 (2004) 7-10
15. Bale T.L., and Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 525-557
16. Barbon A., Popoli M., La Via L., Moraschi S., Vallini I., Tardito D., Tiraboschi E., Musazzi L., Giambelli R., Gennarelli M., Racagni G., and Barlati S. Regulation of editing and expression of glutamate alpha-amino-propionic-acid (AMPA)/kainate receptors by antidepressant drugs. Biol. Psychiatry 59 (2006) 713-720
17. Bartolomucci A., de Biurrun G., Czeh B., van Kampen M., and Fuchs E. Selective enhancement of spatial learning under chronic psychosocial stress. Eur. J. Neurosci. 15 (2002) 1863-1866
18. Bartolomucci A., Palanza P., Sacerdote P., Panerai A.E., Sgoifo A., Dantzer R., and Parmigiani S. Social factors and individual vulnerability to chronic stress exposure. Neurosci. Biobehav. Rev. 29 (2005) 67-81
19. Bennur S., Shankaranarayana Rao B.S., Pawlak R., Strickland S., McEwen B.S., and Chattarji S. Stress-induced spine loss in the medial amygdala is mediated by tissue-plasminogen activator. Neuroscience 144 (2007) 8-16
20. Bhargava A., Mathias R.S., McCormick J.A., Dallman M.F., and Pearce D. Glucocorticoids prolong Ca(2+) transients in hippocampal-derived H19-7 neurons by repressing the plasma membrane Ca(2+)-ATPase-1. Mol. Endocrinol. 16 (2002) 1629-1637
21. Bianchi M., Hagan J.J., and Heidbreder C.A. Neuronal plasticity, stress and depression: involvement of the cytoskeletal microtubular system?. Curr. Drug Targets CNS Neurol. Disord. 4 (2005) 597-611
22. Birnstiel S., and Beck S.G. Modulation of the 5-hydroxytryptamine4 receptor-mediated response by short-term and long-term administration of corticosterone in rat CA1 hippocampal pyramidal neurons. J. Pharmacol. Exp. Ther. 273 (1995) 1132-1138
23. Birnstiel S., List T.J., and Beck S.G. Chronic corticosterone treatment maintains synaptic activity of CA1 hippocampal pyramidal cells: acute high corticosterone administration increases action potential number. Synapse 20 (1995) 117-124
24. Blank T., Nijholt I., Eckart K., and Spiess J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 22 (2002) 3788-3794
25. Bodnoff S.R., Humphreys A.G., Lehman J.C., Diamond D.M., Rose G.M., and Meaney M.J. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J. Neurosci. 15 (1995) 61-69
26. Bonanno G., Giambelli R., Raiteri L., Tiraboschi E., Zappettini S., Musazzi L., Raiteri M., Racagni G., and Popoli M. Chronic antidepressants reduce depolarization-evoked glutamate release and protein interactions favoring formation of SNARE complex in hippocampus. J. Neurosci. 25 (2005) 3270-3279
27. Borsody M.K., and Weiss J.M. Influence of corticotropin-releasing hormone on electrophysiological activity of locus coeruleus neurons. Brain Res. 724 (1996) 149-168
28. Braga M.F., Aroniadou-Anderjaska V., Manion S.T., Hough C.J., and Li H. Stress impairs alpha(1A) adrenoceptor-mediated noradrenergic facilitation of GABAergic transmission in the basolateral amygdala. Neuropsychopharmacology 29 (2004) 45-58
29. Bramham C.R., Southard T., Ahlers S.T., and Sarvey J.M. Acute cold stress leading to elevated corticosterone neither enhances synaptic efficacy not impairs LTP in the dentate gyrus of freely moving rats. Brain Res. 789 (1998) 245-255
30. Bremner J.D., Krystal J.H., Southwick S.M., and Charney D.S. Noradrenergic mechanisms in stress and anxiety: II. Clinical studies. Synapse 23 (1996) 28-38
31. Brown J., Cooper-Kuhn C.M., Kempermann G., van Praag H., Winkler J., Gage F.H., and Kuhn H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 17 (2003) 2042-2046
32. Brown R.E., Sergeeva O.A., Eriksson K.S., and Haas H.L. Convergent excitation of dorsal raphe serotonin neurons by multiple arousal systems (orexin/hypocretin, histamine and noradrenaline). J. Neurosci. 22 (2002) 8850-8859
33. Brown S.M., Henning S., and Wellman C.L. Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb. Cortex. 15 (2005) 1714-1722
34. Brunson K.L., Baram T.Z., and Bender R.A. Hippocampal neurogenesis is not enhanced by lifelong reduction of glucocorticoid levels. Hippocampus 15 (2005) 491-501
35. Buckley T.M., and Schatzberg A.F. On the interactions of the hypothalamic-pituitary-adrenal (HPA) axis and sleep: normal HPA-axis activity and circadian rhythm, exemplary sleep disorders. J. Clin. Endocrinol. Metab. 90 (2005) 3106-3114
36. Budziszewska B., Siwanowicz J., and Przegalinski E. The effect of chronic treatment with antidepressant drugs on the corticosteroid receptor levels in the rat hippocampus. Pol. J. Pharmacol. 46 (1994) 147-152
37. Cameron H.A., and Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61 (1994) 203-209
38. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435 (2001) 406-417
39. Cerqueira J.J., Catania C., Sotiropoulos I., Schubert M., Kalisch R., Almeida O.F., Auer D.P., and Sousa N. Corticosteroid status influences the volume of the rat cingulate cortex-a magnetic resonance imaging study. J. Psychiatr. Res. 39 (2005) 451-460
40. Cerqueira J.J., Pego J.M., Taipa R., Bessa J.M., Almeida O.F., and Sousa N. Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J. Neurosci. 25 (2005) 7792-7800
41. Chameau P., Qin Y., Spijker S., Smit G., and Joëls M. Glucocorticoids specifically enhance L-type calcium current amplitude and affect calcium channel subunit expression in the mouse hippocampus. J. Neurophysiol. 97 (2007) 5-14
42. Chappell P.B., Smith M.A., Kilts C.D., Bissette G., Ritchie J., Anderson C., and Nemeroff C.B. Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress. J. Neurosci. 6 (1986) 2908-2914
43. Chen H., Pandey G.N., and Dwidedi Y. Hippocampal cell proliferation regulation by repeated stress and antidepressants. Neuroreport 17 (2006) 863-867
44. Cho K., and Little H.J. Effects of corticosterone on excitatory amino acid responses in dopamine-sensitive neurons in the ventral tegmental area. Neuroscience 88 (1999) 837-845
45. Conrad C.D. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus?. Behav. Cogn. Neurosci. Rev. 5 (2006) 41-60
46. Cook S.C., and Wellman C.L. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J. Neurobiol. 60 (2004) 236-248
47. Correll C.M., Rosenkranz J.A., and Grace A.A. Chronic cold stress alters prefrontal cortical modulation of amygdala neuronal activity in rats. Biol. Psychiatry 58 (2005) 382-391
