Stress-related modulation of hippocampal long-term potentiation in rats: Involvement of adrenal steroid receptors

Journal of Neuroscience

Volumn 23, Issue 19, 2003, Pages 7281-7287

  Korz, Volker ^a   Frey, Julietta U ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Corticosterone; Dentate gyrus; Early LTP; Glucocorticoid receptor; Handling; Hippocampal long term potentiation; Late LTP; Mineralocorticoid receptor; Protein synthesis; Reinforcement; Swim stress; adrenoceptors

Indexed keywords

BETA ADRENERGIC RECEPTOR; CORTICOSTEROID RECEPTOR; MINERALOCORTICOID RECEPTOR; STEROID RECEPTOR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; GLUCOCORTICOID RECEPTOR; PROPRANOLOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE RELEASE; DENTATE GYRUS; DRUG RECEPTOR BINDING; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR AFFINITY; REINFORCEMENT; STRESS; SYNAPTIC TRANSMISSION; ADRENAL GLAND; ANIMAL; ANIMAL BEHAVIOR; DRUG ANTAGONISM; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; METABOLISM; MOTIVATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN SYNTHESIS; SWIMMING; WISTAR RAT;

ADRENAL GLANDS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; BEHAVIOR, ANIMAL; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIALS; HANDLING (PSYCHOLOGY); LONG-TERM POTENTIATION; MALE; PROPRANOLOL; PROTEIN BIOSYNTHESIS; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; STRESS; SWIMMING;

EID: 0041737641     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-19-07281.2003     Document Type: Article

References (77)

