Effects of chronic treatment with corticosterone and imipramine on fos immunoreactivity and adult hippocampal neurogenesis

Behavioural Brain Research

Volumn 238, Issue 1, 2013, Pages 170-177

  Diniz, L ^a   dos Santos, T B ^a   Britto, L R G ^b   Cespedes I C ^a   Garcia, M C ^a   Spadari Bratfisch, R C ^a   Medalha, C C ^a   de Castro, G M ^a   Montesano, F T ^a   Viana, M B ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Anxiety; Corticosterone; Fos immunoreactivity; Hippocampal neurogenesis; Imipramine; Panic

Indexed keywords

CORTICOSTERONE; DOUBLECORTIN; IMIPRAMINE; PROTEIN C FOS; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; CELL COUNT; CONTROLLED STUDY; HIPPOCAMPUS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; MALE; MEDIAL AMYGDALA; NERVE CELL DIFFERENTIATION; NEUROBIOLOGY; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THALAMUS VENTRAL NUCLEUS;

AMYGDALA; ANIMALS; CORTICOSTERONE; HIPPOCAMPUS; HYPOTHALAMUS; IMIPRAMINE; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR;

EID: 84868697853     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.10.024     Document Type: Article

References (82)

1. American Psychiatric Association, task force on DSM-IV Diagnostic and statistical manual of mental disorders DSM-IV-TR 2000, APA Press, Washington, DC. 4 ed., text revision.
2. Baldwin D.S., Waldman S., Allgulander C. Evidence-based pharmacological treatment of generalized anxiety disorder. International Journal of Neuropsychopharmacology 2011, 14(5):697-710.
3. Batelaan N.M., Van Balkom A.J., Stein D.J. Evidence-based pharmacotherapy of panic disorder: an update. International Journal of Neuropsychopharmacology 2011, 1-13.
4. Klein D.F. False suffocation alarms, spontaneous panics, and related conditions: an integrative hypothesis. Archives of General Psychiatry 1993, 50(4):306-317. [Review].
5. Coplan J.D., Pine D., Papp L., Martinez J., Cooper T., Rosenblum L.A., et al. Uncoupling of the noradrenergic-hypothalamic-pituitary-adrenal axis in panic disorder patients. Neuropsychopharmacology 1995, 13(1):65-73.
6. Graeff F.G., Garcia-Leal C., Del-Ben C.M., Guimaraes F.S. Does the panic attack activate the hypothalamic-pituitary-adrenal axis?. Anais da Academia Brasileira de Ciências 2005, 77(3):477-491.
7. Graeff F.G. Ansiedade, pânico e eixo hipotálamo-pituitário-adrenal. Revista Brasileira de Psiquiatria 2007, 29(1):S3-S6.
8. Roy-Byrne P.P., Uhde T.W., Post R.M., Gallucci W., Chrousos G.P., Gold P.W. The corticotropin-releasing hormone stimulation test in patients with panic disorder. American Journal of Psychiatry 1986, 143(7):896-899.
9. 2 inhalation study. American Journal of Psychiatry 2006, 163(4):738-740.
10. 2 challenge induced HPA axis activation in panic. International Journal of Neuropsychopharmacology 2007, 10(6):797-804.
11. Graeff F.G., Zangrossi H. Animal models of anxiety. Biological psychiatry 2002, 879-893. John Wiley & Sons, London. D. D'Haenen, J.A. Den Boer, P. Willner (Eds.).
12. Handley S.L., McBlane J.W. 5HT drugs in animal models of anxiety. Psychopharmacology 1993, 112(1):13-20.
13. Griebel G. 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30 years of research. Pharmacology & Therapeutics 1995, 65(3):319-395.
14. Graeff F.G., Viana M.B., Tomaz C. The elevated T maze, a new experimental model of anxiety and memory: effect of diazepam. Brazilian Journal of Medical and Biological Research 1993, 26(1):67-70.
15. Graeff F.G., Netto C.F., Zangrossi H. The elevated T-maze as an experimental model of anxiety. Neuroscience and Biobehavioral Reviews 1998, 23(2):237-246.
16. Viana M.B., Tomaz C., Graeff F.G. The elevated T-maze: a new animal model of anxiety and memory. Pharmacology Biochemistry and Behavior 1994, 50(3):549-554.