48. Coste S.C., Kesterson R.A., Heldwein K.A., Stevens S.L., Heard A.D., Hollis J.H., Murray S.E., Hill J.K., Pantely G.A., Hohimer A.R., Hatton D.C., Phillips T.J., Finn D.A., Low M.J., Rittenberg M.B., Stenzel P., and Stenzel-Poore M.P. Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat. Genet. 24 (2000) 403-409
49. Cota D., Steiner M.A., Marsicano G., Cervino C., Herman J.P., Grubler Y., Stalla J., Pasquali R., Lutz B., Stalla G.K., and Pagotto U. Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. Endocrinology 148 (2007) 1574-1581
50. Czeh B., Michaelis T., Watanabe T., Frahm J., de Biurrun G., van Kampen M., Bartolomucc A., and Fuchs E. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl. Acad. Sci. USA 98 (2001) 12796-12801
51. Czeh B., Muller-Keuker J.I., Rygula R., Abumaria N., Hiemke C., Domenici E., and Fuchs E. Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology (2006) [Epub ahead of print]
52. Czeh B., Welt T., Fischer A.K., Erhardt A., Schmitt W., Muller M.B., Toschi N., Fuchs E., and Keck M.E. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry 52 (2002) 1057-1065
53. Czyrak A., Mackowiak M., Chocyk A., Fijal K., Tokarski K., Bijak M., and Wedzony K. Prolonged corticosterone treatment alters the responsiveness of 5-HT1A receptors to 8-OH-DPAT in rat CA1 hippocampal neurons. Naunyn Schmiedebergs Arch. Pharmacol. 366 (2002) 357-367
54. Dallman M.F. Fast glucocorticoid actions on brain: back to the future. Front Neuroendocrinol. 26 (2005) 103-108
55. Dayer A.G., Ford A.A., Cleaver K.M., Yassaee M., and Cameron H.A. Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol. 460 (2003) 563-572
56. DeBock F., Kurz J., Azad S.C., Parsons C.G., Hapfelmeier G., Zieglgansberger W., and Rammes G. Alpha2-adrenoreceptor activation inhibits LTP and LTD in the basolateral amygdala: involvement of Gi/o-protein-mediated modulation of Ca2+-channels and inwardly rectifying K+-channels in LTD. Eur. J. Neurosci. 17 (2003) 1411-1424
57. De Goeij D.C., Dijkstra H., and Tilders F.J. Chronic psychosocial stress enhances vasopressin, but not corticotropin-releasing factor, in the external zone of the median eminence of male rats: relationship to subordinate status. Endocrinology 131 (1992) 847-853
58. De Kloet E.R., Joëls M., and Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6 (2005) 463-475
59. De Kloet E.R., Vreugdenhil E., Oitzl M., and Joëls M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19 (1998) 269-301
60. Denver R.J. Endocannabinoids link rapid, membrane-mediated corticosteroid actions to behavior. Endocrinology 148 (2007) 490-492
61. Deussing J.M., Kuhne C., Putz B., Panhuysen M., Breu J., Stenzel-Poore M.P., Holsboer F., and Wurst W. Expression profiling identifies the CRH/CRH-R1 system as a modulator of neurovascular gene activity. J. Cereb. Blood Flow Metab. (2007) [Epub ahead of print]
62. Di S., Malcher-Lopes R., Halmos K.C., and Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 23 (2003) 4850-4857
63. Diamond D.M., Bennette M.C., Fleshner M., and Rose G.M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2 (1992) 421-430
64. Donohue H.S., Gabbott P.L., Davies H.A., Rodriguez J.J., Cordero M.I., Sandi C., Medvedev N.I., Popov V.I., Colyer F.M., Peddie C.J., and Stewart M.G. Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 140 (2006) 597-606
65. Dubrovsky B., Tatarinov A., Gijsbers K., Harris J., and Tsiodras A. Effects of arginine-vasopressin (AVP) on long-term potentiation in intact anesthetized rats. Brain Res. Bull. 59 (2003) 467-472
66. Duma D., Jewell C.M., and Cidlowski J.A. Multiple glucocorticoid receptor isoforms and mechanisms of post-translational modification. J. Steroid Biochem. Mol. Biol. 102 (2006) 11-21
67. Duvarci S., and Pare D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J. Neurosci. 27 (2007) 4482-4491
68. Ehninger D., and Kempermann G. Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes Brain Behav. 5 (2006) 29-39
69. El Yacoubi M., Bouali S., Popa D., Naudon L., Leroux-Nicollet I., Hamon M., Costentin J., Adrien J., and Vaugeois J.M. Behavioral, neurochemical, and electrophysiological characterization of a genetic mouse model of depression. Proc. Natl. Acad. Sci. USA 100 (2003) 6227-6232
70. Engelmann M., and Ludwig M. The activity of the hypothalamo-neurohypophysial system in response to acute stressor exposure: neuroendocrine and electrophysiological observations. Stress 7 (2004) 91-96
71. Fairchild G., Leitch M.M., and Ingram C.D. Acute and chronic effects of corticosterone on 5-HT1A receptor-mediated autoinhibition in the rat dorsal raphe nucleus. Neuropharmacology 45 (2003) 925-934
72. Falconer E.M., and Galea L.A. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res. 975 (2003) 22-36
73. Fehm H.L., Kern W., and Peters A. The selfish brain: competition for energy resources. Prog. Brain Res. 153 (2006) 129-140
74. Feldker D.E., Morsink M.C., Veenema A.H., Datson N.A., Proutski V., Lathouwers D., de Kloet E.R., and Vreugdenhil E. The effect of chronic exposure to highly aggressive mice on hippocampal gene expression of non-aggressive subordinates. Brain Res. 1089 (2006) 10-20
75. Ferry B., Magistretti P.J., and Pralong E. Noradrenaline modulates glutamate-mediated neurotransmission in the rat basolateral amygdala in vitro. Eur. J. Neurosci. 9 (1997) 1356-1364
76. Fontella F.U., Vendite D.A., Tabajara A.S., Porciuncula L.O., da Silva Torres I.L., Jardim F.M., Martini L., Souza D.O., Netto C.A., and Dalmaz C. Repeated restraint stress alters hippocampal glutamate uptake and release in the rat. Neurochem. Res. 29 (2004) 1703-1709
77. Fuchs E. Social stress in tree shrews as an animal model of depression: an example of a behavioral model of a CNS disorder. CNS Spectr. 10 (2005) 182-190
78. Gadek-Michalska A., and Bugajski J. Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J. Physiol. Pharmacol. 54 (2003) 449-459
79. Galea L.A., McEwen B.S., Tanapat P., Deak T., Spencer R.L., and Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81 (1997) 689-697
80. Garcia A., Marti O., Valles A., Dal-Zotto S., and Armario A. Recovery of the hypothalamic-pituitary-adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology 72 (2000) 114-125