1. Akirav I, Richter-Levin G (1999) Priming stimulation in the basolateral amygdala modulates synaptic plasticity in the rat dentate gyrus. Neurosci Lett 270:83-86.
2. Akirav I, Richter-Levin G (2002) Mechanisms of amygdala modulation of hippocampal plasticity. J Neurosci 22:9912-9921.
3. Akirav I, Sandi C, Richter-Levin G (2001) Differential activation of hippocampus and amygdala following spatial learning under stress. Eur J Neurosci 14:719-725.
4. Bhargava A, Meijer OC, Dallman MF, Pearce D (2000) Plasma membrane calcium pump isoform 1 gene expression is repressed by corticosterone and stress in rat hippocampus. J Neurosci 20:3129-3138.
5. Cahill L, McGaugh JL (1998) Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 21:294-299.
6. Cato AC, Ponta H, Herrlich P (1992a) Regulation of gene expression by steroid hormones. Prog Nucleic Acid Res Mol Biol 43:1-36.
7. Cato AC, Konig H, Ponta H, Herrlich P (1992b) Steroids and growth promoting factors in the regulation of expression of genes and gene networks. J Steroid Biochem Mol Biol 43:63-68.
8. Cato AC, Nestl A, Mink S (2002) Rapid actions of steroid receptors in cellular signaling pathways. Sci STKE 2002:RE9.
9. Conrad CD, Lupien SJ, McEwen BS (1999) Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiol Learn Mem 72:39-46.
10. De Kloet ER, Oitzl MS, Joels M (1993) Functional implications of brain corticosteroid receptor diversity. Cell Mol Neurobiol 13:433-455.
11. De Kloet ER, Oitzl MS, Joels M (1999) Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422-426.
12. Diamond DM, Bennett MC, Fleshner M, Rose GM (1992) Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2:421-430.
13. Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR (1990) Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249:1266-1272.
14. Douma BR, Korte SM, Buwalda B, la Fleur SE, Bohus B, Luiten PG (1998) Repeated blockade of mineralocorticoid receptors, but not of glucocorticoid receptors impairs food rewarded spatial learning. Psychoneuroendocrinology 23:33-44.
15. Drouin J, Sun YL, Tremblay S, Lavender P, Schmidt TJ, de Lean A, Nemer M (1992) Homodimer formation is rate limiting for high affinity binding by the glucocorticoid receptor. Mol Endocrinol 6:1299-1309.
16. Duman RS, Strada SJ, Enna SJ (1989) Glucocorticoid administration increases receptor-mediated and forskolin-stimulated cyclic AMP accumulation in rat brain cerebral cortical slices. Brain Res 477:166-171.
17. Filipini D, Gijsbers K, Birmingham MK, Kraulis I, Dubrovsky B (1991) Modulation by adrenal steroids of limbic function. J Steroid Biochem Mol Biol 39:245-252.
18. Foy MR, Stanton ME, Levine S, Thompson RF (1987) Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol 48:138-149.
19. Frey S, Bergado-Rosado J, Seidenbecher T, Pape HC, Frey JU (2001) Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci 21:3697-3703.
20. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
21. Frey U, Morris RGM (1998) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545-552.
22. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
23. Gesing A, Bilang-Bleuel A, Droste SK, Linthorst AC, Holsboer F, Reul JM (2001) Psychological stress increases hippocampal mineralocorticoid receptor levels: involvement of corticotropin-releasing hormone. J Neurosci 21:4822-4829.
24. Gilad GM (1987) The stress-induced response of the septo-hippocampal cholinergic system. A vectorial outcome of psychoneuroendocrinological interactions. Psychoneuroendocrinology 12:167-184.
25. Gilad GM, Rabey JM, Gilad VH (1987) Presynaptic effects of glucocorticoids on dopaminergic and cholinergic synaptosomes. Implications for rapid endocrine-neural interactions in stress. Life Sci 40:2401-2408.
26. Heck S, Kullmann M, Gast A, Ponta H, Rahmsdorf HJ, Herrlich P, Cato ACB (1994) A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of the transcription factor AP-1. EMBO J 13:4087-4095.
27. Herman JP (1993) Regulation of adrenocorticosteroid receptor mRNA expression in the central nervous system. Cell Mol Neurobiol 13:349-372.
28. Herman JP, Spencer R (1998) Regulation of hippocampal glucocorticoid receptor gene transcription and protein expression in vivo. J Neurosci 18:7462-7473.
29. Izquierdo I, Medina JH (1995) Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol Learn Mem 63:19-32.
30. Joels M, De Kloet ER (1994) Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Prog Neurobiol 43:1-36.
31. Kant GJ, Michael HY, D'Angelo PC, Brown AJ, Eggleston T (1988) Maze performances: a direct comparison of food vs. water mazes. Pharmacol Biochem Behav 31:487-491.
32. Karst H, Karten YJG, Reichardt HM, De Kloet ER, Schütz G, Joels M (2000) Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers. Nat Neurosci 3:977-978.
33. 2+ conductances: relevance to brain aging. Proc Natl Acad Sci USA 89:8527-8531.
34. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev 3:453-462.
35. Kim JJ, Yoon KS (1998) Stress: metaplastic effects in the hippocampus. Trends Neurosci 21:505-509.
36. Kim JJ, Foy MR, Thompson RF (1996) Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci USA 93:4750-4753.
37. Kim JJ, Lee HJ, Han JS, Packard MG (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21:5222-5228.
38. Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39-42.
39. Li S, Cullen WK, Anwyl R, Rowan MJ (2003) Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 6:526-531.
