Antidepressants differentially modify the extinction of an aversive memory task in female rats

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 37, Issue 1, 2012, Pages 33-40

  Melo, Thieza G ^a   Izídio, Geison S ^a   Ferreira, Luane S ^a   Sousa, Diego S ^a   Macedo, Priscila T ^a   Cabral, Alícia ^a   Ribeiro, Alessandra M ^a   Silva, Regina H ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

Aversive memory; Depression; Fluoxetine; Mirtazapine; Nortriptyline

Indexed keywords

FLUOXETINE; MIRTAZAPINE; NORTRIPTYLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AVERSIVE BEHAVIOR; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DEPRESSION; DRUG EFFICACY; EVENING DOSAGE; FEMALE; FORCED SWIMMING TEST; HOPELESSNESS; LEARNING; LONG TERM CARE; MAZE TEST; MEMORY; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; NONHUMAN; RAT; REINFORCEMENT;

ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; AVOIDANCE LEARNING; EXTINCTION, PSYCHOLOGICAL; FEMALE; FLUOXETINE; MAZE LEARNING; MEMORY; MIANSERIN; NORTRIPTYLINE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR;

EID: 84857786161     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.01.012     Document Type: Article

References (101)

1. American Psychiatric Association (APA) Diagnostic and statistical manual of mental disorders 2000, American Psychatric Association, Washington, DC. 4th Ed.
2. Astur R.S., Tropp J., Sava S., Constable R.T., Marku E.J. Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behav Brain Res 2004, 151:103-115.
3. Austin M.P., Mitchell P., Goodwin G.M. Cognitive deficits in depression: possible implications for functional neuropathology. Br J Psychiatry 2001, 178:200-206.
4. Basso A.M., Gallagher K.B., Mikusa J.P., Rueter L.E. Vogel conflict test: sex differences and pharmacological validation of the model. Behav Brain Res 2011, 218:174-183.
5. Bekker M.H.J., van Mens-Verhulst J. Anxiety disorders: sex differences in prevalence, degree, and background, but gender-neutral treatment. Gend Med 2007, 4:S188-S193.
6. Bengtsson H.J., Kele J., Johansson J., Hjorth S. Interaction of the antidepressant mirtazapine with α2-adrenoceptors modulating the release of 5-HT in different rat brain regions in vivo. Naunyn Schmiedebergs Arch Pharmacol 2000, 362:406-412.
7. Beralu D.J., McGaugh J.L. Ehancement of extinction memory consolidation: the role of noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol Learn Mem 2006, 86:123-132.
8. Borsini F., Meli A. Is the forced swimming test a suitable model for revealing antidepressant activity?. Psychopharmacology (Berl) 1988, 94(2):147-160.
9. Borsini F., Podhorna J., Marazziti D. Do animal models of anxiety predict anxiolytic-like effects of antidepressants?. Psychopharmacology (Berl) 2002, 163:121-141.
10. Brocco M., Dekeyne A., Veiga S., Girardon S., Millan M.J. Induction of hyperlocomotion in mice exposed to a novel environment by inhibition of serotonin reuptake. A pharmacological characterization of diverse classes of antidepressant agents. Pharmacol Biochem Behav 2002, 71:667-680.
11. Brunello N., Davidson J.R., Deahl M., Kessler R.C., Mendlewicz J., Racagni G., et al. Posttraumatic stress disorder: diagnosis and epidemiology, comorbidity and social consequences, biology and treatment. Neuropsychobiology 2001, 43(3):150-162.
12. Carr G.V., Schechter L.E., Lucki I. Antidepressant and anxiolytic effects of selective 5-HT6 receptor agonists in rats. Psychopharmacology (Berl) 2011, 213:499-507.
13. Cassol-Jr O.J., Comim C.M., Petronilho F., Constantino L.S., Streck E.L., Quevedo J., et al. Low dose dexamethasone reverses depressive-like parameters and memory impairment in rats submitted to sepsis. Neurosci Lett 2010, 473:126-130.
14. Castaneda A.E., Tuulio-Henriksson A., Marttunen M., Suvisaari J., Lönnqvist J. A review on cognitive impairments in depressive and anxiety disorders with a focus on young adults. J Affect Disord 2008, 106(1-2):1-27.