81. Gilbertson M.W., Shenton M.E., Ciszewski A., Kasai K., Lasko N.B., Orr S.P., and Pitman R.K. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat. Neurosci. 5 (2002) 1242-1247
82. Gould E., McEwen B.S., Tanapat P., Galea L.A., and Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA-receptor activation. J. Neurosci. 17 (1997) 2492-2498
83. Gould E., Tanapat P., McEwen B.S., Flugge G., and Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA 95 (1998) 3168-3171
84. Govindarajan A., Rao B.S., Nair D., Trinh M., Mawjee N., Tonegawa S., and Chattarji S. Transgenic brain-derived neurotrophic factor expression causes both anxiogenic and antidepressant effects. Proc. Natl. Acad. Sci. USA 103 (2006) 13208-13213
85. Gronli J., Bramham C., Murison R., Kanhema T., Fiske E., Bjorvatn B., Ursin R., and Portas C.M. Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacol. Biochem. Behav. 85 (2006) 842-849
86. Harbuz M.S., Windle R.J., Jessop D.S., Renshaw D., Ingram C.D., and Lightman S.L. Differential effects of psychological and immunological challenge on the hypothalamo-pituitary-adrenal axis function in adjuvant-induced arthritis. Ann. N. Y. Acad. Sci. 876 (1999) 43-52
87. Heine V.M., Maslam S., Zareno J., Joëls M., and Lucassen P.J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci. 19 (2004) 131-144
88. Heine V., Zareno J., Maslam S., Joëls M., and Lucassen P.J. Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur. J. Neurosci. 21 (2005) 1304-1314
89. Hellsten J., Wennstrom M., Mohapel P., Ekdahl C.T., Bengzon J., and Tingstrom A. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. Eur. J. Neurosci. 16 (2002) 283-290
90. Herrero A.I., Sandi C., and Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol. Learn Mem. 86 (2006) 150-159
91. Hesen W., and Joëls M. Modulation of 5HT1A responsiveness in CA1 pyramidal neurons by in vivo activation of corticosteroid receptors. J. Neuroendocrinol. 8 (1996) 433-438
92. Hill M.N., Ho W.S., Sinopoli K.J., Viau V., Hillard C.J., and Gorzalka B.B. Involvement of the endocannabinoid system in the ability of long-term tricyclic antidepressant treatment to suppress stress-induced activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 31 (2006) 2591-2599
93. Holderbach R., Clark K., Moreau J.L., Bischofberger J., and Normann C. Enhanced long-term synaptic depression in an animal model of depression. Biol. Psychiatry (2006)
94. Hopkins W.F., and Johnston D. Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science 226 (1984) 350-352
95. Hu Z., Yuri K., Ozawa H., Lu H., and Kawata M. The in vivo time course for elimination of adrenalectomy-induced apoptotic profiles from the granule cell layer of the rat hippocampus. J. Neurosci. 17 (1997) 3981-3989
96. Huang C.C., Hsu K.S., and Gean P.W. Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P- and/or Q-type calcium channels in the rat amygdale. J. Neurosci. 16 (1996) 1026-1033
97. Huang G.J., and Herbert J. The role of 5-HT1A receptors in the proliferation and survival of progenitor cells in the dentate gyrus of the adult hippocampus and their regulation by corticoids. Neuroscience 135 (2005) 803-813
98. Huber D., Veinante P., and Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdale. Science 308 (2005) 245-248
99. Hui Z., Guang-Yu M., Chong-Tao X., Quan Y., and Xiao-Hu X. Phenytoin reverses the chronic stress-induced impairment of memory consolidation for water maze training and depression of LTP in rat hippocampal CA1 region, but does not affect motor activity. Cogn. Brain Res. 24 (2005) 380-385
100. Izquierdo A., Wellman C.L., and Holmes A. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J. Neurosci. 26 (2006) 5733-5738
101. Izumi Y., and Zorumski C.F. Norepinephrine promotes long-term potentiation in the adult rat hippocampus in vitro. Synapse 31 (1999) 196-202
102. Jackson M.E., and Moghaddam B. Distinct patterns of plasticity in prefrontal cortex neurons that encode slow and fast responses to stress. Eur. J. Neurosci. 6 (2006) 1702-1710
103. Jayatissa M.N., Bisgaard C., Tingstrom A., Papp M., and Wiborg O. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 31 (2006) 2395-2404
104. Jedema H.P., and Grace A.A. Chronic exposure to cold stress alters electrophysiological properties of locus coeruleus neurons recorded in vitro. Neuropsychopharmacology 28 (2003) 63-72
105. Jedema H.P., Finlay J.M., Sved A.F., and Grace A.A. Chronic cold exposure potentiates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons. Biol. Psychiatry 49 (2001) 351-359
106. Joëls M. Steroid hormones and excitability in the mammalian brain. Front Neuroendocrinol. 18 (1997) 2-48
107. Joëls M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sci. 27 (2006) 244-250
108. Joëls M., and de Kloet E.R. Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 245 (1989) 1502-1505
109. Joëls M., and de Kloet E.R. Corticosteroid actions on amino acid-mediated transmission in rat CA1 hippocampal cells. J. Neurosci. 13 (1993) 4082-4090
110. Joëls M., Pu Z., Wiegert O., Oitzl M.S., and Krugers H.J. Learning under stress: how does it work?. Trends Cogn. Sci. 10 (2006) 152-158
111. Joëls M., Stienstra C.M., and Karten Y.J. Effect of adrenalectomy on membrane properties and synaptic potentials in rat dentate granule cells. J. Neurophysiol. 85 (2001) 699-707
112. Joëls M., Velzing E., Nair S., Verkuyl J.M., and Karst H. Acute stress increases calcium current amplitude in rat hippocampus: temporal changes in physiology and gene expression. Eur. J. Neurosci. 18 (2003) 1315-1324
113. Johnson E.O., Kamilaris T.C., Carter C.S., Calogero A.E., Gold P.W., and Chrousos G.P. The biobehavioral consequences of psychogenic stress in a small, social primate (Callithrix jacchus jacchus). Biol. Psychiatry 40 (1996) 317-337
114. Jurgens C.W., Rau K.E., Knudson C.A., King J.D., Carr P.A., Porter J.E., and Doze V.A. Beta1 adrenergic receptor-mediated enhancement of hippocampal CA3 network activity. J. Pharmacol. Exp. Ther. 314 (2005) 552-556
115. Karst H., and Joëls M. Effect of chronic stress on synaptic currents in rat hippocampal dentate gyrus neurons. J. Neurophysiol. 89 (2003) 625-633
116. Karst H., and Joëls M. Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J. Neurophysiol. 94 (2005) 3479-3486
117. Karst H., and Joëls M. Brief RU 38486 treatment normalizes the effects of chronic stress on calcium currents in rat, hippocampal ca1 neurons. Neuropsychopharmacology (2007)