40. Linthorst ACE, Flachskamm C, Barden N, Holsboer F, Reul JMHM (2000) Glucocorticoid receptor impairment alters CNS responses to a psychological stressor: an in vivo microdialysis study in transgenic mice. Eur J Neurosci 12:283-291.
41. Malkoski SP, Handanos CM, Dorin RI (1997) Localization of a negative glucocorticoid response element of the human corticotropin releasing hormone gene. Mol Cell Endocrinol 127:189-199.
42. Matthies H, Frey U, Reymann K, Krug M, Jork R, Schroeder H (1990) Different mechanisms and multiple stages of LTP. Adv Exp Med Biol 268:359-368.
43. McEwen BS, Weiss JM, Schwartz LS (1968) Selective retention of corticosterone by limbic structures in rat brain. Nature 220:911-912.
44. McGaugh JL (2000) Memory: a century of consolidation. Science 287:248-251.
45. McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210.
46. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
47. Oitzl MS, DeKloet ER (1992) Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 106:62-71.
48. Oitzl MS, Josephy M, Spruijt BM (1993) An ACTH/MSH(4-9) analog counteracts the behavioral effects of a mineralocorticoid receptor antagonist. Pharmacol Biochem Behav 44:447-450.
49. Oitzi MS, Fluttert M, De Kloet ER (1994) The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur J Neurosci 6:1072-1079.
50. Oitzl MS, Reichardt HM, Joels M, De Kloet ER (2001) Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc Natl Acad Sci USA 98:12790-12795.
51. Pavlides C, McEwen BS (1999) Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field. Brain Res 851:204-214.
52. Pavlides C, Watanabe Y, McEwen BS (1993) Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 3:183-192.
53. Pavlides C, Watanabe Y, Magarinos AM, McEwen BS (1995) Opposing roles of type I and type II adrenal steroid receptors in hippocampal long-term potentiation. Neuroscience 68:387-394.
54. Pavlides C, Nivon LG, McEwen BS (2002) Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12:245-257.
55. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
56. Reul JM, De Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505-2511.
57. Reul JM, Pearce PT, Funder JW, Krozowski ZS (1989) Type I and type II corticosteroid receptor gene expression in the rat. Mol Endocrinol 3:1674-1680.
58. Reul JM, Gesing A, Droste S, Stec IS, Weber A, Bachmann C, Bilang-Bleuel A, Holsboer F, Linthorst AC (2000) The brain mineralocorticoid receptor: greedy for ligand, mysterious in function. Eur J Pharmacol 405:235-249.
59. Roozendaal B, Nguyen BT, Power AE, McGaugh JL (1999) Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc Natl Acad Sci USA 96:11642-11647.
60. Roozendaal B, Quirarte GL, McGaugh JL (2002) Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/PKA system in influencing memory consolidation. Eur J Neurosci 15:553-560.
61. Sandi C (1998) The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast 6:41-52.
62. Sandi C, Loscertales M, Guaza C (1997) Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci 9:637-642.
63. Schmidt P, Holsboer F, Spengler D (2001) adrenergic receptors potentiate glucocorticoid receptor transactivation via G-protein beta gamma-subunits and the phosphoinositide 3-kinase pathway. Mol Endocrinol 15:553-564.
64. Seidenbecher T, Reymann KG, Balschun D (1997) A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc Natl Acad Sci USA 94:1494-1499.
65. Shakesby AC, Anwyl R, Rowan MJ (2002) Overcoming the effects of stress on synaptic plasticity in the intact hippocampus: rapid actions of serotonergic and antidepressant agents. J Neurosci 22:3638-3644.
66. Shors TJ (2001) Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol Learn Mem 75:10-29.
67. Shors TJ, Seib TB, Levine S, Thompson RF (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224-226.
68. Smigra M, Nishiyama N, Saito H (1998) Mineralocorticoid receptor-mediated enhancement of neuronal excitability and synaptic plasticity in the dentate gyrus in vivo is dependent on the beta-adrenergic activity. J Neurosci Res 51:593-601.
69. Spanis CW, Bianchin MM, Izquierdo I, McGaugh JL (1999) Excitotoxic basolateral amygdala lesions potentiate the memory impairment effect of muscimol injected into the medial septal area. Brain Res 816:329-336.
70. Stefanski V, Knopf G, Schulz S (2001) Long-term colony housing in Long Evans rats: immunological, hormonal, and behavioral consequences. J Neuroimmunol 114:122-130.
71. Straube T, Korz V, Frey JU (2003) Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neurosci Lett 344:5-8.
72. van Steensel B, van Binnendijk EP, Hornsby CD, van der Voort HT, Krozowski ZS, De Kloet ER, van Driel R (1996) Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. J Cell Sci 109:787-792.
73. Xu L, Anwyl R, Rowan MJ (1997) Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387:497-500.
74. Xu L, Holscher C, Anwyl R, Rowan MJ (1998a) Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc Natl Acad Sci USA 95:3204-3208.
75. Xu L, Anwyl R, Rowan MJ (1998b) Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394:891-894.
76. Zhang XK, Dong JM, Chiu JF (1991) Regulation of alpha-fetoprotein gene expression by antagonism between AP-1 and the glucocorticoid receptor at their overlapping binding site. J Biol Chem 266:8248-8254.
77. Zhou J, Zhang F, Zhang Y (2000) Corticosterone inhibits generation of long-term potentiation in rat hippocampal slice: involvement of brain-derived neurotrophic factor. Brain Res 885:182-191.