15. Castrén E., Rantamäki T. The role of BDNF and its receptors in depression and antidepressant drug action: reactivation of developmental plasticity. Dev Neurobiol 2010, 70:289-297.
16. Cheng Y.F., Wang C., Lin H.B., Li Y.F., Huang Y., Xu J.P., et al. Inhibition of phosphodiesterase-4 reverses memory deficits produced by Aβ25-35 or Aβ1-40 peptide in rats. Psychopharmacology (Berl) 2010, 212(2):181-191.
17. Consoni F.T., Vital M.A., Andreatini R. Dual monoamine modulation for the antidepressant-like effect of lamotrigine in the modified forced swimming test. Eur Neuropsychopharmacol 2006, 16(6):451-458.
18. Cryan J.F., Lucki I. Antidepressant-like behavioral effects mediated by 5-Hydroxytryptamine(2C) receptors. J Pharmacol Exp Ther 2000, 295:1120-1126.
19. Cryan J.F., Valentino R.J., Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 2005, 29:547-569.
20. Curtis V. Women are not the same as men: specific clinical issues for female patients with bipolar disorder. Bipolar Disord 2005, 7:16-24.
21. Dagtekin O., Marcus H., Müller C., Böttinger B.W., Spöhr F. Liquid therapy for serotonin syndrome after intoxication with venlafaxine, lamotrigine and diazepam. Minerva Anestesiol 2011, 77(1):93-95.
22. de Boer T.H., Nefkens F., van Helvoirt A., van Delft A.M. Differences in modulation of noradrenergic and serotonergic transmission by the alpha-2 adrenoceptor antagonists, mirtazapine, mianserin and idazoxan. J Pharmacol Exp Ther 1996, 277:852-860.
23. Djordjevic A., Djordjevic J., Elaković I., Adzic M., Matić G., Radojcic M.B. Fluoxetine affects hippocampal plasticity, apoptosis and depressive-like behavior of chronically isolated rats. Prog Neuropsychopharmacol Biol Psychiatry 2012, 36:92-100.
24. Dranovsky A., Hen R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 2006, 59:1136-1143.
25. Drapier D., Bentué-Ferrer D., Laviolle B., Millet B., Allain H., Bourin M., et al. Effects of acute fluoxetine, paroxetine and desipramine on rats tested on the elevated plus-maze. Behav Brain Res 2007, 176:202-209.
26. Dulawa S.C., Holick K.A., Gundersen B., Hen H. Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 2004, 29:1321-1330.
27. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006, 59:1116-1127.
28. Dunlop B.W., Davis P.G. Combination treatment with benzodiazepines and SSRIs for comorbid anxiety and depression: a review. Prim Care Companion J Clin Psychiatry 2008, 10:222-228.
29. File S.E., Ouagazzal A.M., Gonzalez L.E., Overstreet D.H. Chronic fluoxetine in tests of anxiety in rat lines selectively bred for differential 5-HT1A receptor function. Pharmacol Biochem Behav 1999, 62:695-701.
30. Friedman L. A renaissance for Freud's papers on technique. Psychoanal Q 2008, 77:1031-1044.
31. Gabriele A., Packard M.G. Evidence of a role for multiple memory systems in behavioral extinction. Neurobiol Learn Mem 2006, 85:289-299.
32. Gambi F., De Berardis D., Campanella D., Carano A., Sepede G., Salini G., et al. Mirtazapine treatment of generalized anxiety disorder: a fixed dose, open label study. J Psychopharmacol 2005, 19:483-487.
33. Griebel G., Blanchard D.C., Agnes R.S., Blanchard R.J. Differential modulation of antipredator defensive behavior in Swiss-Webster mice following acute or chronic administration of imipramine and fluoxetine. Psychopharmacology (Berl) 1995, 120:57-66.
34. Haddjeri N., Blier P., Montigny C. Effect of the alpha-2 adrenoceptor antagonist mirtazapine on the 5-hydroxytryptamine system in the rat brain. J Pharmacol Exp Ther 1996, 277:861-871.
35. Hansson A.C., Rimondini R., Heilig M., Mathé A.A., Sommer W.H. Dissociation of antidepressant-like activity of escitalopram and nortriptyline on behaviour and hippocampal BDNF expression in female rats. J Psychopharmacol 2011, 25:1378-1387.
36. Harmer C.J., Mackay C.E., Reid C.B., Cowen P.J., Goodwin G.M. Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biol Psychiatry 2006, 59:816-820.