118. Karst H., Berger S., Turiault M., Tronche F., Schutz G., and Joëls M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. USA 102 (2005) 19204-19207
119. Karst H., Karten Y.J., Reichardt H.M., de Kloet E.R., Schutz G., and Joëls M. Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers. Nat. Neurosci. 3 (2000) 977-978
120. Karst H., Nair S., Velzing E., Rumpff-van Essen L., Slagter E., Shinnick-Gallagher P., and Joëls M. Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons. Eur. J. Neurosci. 16 (2002) 1083-1089
121. Karst H., Wadman W.J., and Joëls M. Corticosteroid receptor-dependent modulation of calcium currents in rat hippocampal CA1 neurons. Brain Res. 649 (1994) 234-242
122. Karten Y.J., Nair S.M., van Esssen L., Silburg R., and Joëls M. Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc. Natl. Acad. Sci. USA 96 (1999) 13456-13461
123. Karten Y.J., Slagter E., and Joëls M. Effect of long-term elevated corticosteroid levels on field responses to synaptic stimulation, in the rat CA1 hippocampal area. Neurosci. Lett. 265 (1999) 41-44
124. Karten Y.J., Stienstra C.M., and Joëls M. Corticosteroid effects on serotonin responses in granule cells of the rat dentate gyrus. J. Neuroendocrinol. 13 (2001) 233-238
125. Kavushansky A., Vouimba R.M., Cohen H., and Richter-Levin G. Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus 16 (2006) 35-42
126. Keller J., and Schatzberg A.F. Clinical and biological effects of mifepristone treatment for psychotic treatment. Neuropsychopharmacology 31 (2006) 2597-2795
127. Kempermann G., Jessberger S., Steiner B., and Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27 (2004) 447-452
128. Kerr D.S., Campbell L.W., Hao S.Y., and Landfield P.W. Corticosteroid modulation of hippocampal potentials: increased effect with aging. Science 245 (1989) 1505-1509
129. Kerr D.S., Campbell L.W., Applegate M.D., Brodish A., and Landfield P.W. Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J. Neurosci. 11 (1991) 1316-1324
130. Kerr D.S., Campbell L.W., Thibault O., and Landfield P.W. Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca2+ conductances: relevance to brain aging. Proc. Natl. Acad. Sci. USA 89 (1992) 8527-8531
131. Kim J.J., and Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3 (2002) 453-462
132. Kim J.J., Koo J.W., Lee H.J., and Han J.S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J. Neurosci. 25 (2005) 1532-1539
133. Kim J.J., Lee H.J., Han J.S., and Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J. Neurosci. 21 (2001) 5222-5228
134. Kitayama N., Vaccarino V., Kutner M., Weiss P., and Bremner J.D. Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis. J. Affect Disord. 88 (2005) 79-86
135. Kitchener P., Di Blasi F., Borrelli E., and Piazza P.V. Differences between brain structures in nuclear translocation and DNA binding of the glucocorticoid receptor during stress and the circadian cycle. Eur. J. Neurosci. 19 (2004) 1837-1846
136. Kitchigina V., Vankov A., Harley C., and Sara S.J. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur. J. Neurosci. 9 (1997) 41-47
137. Kitraki E., Kremmyda O., Youlatos D., Alexis M., and Kittas C. Spatial performance and corticosteroid receptor status in the 21-day restraint stress paradigm. Ann. N. Y. Acad. Sci. 1018 (2004) 323-327
138. Knopfel T., Vranesic I., Gahwiler B.H., and Brown D.A. Muscarinic and beta-adrenergic depression of the slow Ca2(+)-activated potassium conductance in hippocampal CA3 pyramidal cells is not mediated by a reduction of depolarization-induced cytosolic Ca2+ transients. Proc. Natl. Acad. Sci. USA 87 (1990) 4083-4087
139. Kole M.H., Czeh B., and Fuchs E. Homeostatic maintenance in excitability of tree shrew hippocampal CA3 pyramidal neurons after chronic stress. Hippocampus 14 (2004) 742-751
140. Kole M.H.P., Costoli T., Koolhaas J.M., and Fuchs E. Bidirectional shift in the cornu ammonis 3 pyramidal dendritic organization following brief stress. Neuroscience 125 (2004) 337-347
141. Kole M.H., Koolhaas J.M., Luiten P.G., and Fuchs E. High-voltage-activated Ca2+ currents and the excitability of pyramidal neurons in the hippocampal CA3 subfield in rats depend on corticosterone and time of day. Neurosci. Let. 307 (2001) 53-56
142. Kole M.H.P., Swan L., and Fuchs E. The antidepressant tianeptine persistently modulates glutamate receptor currents of the hippocampal CA3 commissural associational synapse tin chronically stressed rat. Eur. J. Neurosci. 16 (2002) 807-816
143. Korz V., and Frey J.U. Stress-related modulation of hippocampal long-term potentiation in rats: involvement of adrenal steroid receptors. J. Neurosci. 19 (2003) 7281-7287
144. Korz V., and Frey J.U. Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J. Neurosci. 25 (2005) 7393-7400
145. Kozorovitskiy Y., and Gould E. Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J. Neurosci. 24 (2004) 6755-6759
146. Krugers H.J., Alfarez D.N., Karst H., Parashkouhi K., Van Gemert N., and Joëls M. Corticosterone shifts different forms of synaptic potentiation in opposite directions. Hippocampus 15 (2005) 697-703
147. Krugers H.J., Goltstein P.M., van der Linden S., and Joëls M. Blockade of glucocorticoid receptors rapidly restores hippocampal CA1 synaptic plasticity after exposure to chronic stress. Eur. J. Neurosci. 23 (2006) 3051-3055
148. Krugers H.J., van der Linden S., van Olst E., Alfarez D.N., Maslam S., Lucassen P.J., and Joëls M. Dissociation between apoptosis, neurogenesis, and synaptic potentiation in the dentate gyrus of adrenalectomized rats. Synapse 61 (2007) 221-230
149. Laaris N., Haj-Dahmane S., Hamon M., and Lanfumey L. Glucocorticoid receptor-mediated inhibition by corticosterone of 5-HT1A autoreceptor functioning in the rat dorsal raphe nucleus. Neuropharmacology 34 (1995) 1201-1210
150. Laaris N., Le Poul E., Laporte A.M., Hamon M., and Lanfumey L. Differential effects of stress on presynaptic and postsynaptic 5-hydroxytryptamine-1A receptors in the rat brain: an in vitro electrophysiological study. Neuroscience 91 (1999) 947-958
151. Lambert K.G., Buckelew S.K., Staffiso-Sandoz G., Gaffga S., Carpenter W., Fisher J., and Kinsley C.H. Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats. Physiol. Behav. 65 (1998) 43-49
