Overcoming the Effects of Stress on Synaptic Plasticity in the Intact Hippocampus: Rapid Actions of Serotonergic and Antidepressant Agents

Journal of Neuroscience

Volumn 22, Issue 9, 2002, Pages 3638-3644

  Shakesby, Alison C ^a   Anwyl, Roger ^a   Rowan, Michael J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

5 hydroxytryptamine; Acute stress; Antidepressant; Fenfluramine; Fluoxetine; In vivo; Long term potentiation; Synaptic plasticity; Tianeptine

Indexed keywords

ANTIDEPRESSANT AGENT; FENFLURAMINE; FLUOXETINE; SEROTONIN; SEROTONIN AGONIST; TIANEPTINE; CORTICOSTERONE; SEROTONIN RECEPTOR AFFECTING AGENT; SEROTONIN UPTAKE INHIBITOR; THIAZEPINE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENANTIOMER; HIPPOCAMPUS; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RACEMIC MIXTURE; RAT; SEROTONIN UPTAKE; STRESS; ANIMAL; BLOOD; DRUG ANTAGONISM; ELECTRODE; EXCITATORY POSTSYNAPTIC POTENTIAL; EXERCISE TEST; LONG TERM POTENTIATION; PHYSIOLOGY; SYNAPSE; WISTAR RAT;

ANIMALS; ANTIDEPRESSIVE AGENTS; CORTICOSTERONE; DRUG ANTAGONISM; ELECTRODES, IMPLANTED; EXCITATORY POSTSYNAPTIC POTENTIALS; EXERCISE TEST; FENFLURAMINE; FLUOXETINE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SEROTONIN; SEROTONIN AGENTS; SEROTONIN UPTAKE INHIBITORS; STRESS; SYNAPSES; THIAZEPINES;

EID: 0036581111     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-09-03638.2002     Document Type: Article

References (74)