37. Holmes A., Rodgers R.J. Prior exposure to the elevated plus-maze sensitizes mice to the acute behavioral effects of fluoxetine and phenelzine. Eur J Pharmacol 2003, 459:221-230.
38. Homberg J.R., Olivier J.D., Blom T., Arentsen T., van Brunschot C., Schipper P., et al. Fluoxetine exerts age-dependent effects on behavior and amygdala neuroplasticity in the rat. PLoS One 2011, 31:e16646.
39. Iñiguez S.D., Warren B.L., Bolaños-Guzmán C.A. Short- and long-term functional consequences of fluoxetine exposure during adolescence in male rats. Biol Psychiatry 2010, 67:1057-1066.
40. Kendler K.S., Thornton L.M., Prescott C.A. Gender differences in the rates of exposure to stressful life events and sensitivity to their depressogenic effects. Am J Psychiatry 2001, 158:587-593.
41. Kurt M., Arik A.C., Celik S. The effects of sertraline and fluoxetine on anxiety in the elevated plus-maze test in mice. J Basic Physiol Pharmacol 2000, 11:173-180.
42. Lebrón K., Milad M.R., Quirk G.J. Delayed recall of fear extinction in rats with lesions of ventral medial prefrontal cortex. Learn Mem 2004, 11:544-548.
43. MacQueen G.M., Campbell S., McEwen B.S., Macdonald K., Amano S., Joffe R.T., et al. Course of illness, hippocampal function, and hippocampal volume in major depression. PNAS 2003, 100(3):1387-1392.
44. Mahendran R., Yap H.L. Clinical practice guidelines for depression. Singapore Med J 2005, 46:610-615.
45. Mallei A., Giambelli R., Gass P., Racagni G., Mathé A.A., Vollmayr B., et al. Synaptoproteomics of learned helpless rats involve energy metabolism and cellular remodeling pathways in depressive-like behavior and antidepressant response. Neuropharmacology 2011, 60:1243-1253.
46. Marks I., Lovell K., Noshirvani H., Livanou M., Thrasher S. Treatment of posttraumatic stress disorder by exposure and/or cognitive restructuring. Arch Gen Psychiatry 1998, 55:317-325.
47. McCabe C., Mishor Z., Cowen P.J., Harmer C.J. Diminished neural processing of aversive and rewarding stimuli during selective serotonin reuptake inhibitor treatment. Biol Psychiatry 2010, 67:439-445.
48. McEwen B.S., Chattarji S. Molecular mechanisms of neuroplasticity and pharmacological implications: the example of tianeptine. Eur Neuropsychopharmacol 2004, 14:S497-S502.
49. McLean C.P., Anderson E.R. Brave men and timid women? A review of the gender differences in fear and anxiety. Clin Psychol Rev 2009, 29:496-505.
50. Mirza N.R., Nielsen E.Ø., Troelsen K.B. Serotonin transporter density and anxiolytic-like effects of antidepressants in mice. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:858-866.
51. Miyamoto D., Iijima M., Yamamoto H., Nomura H., Matsuki N. Behavioural effects of antidepressants are dependent and independent on the integrity of the dentate gyrus. Int J Neuropsychopharmacol 2010, 3:1-10.
52. Monti B., Berteotti C., Contestabile A. Subchronic rolipram delivery activates hippocampal CREB and arc, enhances retention and slows down extinction of conditioned fear. Neuropsychopharmacology 2006, 31:278-286.
53. Morgan M.A., LeDoux J.E. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci 1995, 109:681-688.
54. Mueller E.M., Hofmann S.G., Cherry J.A. The type IV phosphodiesterase inhibitor rolipram disturbs expression and extinction of conditioned fear in mice. Neuropharmacology 2010, 59:1-8.
55. Munguba H., Cabral A., Leão A.H., Barbosa F.F., Izídio G.S., Ribeiro A.M., et al. Pre-training anandamide infusion within the basolateral amygdala impairs plus-maze discriminative avoidance task in rats. Neurobiol Learn Mem 2011, 95:527-533.
56. Nandam L.S., Jhaveri D., Bartlett P. 5-HT7, neurogenesis and antidepressants: a promising therapeutic axis for treating depression. Clin Exp Pharmacol Physiol 2007, 34:546-551.
57. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
58. Nishino T., Takeuchi T., Takechi K., Kamei C. Evaluation of anxiolytic-like effects of some short-acting benzodiazepine hypnotics in mice. J Pharmacol Sci 2008, 107:349-354.