152. Landgraf R. Neuropeptides in anxiety modulation. Handb. Exp. Pharmacol. (2005) 335-369
153. Lanfumey L., Pardon M.C., Laaris N., Joubert C., Hanoun N., Hamon M., and Cohen-Salmon C. 5-HT1A autoreceptor desensitization by chronic ultramild stress in mice. Neuroreport 10 (1999) 3369-3374
154. Lee K.J., Kim S.J., Kim S.W., Choi S.H., Shin Y.C., Park S.H., Moon B.H., Cho E., Lee M.S., Choi S.H., Chun B.G., and Shin K.H. Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp. Mol. Med. 38 (2006) 44-54
155. Li Y.F., Chen H.X., Liu Y., Zhang Y.Z., Liu Y.Q., and Li J. Agmatine increases proliferation of cultured hippocampal progenitor cells and hippocampal neurogenesis in chronically stressed mice. Acta Pharmacol. Sin. 27 (2006) 1395-1400
156. Liston C., Miller M.M., Goldwater D.S., Radley J.J., Rocher A.B., Hof P.R., Morrison J.H., and McEwen B.S. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J. Neurosci. 26 (2006) 7870-7874
157. Liu J., Yu B., Neugebauer V., Grigoriadis D.E., Rivier J., Vale W.W., Shinnick-Gallagher P., and Gallagher J.P. Corticotropin-releasing factor and Urocortin I modulate excitatory glutamatergic synaptic transmission. J. Neurosci. 24 (2004) 4020-4029
158. Lowry C.A., Rodda J.E., Lightman S.L., and Ingram C.D. Corticotropin-releasing factor increases in vitro firing rates of serotonergic neurons in the rat dorsal raphe nucleus: evidence for activation of a topographically organized mesolimbocortical serotonergic system. J. Neurosci. 20 (2000) 7728-7736
159. Lu Y.F., Moriwaki A., Tomizawa K., Onuma H., Cai X.H., and Matsui H. Effects of vasopressin and involvement of receptor subtypes in the rat central amygdaloid nucleus in vitro. Brain Res. 768 (1997) 266-272
160. Lucassen P.J., Muller M.B., Holsboer F., Bauer J., Holtrop A., Wouda J., Hoogendijk W.J., de Kloet E.R., and Swaab D.F. Hippocampal apoptosis in major depression is a minor event and absent from subareas at risk for glucocorticoid overexposure. Am. J. Pathol. 158 (2001) 453-468
161. Lucassen P.J., Vollmann-Honsdorf G.K., Gleisberg M., Czeh B., de Kloet E.R., and Fuchs E. Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur. J. Neurosci. 14 (2001) 161-166
162. Luine V. Sex differences in chronic stress effects on memory in rats. Stress 5 (2002) 205-216
163. Lupien S.J., Fiocco A., Wan N., Maheu F., Lord C., Schramek T., and Tu M.T. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30 (2005) 225-242
164. Lynch M.A. Long-term potentiation and memory. Physiol. Rev. 84 (2004) 87-136
165. Magarinos A.M., and McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 69 (1995) 83-88
166. Magarinos A.M., and McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69 (1995) 89-98
167. Magarinos A.M., Deslandes A., and McEwen B.S. Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur. J. Pharmacol. 371 (1999) 113-122
168. Magarinos A.M., McEwen B.S., Flugge G., and Fuchs E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J. Neurosci. 16 (1996) 3534-3540
169. Magarinos A.M., Verdugo J.M., and McEwen B.S. Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. USA 94 (1997) 14002-14008
170. Malberg J.E., and Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28 (2003) 1562-1571
171. Malberg J.E., Eisch A.J., Nestler E.J., and Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000) 9104-9110
172. Malcher-Lopes R., Di S., Marcheselli V.S., Weng F.J., Stuart C.T., Bazan N.G., and Tasker J.G. Opposing crosstalk between leptin and glucocorticoids rapidly modulates synaptic excitation via endocannabinoid release. J. Neurosci. 24 (2006) 6643-6650
173. Manikandan S., Padma M.K., Srikumar R., Jeya Parthasarathy N., Muthuvel A., and Sheela Devi R. Effects of chronic noise stress on spatial memory of rats in relation to neuronal dendritic alteration and free radical-imbalance in hippocampus and medial prefrontal cortex. Neurosci. Lett. 399 (2006) 17-22
174. Marin M.T., Cruz F.C., and Planeta C.S. Chronic restraint or variable stresses differently affect the behavior, corticosterone secretion and body weight in rats. Physiol. Behav. 90 (2007) 29-35
175. Maroun M., and Richter-Levin G. Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J. Neurosci. 11 (2003) 4406-4409
176. Mayer J.L., Klumpers L., Maslam S., de Kloet E.R., Joëls M., and Lucassen P.J. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J. Neuroendocrinol. 18 (2006) 629-631
177. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22 (1999) 105-122
178. McEwen B.S. Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann. N. Y. Acad. Sci. 1032 (2004) 1-7
179. McEwen B.S., Margarinos A.M., and Reagan L.P. Structural plasticity and tianeptine: cellular and molecular targets. Eur. Psychiatry 17 (2002) 318-330
180. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27 (2004) 1-28
181. McKittrick C.R., Blanchard D.C., Blanchard R.J., McEwen B.S., and Sakai R.R. Serotonin receptor binding in a colony model of chronic social stress. Biol. Psychiatry 37 (1995) 383-393
182. McKittrick C.R., Magarinos A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., and Sakai R.R. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36 (2000) 85-94
183. 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
184. Mineur Y.S., Belzung C., and Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav. Brain Res. 175 (2006) 43-50
185. Mirescu C., and Gould E. Stress and adult neurogenesis. Hippocampus 16 (2006) 233-238
186. Mitra R., Jadhav S., McEwen B.S., Vyas A., and Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. USA 102 (2005) 9371-9376
187. Mitra R., Sundlass K., Parker K.J., Schatzberg A.F., and Lyons D.M. Social stress-related behavior affects hippocampal cell proliferation in mice. Physiol. Behav. 89 (2006) 123-127
188. Mizuno Y., Oomura Y., Hori N., and Carpenter D.O. Action of vasopressin on CA1 pyramidal neurons in rat hippocampal slices. Brain Res. 309 (1984) 241-246
189. Moghaddam B. Stress activation of glutamate neurotransmission in the prefrontal cortex: implications for dopamine-associated psychiatric disorders. Biol. Psychiatry 51 (2002) 775-787
190. Moore H., Rose H.J., and Grace A.A. Chronic cold stress reduces the spontaneous activity of ventral tegmental dopamine neurons. Neuropsychopharmacology 24 (2001) 410-419