17. Teixeira R.C., Zangrossi H., Graeff F.G. Behavioral effects of acute and chronic imipramine in the elevated T maze model of anxiety. Pharmacology Biochemistry and Behavior 2000, 65(4):571-576.
18. Poltronieri S.C., Zangrossi H., Viana M.B. Antipanic-like effect of serotonin reuptake inhibitors in the elevated T-maze. Behavioural Brain Research 2003, 147(1-2):185-192.
19. Diniz L., Dos Reis B.B., de Castro G.M., Medalha C.C., Viana M.B. Effects of chronic corticosterone and imipramine administration on panic and anxiety-related responses. Brazilian Journal of Medical and Biological Research 2011, 44(10):1048-1053.
20. Marchesi C. Pharmacological management of panic disorder. Neuropsychiatric Disease and Treatment 2008, 4(1):93-106.
21. Hale W., Bouwknecht J.A., Spiga F., Shekhar A., Lowry C.A. Exposure to high- and low-light conditions in an open-field test of anxiety increases c-Fos expression in specific subdivisions of the rat basolateral amygdaloid complex. Brain Research Bulletin 2006, 71:174-182.
22. Sapolsky R.M. Depression antidepressants, and the shrinking hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(22):12320-12322.
23. Hellsten J., Wennström M., Mohapel P., Ekdahl C.T., Bengzon J., Tingström A. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. European Journal of Neuroscience 2002, 16(2):283-290.
24. Murray F., Smith D.W., Hulson P.H. Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. European Journal of Pharmacology 2008, 583(1):115-127.
25. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. Journal of Neuroscience 2000, 20(24):9104-9110.
26. Hsu S.M., Raine L. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody procedures. Journal of Histochemistry and Cytochemistry 1981, 29:577-580.
27. Silveira M.C., Zangrossi H., de Barros Viana M., Silveira R., Graeff F.G. Differential expression of Fos protein in the rat brain induced by performance of avoidance or escape in the elevated T-maze. Behavioural Brain Research 2001, 126(1-2):13-21.
28. de Andrade J.S., Abrão R.O., Céspedes I.C., Garcia M.C., Nascimento J.O.G., Spadari-Bratfisch R.C., et al. Acute restrain differently alters defensive responses and fos immunoreactivity in the rat brain. Behavioural Brain Research 2012, 232(1):20-29.
29. Paxinos G., Watson C. The rat brain in stereotaxic coordinates: compact sixth edition 2008, Academic Press, Sidney.
30. Brummelte S., Galea L.A. Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 2010, 168(3):680-690.
31. McGimsey W.C., Cidlowski J.A., Stumpf W.E., Sar M. Immunocytochemical localization of the glucocorticoid receptor in rat brain, pituitary, liver, and thymus with two new polyclonal antipeptide antibodies. Endocrinology 1991, 129(6):3064-3072.
32. Bamberger C.M., Schulte H.M., Chrousos G.P. Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocrine Reviews 1996, 17(3):245-261.
33. Rhen T., Cidlowski J.A. Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. New England Journal of Medicine 2005, 353(16):1711-1723.
34. Lu N.Z., Cidlowski J.A. Glucocorticoid receptor isoforms generate transcription specificity. Trends in Cell Biology 2006, 16(6):301-307.
35. Sheehan T.P., Chambers R.A., Russell D.S. Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Research. Brain Research Reviews 2004, 46:71-117.
36. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2005, 29:1201-1213.
37. Singewald G.M., Rjabokon A., Singewald N., Ebner K. The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacology 2011, 36(4):793-804.
38. Gray J.A. The neuropsychology of anxiety 1987, Oxford University Press, Oxford.
39. Gray J.A., McNaughton N. The neuropsychology of anxiety 2001, Oxford University Press, Oxford.
40. McNaughton N., Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neuroscience and Biobehavioral Reviews 2004, 28:285-305.