59. Nowakowska E., Chodera A., Kus K. Behavioral and memory improving effects of mirtazapine in rats. Pol J Pharmacol 1999, 51:463-469.
60. Paizanis E., Hamon M., Lanfumey L. Hippocampal neurogenesis, depressive disorders, and antidepressant therapy. Neural Plast 2007, 2007:1-7.
61. Parker G., Brotchie H. Gender differences in depression. Int Rev Psychiatry 2010, 22:429-436.
62. Patti C.L., Kameda S.R., Carvalho R.C., Takatsu-Coleman A.L., Lopez G.B., Niigaki S.T., et al. Effects of morphine on the plus-maze discriminative avoidance task: role of state-dependent learning. Psychopharmacology (Berl) 2006, 184:1-12.
63. Perrot-Sinal T.S., Gregus A., Boudreau D., Kalynchuk L.E. Sex and repeated restraint stress interact to affect cat odor-induced defensive behavior in adult rats. Brain Res 2004, 1027:161-171.
64. Petersén A., Wörtwein G., Gruber S.H., El-Khoury A., Mathé A.A. Nortriptyline mediates behavioral effects without affecting hippocampal cytogenesis in a genetic rat depression model. Neurosci Lett 2009, 451:148-151.
65. Pittenger C., Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacol Rev 2008, 33:88-109.
66. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatment. Nature 1977, 266:730-732.
67. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978, 47:379-391.
68. Quirk G.J., Garcia R., González-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 2006, 60:337-343.
69. Rauch S.L., Shin L.M., Phelps E.A. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research - past, present, and future. Biol Psychiatry 2006, 60:376-382.
70. Rauggi R., Cassanelli A., Raone A., Tagliamonte A., Gambarana C. Study of mirtazapine antidepressant effects in rats. Int J Neuropsychopharmacol 2005, 8:369-379.
71. Rawlings N.B., Norbury R., Cowen P.J., Harmer C.J. A single dose of mirtazapine modulates neural responses to emotional faces in healthy people. Psychopharmacology (Berl) 2010, 212:625-634.
72. Reneric J.P., Bouvard M., Stinus L. In the rat forced swimming test, chronic but not subacute administration of dual 5-HT/NA antidepressant treatments may produce greater effects than selective drugs. Behav Brain Res 2002, 136:521-532.
73. Ribeiro A.M., Barbosa F.F., Godinho M.R., Fernandes V.S., Munguba H., Alves L.M., et al. Sex differences in aversive memory in rats: possible role of extinction and reactive emotional factors. Brain Cogn 2010, 74:145-151.
74. Ribeiro A.M., Barbosa F.F., Munguba H., Costa M.S., Cavalcante J.S., Silva R.H. Basolateral amygdala inactivation impairs learned (but not innate) fear response in rats. Neurobiol Learn Mem 2011, 95:433-440.
75. Robert G., Drapier D., Bentué-Ferrer D., Renault A., Reymann J.M. Acute and chronic anxiogenic-like response to fluoxetine in rats in the elevated plus-maze: modulation by stressful handling. Behav Brain Res 2011, 220:344-348.
76. Rodgers R.J., Dalvi A. Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 1997, 21:801-810.
77. Rodgers R.J., Shepherd J.K. Influence of prior maze experience on behaviour and response to diazepam in the elevated plus-maze and light/dark tests of anxiety in mice. Psychopharmacology (Berl) 1993, 113:237-242.
78. Rodgers R.J., Cao B.J., Dalvi A., Holmes A. Animal models of anxiety: an ethological perspective. Braz J Med Biol Res 1997, 30:289-304.
79. Rogóz Z. Effects of co-treatment with mirtazapine and low doses of risperidone on immobility time in the forced swimming test in mice. Pharmacol Rep 2010, 62:1191-1196.
80. Sahay A., Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci 2007, 10:1110-1115.
81. Santarelli L., Saxe M., Gross C., Battaglia F., Dulawa S., Weisstaub N., et al. Requirement of hippocampal neurogenesis for the behavioral effectc of antidepressants. Science 2003, 301:805-809.
82. Schüle C., Baghai T., Goy J., Bidlingmaier M., Strasburger C., Laakmann G. The influence of mirtazapine on anterior pituitary hormone secretion in healthy male subjects. Psychopharmacology (Berl) 2002, 163:95-101.