191. Morilak D.A., Barrera G., Echevarria D.J., Garcia A.S., Hernandez A., Ma S., and Petre C.O. Role of brain norepinephrine in the behavioral response to stress. Prog. Neuropsychopharmacol. Biol. Psychiatry 29 (2005) 1214-1224
192. Muhlethaler M., Charpak S., and Dreifuss J.J. Contrasting effects of neurohypophysial peptides on pyramidal and non-pyramidal neurones in the rat hippocampus. Brain Res. 308 (1984) 97-107
193. Muller M.B., Lucassen P.J., Yassouridis A., Hoogendijk W.J., Holsboer F., and Swaab D.F. Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur. J. Neurosci. 14 (2001) 1603-1612
194. Muller M.B., Zimmermann S., Sillaber I., Hagemeyer T.P., Deusiing J.M., Timpl P., Kormann M.S., Droste S.K., Kuhn R., Reul J.M., Holsboer F., and Wurst W. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nat. Neurosci. 6 (2003) 1100-1107
195. Murakami S., Imbe H., Morikawa Y., Kubo C., and Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci. Res. 53 (2005) 129-139
196. Nacher J., Gomez-Climent M.A., and McEwen B. Chronic non-invasive glucocorticoid administration decreases polysialylated neural cell adhesion molecule expression in the adult rat dentate gyrus. Neurosci. Lett. 370 (2004) 40-44
197. Nacher J., Pham K., Gil-Fernandez V., and McEwen B.S. Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience 126 (2004) 503-509
198. Nair A., Vadodaria K.C., Banerjee S.B., Benekareddy M., Dias B.G., Duman R.S., and Vaidya V.A. Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic amp response element-binding protein expression in the postnatal and adult rat hippocampus. Neuropsychopharmacology (2006) [Epub ahead of print]
199. Nair S.M., Karst H., Dumas T., Philips R., M Sapolsky R., Rumpff-van Essen L., Maslam S., Lucassen P.J., and Joëls M. Gene expression profiles associated with survival of individual rat dentate cells after endogenous corticosteroid deprivation. Eur. J. Neurosci. 20 (2004) 3233-3243
200. Nakao K., Matsuyama K., Matsuki N., and Ikegaya Y. Amygdala stimulation modulates hippocampal synaptic plasticity. Proc. Natl. Acad. Sci. USA 101 (2004) 14270-14275
201. Nemeroff C.B., and Vale W.W. The neurobiology of depression: inroads to treatment and new drug discovery. J. Clin. Psychiatry 66 Suppl. 7 (2005) 5-13
202. Nie Z., Schweitzer P., Roberts A.J., Madamba S.G., Moore S.D., and Siggins G.R. Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 303 (2004) 1512-1514
203. Ohl F., and Fuchs E. Memory performance in tree shrews: effects of stressful experiences. Neurosci. Biobehav. Rev. 23 (1998) 319-323
204. Okuhara D.Y., and Beck S.G. Corticosteroids influence the action potential firing pattern of hippocampal subfield CA3 pyramidal cells. Neuroendocrinology 67 (1998) 58-66
205. J.E. Olijslagers, E.R. de Kloet, M. Joëls, H. Karst, Rapid enhancement of hippocampal glutamate transmission by corticosterone is mediated via the MEK/ERK pathway. FENS Forum Meeting 2006, abstract 152.17.
206. Pascual-Le Tallec L., and Lombes M. The mineralocorticoid receptor: a journey exploring its diversity and specificity of action. Mol. Endocrinol. 19 (2005) 2211-2221
207. Pavcovich L.A., Cancela L.M., Volosin M., Molina V.A., and Ramirez O.A. Chronic stress-induced changes in locus coeruleus neuronal activity. Brain Res. Bull. 24 (1990) 293-296
208. Pavlides C., and McEwen B.S. Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field. Brain Res. 851 (1999) 204-214
209. Pavlides C., Kimura A., Magarinos A.M., and McEwen B.S. Hippocampal homosynaptic long-term depression/depotentiation induced by adrenal steroids. Neurosciences 68 (1995) 379-385
210. Pavlides C., Nivon L.G., and McEwen B.S. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12 (2002) 245-257
211. Pavlides C., Watanabe Y., and McEwen B.S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 3 (1993) 183-192
212. Pawlak R., Rao B.S., Melchor J.P., Chattarji S., McEwen B., and Strickland S. Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc. Natl. Acad. Sci. USA 102 (2005) 18201-18206
213. Pernar L., Curtis A.L., Vale W.W., Rivier J.E., and Valentino R.J. Selective activation of corticotropin-releasing factor-2 receptors on neurochemically identified neurons in the rat dorsal raphe nucleus reveals dual actions. J. Neurosci. 24 (2004) 1305-1311
214. Pfaff D.W., Silva M.T., and Weiss J.M. Telemetered recording of hormone effects on hippocampal neurons. Science 172 (1971) 394-395
215. Pham K., Nacher J., Hof P.R., and McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17 (2003) 879-886
216. Qin Y., Karst H., and Joëls M. Chronic unpredictable stress alters gene expression in rat single dentate granule cells. J. Neurochem. 89 (2004) 364-374
217. Radecki D.T., Brown L.M., Martinez J., and Teyler T.J. BDNF protects against stress-induced impairments in spatial learning and memory and LTP. Hippocampus 15 (2005) 246-253
218. Radley J.J., Rocher A.B., Janssen W.G.M., Hof P.R., McEwen B.S., and Morrison J.H. Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp. Neurol. 196 (2005) 199-203
219. Radley J.J., Rocher A.B., Miller M., Janssen W.G., Liston C., Hof P.R., McEwen B.S., and Morrison J.H. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb. Cortex. 16 (2006) 313-320
220. Radley J.J., Sisti H.M., Hao J., Rocher A.B., McCall T., Hof P.R., McEwen B.S., and Morrison J.H. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125 (2004) 1-6
221. Rainnie D.G., Fernhout B.J., and Shinnick-Gallagher P. Differential actions of corticotropin releasing factor on basolateral and central amygdaloid neurones, in vitro. J. Pharmacol. Exp. Ther. 263 (1992) 846-858
222. Rajkowska G., Miguel-Hidalgo J.J., Dubey P., Stockmeier C.A., and Krishnan K.R. Prominent reduction in pyramidal neurons density in the orbitofrontal cortex of elderly depressed patients. Biol. Psychiatry 58 (2005) 297-306
223. Reber S.O., Birkeneder L., Veenema A.H., Obermeier F., Falk W., Straub R.H., and Neumann I.D. Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 148 (2007) 670-682
224. Retana-Marquez S., Bonilla-Jaime H., Vazquez-Palacios G., Dominguez-Salazar E., Martinez-Garcia R., and Velazquez-Moctezuma J. Body weight gain and diurnal differences of corticosterone changes in response to acute and chronic stress in rats. Psychoneuroendocrinology 28 (2003) 207-227