1. Acsady L, Arabadzisz D, Katona I, Freund TF (1996) Topographical distribution of dorsal and median raphe neurons with hippocampal, septal and dual projection. Acta Biol Hung 47:9-19.
2. Amat J, Matus-Amat P, Watkins L, Maier S (1998) Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Res 797:12-22.
3. Azmitia EC (1981) Bilateral serotonergic projections to the dorsal hippocampus of the rat: simultaneous localization of 3H-5HT and HRP after retrograde transport. J Comp Neurol 203:737-743.
4. Barnes N, Sharp T (2000) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152.
5. Bliss T, Goddard G, Riives M (1983) Reduction of long-term potentiation in the dentate gyrus of the rat following selective depletion of monoamines. J Physiol (Lond) 334:475-491.
6. Broqua P, Baudrie V, Laude D, Chaouloff F (1992) Influence of the novel antidepressant tianeptine on neurochemical, neuroendocrinological, and behavioral effects of stress in rats. Biol Psychiatry 31:391-400.
7. Chaouloff F, Berton O, Mormede P (1999) Serotonin and stress. Neuropsychopharmacology 21:28S-32S.
8. Conrad C, Galea L, Kuroda Y, McEwen B (1996) Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110:1321-1334.
9. Corradetti R, Ballerini L, Pugliese A, Pepeu G (1992) Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices. Neuroscience 46:511-518.
10. Czéh 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.
11. de Kloet ER (2000) Stress in the brain. Eur J Pharmacol 405:187-198.
12. de Quervain D-F, Roozendaal B, McGaugh J (1998) Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394:787-790.
13. De Simoni M, De Luigi A, Clavenna A, Manfridi A (1992) In vivo studies on the enhancement of serotonin uptake by tianeptine. Brain Res 574:93-97.
14. Delbende C, Tranchand Bunel D, Tarozzo G, Grino M, Oliver C, Mocaer E, Vaudry H (1994) Effect of chronic treatment with the antidepressant tianeptine on the hypothalamic-pituitary-adrenal axis. Eur J Pharmacol 251:245-251.
15. Diamond DM, Bennett MC, Stevens KE, Wilson RL, Rose GM (1990) Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat. Psychobiology 18:273-281.
16. Diamond DM, Fleshner M, Ingersoll N, Rose RM (1996) Psychological stress impairs spatial working memory: Relevance to electrophysiological studies of hippocampal function. Behav Neurosci 110:661-672.
17. Dresse A, Scuvee-Moreau J (1988) Electrophysiological effects of tianeptine on rat locus coeruleus, raphe dorsalis and hippocampus activity. Clin Neuropharmacol [Suppl 2] 11:S55-S58.
18. Duman R, Malberg J, Nakagawa S, D'Sa C (2000) Neuronal plasticity and survival in mood disorders. Biol Psychiat 48:732-739.
19. Edwards E, Kornrich W, Houtten P, Henn F (1993) Presynaptic serotonin mechanisms in rats subjected to inescapable shock. Neuropharmacology 31:323-330.
20. Fattaccini C, Bolaños-Jimenez F, Gozlan H, Hamon M (1990) Tianeptine stimulates uptake of 5-hydroxytryptamine in vivo in the rat brain. Neuropharmacology 29:1-8.
21. Garcia R (2001) Stress, hippocampal plasticity, and spatial learning. Synapse 40:180-183.
22. Ge J, Barnes NM, Costall B, Naylor RJ (1997) Effect of aversive stimulation on 5-hydroxytryptamine and dopamine metabolism in the rat brain. Pharmacol Biochem Behav 58:775-783.
23. Graeff F, Guimaraes F, DeAndrade T, Deakin J (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129-141.
24. Grahn R, Will M, Hammack S, Maswood S, McQueen M, Watkins L, Maier S (1999) Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 826:35-43.
25. Healy D, Drugan R (1996) Escapable stress modulates retention of spatial learning in rats: preliminary evidence for involvement of neurosteroids. Psychobiology 24:110-117.
26. Hervas I, Artigas F (1998) Effect of fluoxetine on extracellular 5-hydroxytryptamine in rat brain. Role of 5-HT autoreceptors. Eur J Pharmacol 358:9-18.
27. Imai H, Steindler DA, Kitai ST (1986) The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 243:363-380.
28. Izquierdo I, Medina JH (1997) The biochemistry of memory formation and its regulation by hormones and neuromodulators. Psychobiology 25:1-9.
29. Jacobs BL, Fornal CA (1999) Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21:9S-15S.
30. Joëls M (2001) Corticosteroid actions in the hippocampus. J Neuroendocrinol 13:657-669.
31. Joseph MH, Kennett GA (1983) Stress-induced release of 5-HT in the hippocampus and its dependence on increased tryptophan availability: an in vivo electrochemical study. Brain Res 270:251-257.
32. Kim J, Yoon K (1998) Stress: metaplastic effects in the hippocampus. Trends Neurosci 21:505-509.
33. Kim J, Lee H, Han J, Packard M (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21:5222-5228.
34. 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.
35. Kirby LG, Chou-Green JM, Davis K, Lucki I (1997) The effects of different stressors on extracellular 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 760:218-230.
36. Köhler C, Steinbusch H (1982) Identification of serotonin and non-serotonin-containing neurons of the mid-brain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain. Neuroscience 7:951-975.
37. Labrid C, Mocaër E, Kamoun A (1992) Neurochemical and pharmacological properties of tianeptine, a novel antidepressant. Br J Psychiat [Suppl 15] 160:56-60.
38. Leung LS (1979) Orthodromic activation of hippocampal CA1 region of the rat. Brain Res 176:49-63.
39. Levkovitz Y, Grisaru N, Segal M (2001) Transcranial magnetic stimulation and antidepressive drugs share similar cellular effects in rat hippocampus. Neuropsychopharmacology 24:608-616.