41. Cullinan W.E., Herman J.P., Battaglia D.F., Akil H., Watson S.J. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 1995, 64(2):477-505.
42. Dayas C.V., Buller K.M., Crane J.W., Xu Y., Day T.A. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. European Journal of Neuroscience 2001, 14(7):1143-1152.
43. Windle R.J., Kershaw Y.M., Shanks N., Wood S.A., Lightman S.L., Ingram C.D. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. Journal of Neuroscience 2004, 24(12):2974-2982.
44. Nikulina E.M., Covington H.E., Ganschow L., Hammer R.P., Miczek K.A. Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: fos in the ventral tegmental area and amygdala. Neuroscience 2004, 123(4):857-865.
45. Rosen J.B., Fanselow M.S., Young S.L., Sitcoske M., Maren S. Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Research 1998, 796(1-2):132-142.
46. Adamec R.E., Burton P., Shallow T., Budgell J. Unilateral block of NMDA receptors in the amygdala prevents predator stress-induced lasting increases in anxiety-like behavior and unconditioned startle-effective hemisphere depends on the behavior. Physiology and Behavior 1999, 65(4-5):739-751.
47. Adamec R., Toth M., Haller J., Halasz J., Blundell J. A comparison of activation patterns of cells in selected prefrontal cortical and amygdala areas of rats which are more or less anxious in response to predator exposure or submersion stress. Physiology and Behavior 2012, 105(3):628-638.
48. Bhatnagar S., Dallman M. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 1998, 84(4):1025-1039.
49. Li H.Y., Sawchenko P.E. Hypothalamic effector neurons and extended circuitries activated in neurogenic stress: a comparison of footshock effects exerted acutely, chronically, and in animals with controlled glucocorticoid levels. Journal of Comparative Neurology 1998, 393(2):244-266.
50. Dunn J.D., Whitener J. Plasma corticosterone responses to electrical stimulation of the amygdaloid complex: cytoarchitectural specificity. Neuroendocrinology 1986, 42(3):211-217.
51. Feldman S., Conforti N., Saphier D. The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience 1990, 37(3):775-779.
52. Dayas C.V., Buller K.M., Day T.A. Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. European Journal of Neuroscience 1999, 11(7):2312-2322.
53. Feldman S., Conforti N., Itzik A., Weidenfeld J. Differential effect of amygdaloid lesions on CRF-41, ACTH and corticosterone responses following neural stimuli. Brain Research 1994, 658(1-2):21-26.
54. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nature Reviews Neuroscience 2009, 10(6):397-409.
55. Sawchenko P.E., Swanson L.W. The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. Journal of Comparative Neurology 1983, 218(2):121-144.
56. Herdade K.C., Strauss C.V., Zangrossi Júnior H., Viana M.B. Effects of medial amygdala inactivation on a panic-related behavior. Behavioural Brain Research 2006, 172(2):316-323.
57. de Medeiros M.A., Carlos Reis L., Eugênio Mello L. Stress-induced c-Fos expression is differentially modulated by dexamethasone, diazepam and imipramine. Neuropsychopharmacology 2005, 30(7).
58. Nashold B.S, Wilson W.P., Slaughter D.G. The midbrain and pain. Advances in neurology 1974, 191-196. Raven press, New York. J.J. Bonica (Ed.).
59. Graeff F.G. Neurotransmitters in the periaqueductal gray and animal models of panic anxiety. New concepts in anxiety 1991, 288-312. MacMillan, London. M. Briley, S.E. File (Eds.).
60. Fanselow M.S. Neural organization of the behaviour system responsible for fear. Psychonomic Bulletin & Review 1994, 1:429-438.
61. Jenck F., Moreau J.L., Martin J.R. Dorsal periaqueductal gray-induced aversion as a simulation of panic anxiety: elements of face and predictive validity. Psychiatry Research 1995, 57(2):181-191.