225. Reul J.M., Stec I., Soder M., and Holsboer F. Chronic treatment of rats with the antidepressant amitriptyline attenuates the activity of the hypothalamic-pituitary-adrenocortical system. Endocrinology 133 (1993) 312-320
226. Roozendaal B. 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25 (2000) 213-238
227. Rosenbrock H., Koros E., Bloching A., Podhorna J., and Borsini F. Effect of chronic intermittent restraint stress on hippocampal expression of marker proteins for synaptic plasticity and progenitor cell proliferation in rats. Brain Res. 1040 (2005) 55-63
228. 2+ and ATP. J. Physiol. 470 (1993) 705-729
229. Saal D., Dong Y., Bonci A., and Malenka R.C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37 (2003) 577-582
230. Sabban E.L., and Kvetnansky R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci. 24 (2001) 91-98
231. Salaria S., Chana G., Caldara F., Feltrin E., Altieri M., Faggioni F., Domenici E., Merlo-Pich E., and Everall I.P. Microarray analysis of cultured human brain aggregates following cortisol exposure: implications for cellular functions relevant to mood disorders. Neurobiol. Dis. 23 (2006) 630-636
232. Sanchez M.M., Aguado F., Sanchez-Toscano F., and Saphier D. Effects of prolonged social isolation on responses of neurons in the bed nucleus of the stria terminalis, preoptic area, and hypothalamic paraventricular nucleus to stimulation of the medial amygdala. Psychoneuroendocrinology 20 (1995) 525-541
233. Sanchez M.M., Ladd C.O., and Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 13 (2001) 419-449
234. Sanchez M.M., Aguado F., Sanchez-Toscano F., and Saphier D. Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139 (1998) 579-587
235. Sandi C. Stress, cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci. 12 (2004) 917-930
236. Sandi C., Davies H.A., Cordero M.I., Rodriguez J.J., Popov V.I., and Stewart M.G. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur. J. Neurosci. 17 (2003) 2447-2456
237. Sandi C., Merino J.J., Cordero M.I., Touyarot K., and 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 102 (2001) 329-339
238. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
239. Saphier D., and Feldman S. Iontophoretic application of glucocorticoids inhibits identified neurones in the rat paraventricular nucleus. Brain Res. 453 (1988) 183-190
240. Sapolsky R.M. Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress (1996) 1-19
241. Sapolsky R.M., and Mott G.E. Social subordinance in wild baboons is associated with suppressed high density lipoprotein-cholesterol concentrations: the possible role of chronic social stress. Endocrinology 121 (1987) 1605-1610
242. Sapolsky R.M., Krey L.C., and McEwen B.S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5 (1985) 1222-1227
243. Seckl J.R., and Fink G. Antidepressants increase glucocorticoid and mineralocorticoid receptor mRNA expression in rat hippocampus in vivo. Neuroendocrinology 55 (1992) 621-626
244. Seib L.M., and Wellman C.L. Daily injections alter spine density in rat medial prefrontal cortex. Neurosci. Lett. 337 (2003) 29-32
245. Sheline Y.I., Gado M.H., and Kraemer H.C. Untreated depression and hippocampal volume loss. Am. J. Psychiatry 160 (2003) 1516-1518
246. Shors T.J. Stressful experience and learning across the lifespan. Annu. Rev. Psychol. 57 (2006) 55-85
247. Shors T.J., and Dryver J. Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus. Brain Res. 666 (1994) 232-238
248. Shors T.J., Chua C., and Falduto J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 21 (2001) 6292-6297
249. Sloviter R.S., Valiquette G., Abrams G.M., Ronk E.C., Sollas A.l., Paul L.A., and Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 243 (1989) 535-538
250. Smith M.A., Makino S., Kvetnansky R., and Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 15 (1995) 1768-1777
251. Sousa N., Lukoyanov N.V., Madeira M.D., Almeida O.F., and Paula-Barbosa M.M. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97 (2000) 253-266
252. Stanton P.K., and Sarvey J.M. Norepinephrine regulates long-term potentiation of both the population spike and dendritic EPSP in hippocampal dentate gyrus. Brain Res. Bull. 18 (1987) 115-119
253. Stewart M.G., Davies H.A., Sandi C., Kraev I.V., Rogachevsky V.V., Peddie C.J., Rodriguez J.J., Cordero M.I., Donohue H.S., Gabbott P.L.A., and Popov I.V. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 131 (2005) 43-54
254. Stienstra C.M., and Joëls M. Effect of corticosteroid treatment in vitro on adrenalectomy-induced impairment of synaptic transmission in the rat dentate gyrus. Neuroendocrinology 12 (2000) 199-205
255. Stienstra C.M., van der Graaf F., Bosma A., Karten K.Y., Hesen W., and Joëls M. Synaptic transmission in the rat dentate gyrus after adrenalectomy. Neuroscience 85 (1998) 1061-1071
256. Stranahan A.M., Khalil D., and Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci. 9 (2006) 526-533
257. Straube T., Korz V., and Frey J.U. Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neurosci. Lett. 344 (2003) 5-8
258. Strohle A., and Holsboer F. Stress responsive neurohormones in depression and anxiety. Pharmacopsychiatry 36 Suppl. 3 (2003) S207-S214
259. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A., and Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 437 (2001) 496-504
260. Tasker J.G., Di S., and Malcher-Lopes R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 147 (2006) 5549-5556
261. Tata D.A., Marciano V.A., and Anderson B.J. Synapse loss from chronically elevated glucocorticoids: relationship to neuropil volume and cell number in hippocampal area CA3. J. Comp. Neurol. 498 (2006) 363-374
262. Thomas R.M., Urban J.H., and Peterson D.A. Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus. Exp. Neurol. 201 (2006) 308-315
263. Tronche F., Kellendonk C., Kretz O., Gass P., Anlag K., Orban P.C., Bock R., Klein R., and Schutz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23 (1999) 99-103
264. Tsankova N.M., Berton O., Renthal W., Kumar A., Neve R.L., and Nestler E.J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9 (2006) 519-525
265. Ungless M.A., Singh V., Crowder T.L., Yaka R., Ron D., and Bonci A. Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron 39 (2003) 401-407