40. Magarinos A, Deslandes A, BS M (1999) Effects of antidepressants and benzodiazepines on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 371:113-122.
41. Malagie I, Deslandes A, Gardier A (2000) Effects of acute and chronic tianeptine administration on serotonin outflow in rats: comparison with paroxetine by using in vivo microdialysis. Eur J Pharmacol 403:55-65.
42. Martin S, Grimwood P, Morris R (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
43. Matsumoto M, Togashi H, Mori K, Ueno K, Ohashi S, Kojima T, Yoshioka M (2001) Evidence for involvement of central 5-HT(4) receptors in cholinergic function associated with cognitive processes: behavioral, electrophysiological, and neurochemical studies. J Pharmacol Exp Ther 296:676-682.
44. McEwen B (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
45. McEwen B, Magarinos A (2001) Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol Clin Exp 16:S7-S19.
46. McGaugh J (2000) Memory: a century of consolidation. Science 287:248-251.
47. Matsuo M, Kataoka Y, Mataki S, Kato Y, Oi K (1996) Conflict situation increases serotonin release in rat dorsal hippocampus: in vivo study with microdialysis and Vogel test. Neurosci Lett 215:197-200.
48. 3H]5-hydroxytryptamine uptake in rat brain synaptosomes: protective effects of buspirone and tianeptine. Eur J Pharmacol 14:255-260.
49. Nowakowska E, Kus K, Chodra A, Rybakowski J (2000) Behavioural effects of fluoxetine and tianeptine, two antidepressants with opposite action mechanisms, in rats. Arzneim Forsch 50:5-10.
50. Oluyomi A, Datla K, Curzon G (1997) Effects of (+) and (-) enantiomers of the antidepressant drug tianeptine on 5-HT-induced behaviour. Neuropharmacology 36:383-387.
51. Park SP, Lopez-Rodriguez F, Wilson CL, Maidment N, Matsumoto Y, Engel J (1999) In vivo microdialysis measures of extracellular serotonin in the rat hippocampus during sleep-wakefulness. Brain Res 833:291-296.
52. Passani M, Pugliese A, Azzurrini M, Corradetti R (1994) Effects of DAU 6215, a novel 5-hydroxytryptamine3 (5-HT3) antagonist on electrophysiological properties of the rat hippocampus. Br J Pharmacol 112:695-703.
53. Pineyro G, Deveault L, Blier P, Dennis T, de Montigny C (1995) Effect of acute and prolonged tianeptine administration on the 5-HT transporter: electrophysiological, biochemical and radioligand binding studies in the rat brain. Naunyn Schmiedebergs Arch Pharmacol 351:111-118.
54. Reid I, Stewart C (2001) How antidepressants work - New perspectives on the pathology of depressive disorder. Br J Psychiat 178:299-303.
55. Rocher C, Gardier AM (2001) Effects of repeated systemic administration of d-fenfluramine on serotonin and glutamate release in rat ventral hippocampus: comparison with methamphetamine using in vivo microdialysis. Naunyn Schmiedebergs Arch Pharmacol 363:422-428.
56. Roozendaal B (2000) Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25:213-238.
57. Sabol K, Richards J, LS S (1992) Fenfluramine-induced increases in extracellular hippocampal serotonin are progressively attenuated in vivo during a four-day fenfluramine regimen in rats. Brain Res 571:64-72.
58. Sapolsky RM (2001) Depression, antidepressants, and the shrinking hippocampus. Proc Natl Acad Sci USA 98:12320-12232.
59. Shors TJ, Seib T, Levine S, Thompson R (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224-226.
60. Shors TJ, Levine S, Thompson RF (1990) Opioid antagonist eliminates the stress-induced impairment of long-term potentiation (LTP). Brain Res 506:316-318.
61. Shors T, Gallegos R, Breindl A (1997) Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse 26:209-217.
62. Spedding M, Deslandes A, Netzer R, Roeper J, Szabo G, Egyed A (1998) Potentiation of CA1 hippocampal population spike potential by the atypical antidepressant tianeptine. Soc Neurosci Abstr 24:685.
63. Stäubli U, Otaky N (1994) Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA-receptor-mediated responses. Brain Res 643:10-16.
64. Stäubli U, Xu F (1995) Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci 15:2445-2452.
65. Stewart C, Reid I (2000) Repeated ECS and fluoxetine administration have equivalent effects on hippocampal synaptic plasticity. Psychopharmacology 148:217-223.
66. Vahabzadeh A, Fillenz M (1994) Comparison of stress-induced changes in noradrenergic and serotonergic neurons in the rat hippocampus using microdialysis. Eur J Neurosci 6:1205-1212.
67. Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643-668.
68. Vollmayr B, Keck S, Henn F, Schloss P (2000) Acute stress decreases serotonin transporter mRNA in the raphe pontis but not in other raphe nuclei of the rat. Neurosci Lett 25:109-112.
69. Von Frijtag JC, Kamal A, Reijmers LGJE, Schrama LH, van den Bos R, Spruijt BM (2001) Chronic imipramine treatment partially reverses the long-term changes of hippocampal synaptic plasticity in socially stressed rats. Neurosci Lett 309:153-156.
70. Whitton P, Sarna G, Datla K, Curzon G (1991) Effects of tianeptine on stress-induced behavioural deficits and 5-HT dependent behaviour. Psychopharmacology (Berl) 104:81-85.
71. Wilde M, Penfield P (1995) Tianeptine. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic efficacy in depression and coexisting anxiety and depression. Drugs 49:411-439.
72. Wilkinson LS, Humby T, Killcross S, Robbins TW, Everitt BJ (1996) Dissociations in hippocampal 5-hydroxytryptamine release in the rat following Pavlovian aversive conditioning to discrete and contextual stimuli. Eur J Neurosci8:1479-1487.
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 (1998) Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc Natl Acad Sci USA 95:3204-3208.