62. Zanoveli J.M., Nogueira R.L., Zangrossi H. Serotonin in the dorsal periaqueductal gray modulates inhibitory avoidance and one-way escape behaviors in the elevated T-maze. European Journal of Pharmacology 2003, 473(2-3):153-161.
63. Yamashita P.S.M., de Bortoli V.C., Zangrossi H. 5-HT2C receptor regulation of defensive responses in the rat dorsal periaqueductal gray. Neuropharmacology 2011, 60(2-3):216-222.
64. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiological Reviews 1972, 72:165-229.
65. Fuxe K., Cintra A., Agnati L.F., Härfstrand A., Wikstrom A.C., Okret S., et al. Studies on the cellular localization and distribution of glucocorticoid receptor and estrogen receptor immunoreactivity in the central nervous system of the rat and their relationship to the monoaminergic and peptidergic neurons of the brain. Journal of Steroid Biochemistry 1987, 27:159-170.
66. Morimoto M., Morita N., Ozawa H., Yokoyama K., Kawata M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neuroscience Research 1996, 26:235-269.
67. Canteras N. The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacology Biochemistry and Behavior 2002, 71:481-491.
68. Shekhar A., Keim S.R. The circumventricular organs form a potential neural pathway for lactate sensitivity: implications for panic disorder. Journal of Neuroscience 1997, 17(24):9726-9735.
69. Shekhar A., Keim S.R. LY354740, a potent group II metabotropic glutamate receptor agonist prevents lactate-induced panic-like response in panic-prone rats. Neuropharmacology 2000, 39(7):1139-1146.
70. Dielenberg R.A., Hunt G.E., McGregor I.S. When a rat smells a cat: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 2001, 104(4):1085-1097.
71. Santos J.M., Macedo C.E., Brandão M.L. Gabaergic mechanisms of hypothalamic nuclei in the expression of conditioned fear. Neurobiology of Learning and Memory 2008, 90(3):560-568.
72. Hess W.R., Brugger M. Das subkortikale Zentrum der affektiven abwehrreacktion. Helvetica Physiologica et Pharmacologica Acta 1943, 1:33-52.
73. Fernandez de Molina A., Hunsperger R.W. Organization of the subcortical system governing defense and flight reactions in the cat. Journal of Physiology 1962, 160:200-213.
74. Panksepp J. Aggression elicited by electrical stimulation of the hypothalamus in albino rats. Physiology & Behavior 1971, 6(4):321-329.
75. Bailey T.W., DiMicco J.A. Chemical stimulation of the dorsomedial hypothalamus elevates plasma ACTH in conscious rats. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2001, 280(1):R8-R15.
76. Schmitt P., Di Scala G., Brandão M.L., Karli P. Behavioral effects of microinjections of SR 95103, a new GABA-A antagonist, into the medial hypothalamus or the mesencephalic central gray. European Journal of Pharmacology 1985, 117(2):149-158.
77. Duman R.S., Nakagawa S., Malberg J. Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 2001, 25:836-844.
78. Surget A., Saxe M., Leman S., Ibarguen-Vargas Y., Chalon S., Griebel G., et al. Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biological Psychiatry 2008, 64:293-301.
79. David D.J., Samuels B.A., Rainer Q., Wang J.W., Marsteller D., Mendez I., et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62(4):479-493.
80. Petrik D., Lagace D.C., Eisch A.J. The neurogenesis hypothesis of affective and anxiety disorders: are we mistaking the scaffolding for the building. Neuropharmacology 2012, 62:21-34.
81. Revest J.M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.V., et al. Adult hippocampal neurogenesis is involved in anxiety- related behaviors. Molecular Psychiatry 2009, 14:959-967.
82. Onksen J.L., Brown E.J., Blendy J.A. Selective deletion of a cell cycle check- point kinase (ATR) reduces neurogenesis and alters responses in rodent models of behavioral affect. Neuropsychopharmacology 2011, 36:960-969.