266. Uno H., Eisele S., Sakai A., Shelton S., Baker E., DeJesus O., and Holden J. Neurotoxicity of glucocorticoids in the primate brain. Horm. Behav. 28 (1994) 336-348
267. Urban I.J. Effects of vasopressin and related peptides on neurons of the rat lateral septum and ventral hippocampus. Prog. Brain Res. 119 (1998) 285-310
268. Valentino R.J., and van Bockstaele E. Opposing regulation of the locus coeruleus by corticotropin-releasing factor and opioids. Psychopharmacology 158 (2001) 331-342
269. Van der Borght K., Wallinga A.E., Luiten P.G., Eggen B.J., and van der Zee E.A. Morris water maze learning in two rat strains increases the expression of the polysialylated form of the neural cell adhesion molecule in the dentate gyrus but has no effect on hippocampal neurogenesis. Behav. Neurosci. 119 (2005) 926-932
270. Van der Hart M.G., Czeh B., de Biurrun G., Michaelis T., Watanabe T., Natt O., Frahm J., and Fuchs E. Substance P receptor antagonist and clomipramine prevent stress-induced alterations in cerebral metabolites, cytogenesis in the dentate gyrus and hippocampal volume. Mol. Psychiatry 7 (2002) 933-941
271. Van Gemert N., and Joëls M. Effect of chronic stress and mifepristone treatment on voltage-dependent Ca2+ currents in rat hippocampal dentate gyrus. J. Neuroendocrinol. 18 (2006) 732-741
272. Van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
273. Van Riel E., Meijer O.C., Steenbergen P.J., and Joëls M. Chronic unpredictable stress causes attenuation of serotonin responses in cornu ammonis 1 pyramidal neurons. Neuroscience 120 (2003) 649-658
274. Venero C., Tilling T., Hermans-Borgmeyer I., Schmidt R., Schachner M., and Sandi C. Chronic stress induces opposite changes in the mRNA expression of the cell adhesion molecules NCAM and L1. Neuroscience 115 (2002) 1211-1219
275. Verkuyl M., Hemby S.E., and Joëls M. Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur. J. Neurosci. 20 (2004) 1665-1673
276. Verkuyl M., Karst H., and Joëls M. GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur. J. Neurosci. 21 (2005) 113-121
277. Vidal C., Jordan W., and Zieglgansberger W. Corticosterone reduces the excitability of hippocampal pyramidal cells in vitro. Brain Res. 383 (1986) 54-59
278. Videbech P., and Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am. J. Psychiatry 161 (2004) 1957-1966
279. Vollmann-Honsdorf K., Flugge G., and Fuchs E. Chronic psychosocial stress does not affect the number of pyramidal neurons in tree shrew hippocampus. Neurosci. Lett. 233 (1997) 121-124
280. Vollmayr B., Simonis C., Weber S., Gass P., and Henn F. Reduced cell proliferation in the dentate gyrus is not correlated with the development of learned helplessness. Biol. Psychiatry 54 (2003) 1035-1040
281. Von Frijtag J.C., Kamal A., Reijmers L.G., Schrama L.H., van den Bos R., and Spruijt B.M. Chronic imipramine treatment partially reverses the long-term changes of hippocampal synaptic plasticity in socially stressed rats. Neurosci. Lett. 309 (2001) 153-156
282. Vouimba R.M., Yaniv D., and Richter-Levin G. Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1. Neuropharmacology 52 (2007) 244-252
283. Vyas A., Jadhav S., and Chattarji S. Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 143 (2006) 387-393
284. Vyas A., Mitra R., Shankaranarayana Rao B.S., and Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 22 (2002) 6810-6818
285. Vyas A., Pillai G., and Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128 (2004) 667-673
286. Warner-Schmidt J.L., and Duman R.S. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16 (2006) 239-249
287. Watanabe Y., Gould E., Cameron H.A., Daniels D.C., and McEwen B.S. Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2 (1992) 431-435
288. Watanabe Y., Gould E., and McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588 (1992) 341-345
289. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J. Neurobiol. 49 (2001) 245-253
290. Westenbroek C., den Boer J.A., Veenhuis M., and ter Horst G.J. Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res. Bull. 64 (2004) 303-308
291. Wiegert O., Joëls M., and Krugers H. Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learn Mem. 13 (2006) 110-113
292. O. Wiegert, M. Joëls, J.M. Henley, H.J. Krugers, Corticosteroid hormones and synaptic plasticity; glutamate receptors on the move, SfN Meeting 2006, abstract 232.18.
293. Wong E.Y., and Herbert J. The corticoid environment: a determining factor for neural progenitors' survival in the adult hippocampus. Eur. J. Neurosci. 20 (2004) 2491-2498
294. Wong E.Y., and Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur. J. Neurosci. 22 (2005) 785-792
295. Wong E.Y., and Herbert J. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137 (2006) 83-92
296. Woolley C.S., Gould E., and McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 31 (1990) 225-231
297. Wossink J., Karst H., Mayboroda O., and Joëls M. Morphological and functional properties of rat dentate granule cells after adrenalectomy. Neuroscience 108 (2001) 263-272
298. Wright R.L., Lightner E.N., Harman J.S., Meijer O.C., and Conrad C.D. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur. J. Neurosci. 24 (2006) 595-605
299. Xu H., Chen Z., He J., Haimanot S., Li X., Dyck L., and Li X.M. Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress-induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 16 (2006) 551-559
300. Xu H., Luo C., Richardson J.S., and Li X.M. Recovery of hippocampal cell proliferation and BDNF levels, both of which are reduced by repeated restraint stress, is accelerated by chronic venlafaxine. Pharmacogenomics J. 4 (2004) 322-331
301. Xu L., Anwyl R., and Rowan M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394 (1998) 891-894
302. Yamada K., McEwen B.S., and Pavlides C. Site and time dependent effects of acute stress on hippocampal long-term potentiation in freely behaving rats. Exp. Brain Res. 152 (2003) 52-59
303. Yehuda R. Advances in understanding neuroendocrine alterations in PTSD and their therapeutic implications. Ann. N. Y. Acad. Sci. 1071 (2006) 137-166
304. Zheng H., Yang Q., and Xu C.T. Effects of chronic stress and phenytoin on the long-term potentiation (LTP) in rat hippocampal CA1 region. Acta Biochim. Biophys. Sin. 36 (2004) 375-378