83. Schüle C., Baghai T., Zwanzger P., Ella R., Eser D., Padberg F., et al. Attenuation of hypothalamic-pituitary-adrenocortical hyperactivity in depressed patients by mirtazapine. Psychopharmacology (Berl) 2003, 166:271-275.
84. Schüle C., Baghai T.C., Eser D., Zwanzger P., Jordan M., Buechs R., et al. Time course of hypothalamic-pituitary-adrenocortical axis activity during treatment with reboxetine and mirtazapine in depressed patients. Psychopharmacology (Berl) 2006, 186:601-611.
85. Schulz D., Buddenberg T., Huston J.P. Extinction-induced "despair" in the water maze, exploratory behavior and fear: effects of chronic antidepressant treatment. Neurobiol Learn Mem 2007, 87:624-634.
86. Scott K.M. Sex differences in the disability associated with mental disorders. Curr Opin Psychiatry 2011, 24:331-335.
87. Silva R.H., Frussa-Filho R. The plus-maze discriminative acoidance task: a new model to study memory-anxiety interactions. Effects of chlordiazepoxide and caffeine. J Neurosci Methods 2000, 102:117-125.
88. Silva R.H., Bellot R.G., Vital M.A., Frussa-Filho R. Effects of long-term ganglioside GM1 administration on a new discriminative avoidance test in normal adult mice. Psychopharmacology (Berl) 1997, 129:322-328.
89. Silva M.T., Alves C.R., Santarem E.M. Anxiogenic-like effect of acute and chronic fluoxetine on rats tested on the elevated plus-maze. Braz J Med Biol Res 1999, 32:333-339.
90. Silva R.H., Abílio V.C., Torres-Leite D., Bergamo M., Chinen C.C., Claro F.T., et al. Concomitant development of oral dyskinesia and memory deficits in reserpine-treated male and female mice. Behav Brain Res 2002, 132:171-177.
91. Silva R.H., Kameda S.R., Carvalho R.C., Rigo G.S., Costa K.L., Taricano I.D., et al. Effects of amphetamine on the plus-maze discriminative avoidance task in mice. Psychopharmacology (Berl) 2002, 160:9-18.
92. Silva R.H., Chehin A.B., Kameda S.R., Takatsu-Coleman A.L., Abilio V.C., Tufik S., et al. Effects of pre- or post-training paradoxical sleep deprivation on two animal models of learning and memory in mice. Neurobiol Learn Mem 2004, 82:90-98.
93. Soeter M., Kindt M. Stimualtion in the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology 2011, [Epub ahead of print]. 10.1038/npp.2011.307.
94. Szymańska M., Budziszewska B., Jaworska-Feil L., Basta-Kaim A., Kubera M., Leśkiewicz M., et al. The effect of antidepressant drugs on the HPA axis activity, glucocorticoid receptor level and FKBP51 concentration in prenatally stressed rats. Psyconeuroendocrinology 2009, 34:822-832.
95. Taylor S.E., Klein L.C., Lewis B.P., Gruenewald T.L., Gurung R.A., Updegraff J.A. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 2000, 107:411-429.
96. Varea E., Castillo-Gómez E., Gómez-Climent M.A., Blasco-Ibáñez J.M., Crespo C., Martínez-Guijarro F.J., et al. Chronic antidepressant treatment induces contrasting patterns of synaptophysin and PSA-NCAM expression in different regions of the adult rat telencephalon. Eur Neuropsychopharmacol 2007, 17:546-557.
97. Wald C., Wu C. Biomedical research. Of mice and women: the bias in animal models. Science 2010, 327:1571-1572.
98. Wang Y., Cui X.L., Liu Y.F., Gao F., Wei D., Li X.W., et al. LPS inhibits the effects of fluoxetine on depression-like behavior and hippocampal neurogenesis in rats. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:1831-1835.
99. Yamamoto S., Morinobu S., Fuchikami M., Kurata A., Kozuru T., Yamawaki S. Effects of single prolonged stress and d-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsychopharmacology 2008, 33:2108-2116.
100. Yamamoto S., Morinobu S., Takei S., Fuchikami M., Matsuki A., Yamawaki S., et al. Single prolonged stress: toward an animal model of posttraumatic stress disorder. Depress Anxiety 2009, 26:1110-1117.
101. Zucker I., Beery A.K. Males still dominate animal studies. Nature 2010, 465:690.