Acute restraint differently alters defensive responses and fos immunoreactivity in the rat brain

Behavioural Brain Research

Volumn 232, Issue 1, 2012, Pages 20-29

  De Andrade, J S ^a   Abrao R O ^a   Cespedes I C ^a   Garcia, M C ^a   Nascimento, J O G ^a   Spadari Bratfisch, R C ^a   Melo, L L ^a   Da Silva, R C B ^a   Viana, M B ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Anxiety; Corticosterone; Fos immunoreactivity; Panic; Restraint; Stress

Indexed keywords

CORTICOSTERONE; PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; AVOIDANCE BEHAVIOR; BASOLATERAL AMYGDALA; BASOMEDIAL AMYGDALA; BRAIN; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; DORSAL RAPHE NUCLEUS; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; ESCAPE BEHAVIOR; FRONTAL CORTEX; IMMOBILIZATION STRESS; INTERMEDIATE LATERAL SEPTUM; LATERAL AMYGDALA; LOCUS CERULEUS; MALE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; ZONA INCERTA;

ANIMALS; ANXIETY; AVOIDANCE LEARNING; BRAIN CHEMISTRY; CORTICOSTERONE; DATA INTERPRETATION, STATISTICAL; ESCAPE REACTION; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; MALE; ONCOGENE PROTEINS V-FOS; PITUITARY-ADRENAL SYSTEM; RATS; RATS, WISTAR; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 84859770441     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.03.034     Document Type: Article

References (97)

1. Cook C.J. Stress induces CRF release in the paraventricular nucleus, and both CRF and GABA release in the amygdala. Physiol Behav 2004, 82(4):751-762.
2. Garcia-Bueno B., Caso J.R., Leza J.C. Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 2008, 32(6):1136-1151.
3. Joels M., Baram T.Z. The neuro-symphony of stress. Nature Rev Neurosci 2009, 10:459-466.
4. Smagin G.N., Harris R.B., Ryan D.H. Corticotropin-releasing factor receptor antagonist infused into the locus ceruleus attenuates immobilization stress-induced defensive withdrawal in rats. Neurosci Lett 1996, 220(3):167-170.
5. MacNeil G., Sela Y., McIntosh J., Zacharko R.M. Anxiogenic behavior in the light-dark paradigm following intraventricular administration of cholecystokinin-8S: restrain stress, or uncontrollable footshock in the CD-1 mouse. Pharmacol Biochem Behav 1997, 58(3):737-746.
6. Harris R.B., Zhou J., Shi M., Redmann S., Mynatt R.L., Ryan D.H. Over expression of agouti protein and stress responsiveness in mice. Physiol Behav 2001, 73(4):599-608.
7. Morilak D.A., Cecchi M., Khoshbouei H. Interactions of norepinephrine and galanin in the central amygdala and lateral bed nucleus of the stria terminalis modulate the behavioral response to acute stress. Life Sci 2003, 73(6):715-726.
8. Archer J. Letter: The Maudsley reactive and nonreactive strains of rats: the need for an objective evaluation of differences. Behav Genet 1975, 5(4):411-413.
9. Pellow S., Chopin P., File S.E., Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14(3):149-167.
10. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 1985, 9(1):37-44.
11. Broekkamp C.L., Rijk H.W., Joly-Gelouin D., Lloyd K.L. Major tranquillizers can be distinguished from minor tranquillizers on the basis of effects on marble burying and swim-induced grooming in mice. Eur J Pharmacol 1986, 126(3):223-229.
12. Chotiwat C., Harris R.B.S. Increased anxiety-like behavior during the post-stress period in mice exposed to repeated restraint stress. Horm Behav 2006, 50:489-495.
13. de Paula Soares V., Vicente M.A., Biojone C., Zangrossi H., Guimarães F.S., Joca S.R. Distinct behavioral consequences of stress models of depression in the elevated T-maze. Behav Brain Res 2011, 225(2):590-595.
14. Viana M.B., Tomaz C.A.B., Graeff F.G. The elevated T-maze: a new animal model of anxiety and memory. Pharmacol Biochem Behav 1994, 49:549-554.
15. Zangrossi H., Graeff F.G. Behavioral validation of the elevated T-maze, a new animal model of anxiety. Brain Res Bull 1997, 44(1):1-5.
16. Teixeira R.C., Zangrossi H., Graeff F.G. Behavioral effects of acute and chronic imipramine in the elevated T-maze model of anxiety. Pharmacol Biochem Behav 2000, 65:571-576.
17. Poltronieri S.C., Zangrossi H., Viana M.B. Antipanic-like effect of serotonin reuptake inhibitors in the elevated T-maze. Behav Brain Res 2003, 147:185-192.
18. 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.).
19. Shin L.M., Liberzon I. The neurocircuitry of fear, stress and anxiety disorders. Neuropsychopharmacology 2010, 35(1):169-191.
20. 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. Behav Brain Res 2001, 126(1-2):13-21.
21. Sena L.M., Bueno C., Pobbe R.L., Andrade T.G., Zangrossi H., Viana M.B. The dorsal raphe nucleus exerts opposed control on generalized anxiety and panic-related defensive responses in rats. Behav Brain Res 2003, 142:125-133.
22. Southwick S.M., Bremner D., Krystal J.H., Charney D.S. Psychobiologic research in post-traumatic stress disorder. Psychiatr Clin North Am 1994, 17(2):251-264.
23. Glaser R., Kiecolt-Glaser J.K. Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 2005, 5(3):243-251.
24. Hsu S.M., Raine L. Protein A, avidin, and biotin in immunohistochemistry. J Histochem Cytochem 1981, 29:1349-1353.
25. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, Sidney.
26. Gray J.A. The neuropsychology of anxiety 1987, Oxford University Press, Oxford.
27. Gray J.A., McNaughton N. The neuropsychology of anxiety 2001, Oxford University Press, Oxford.
28. McNaughton N., Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev 2004, 28:285-305.
29. Blanco E., Castilla-Ortega E., Miranda R., Begega A., Aguirre J.A., Arias J.L., et al. Effects of medial prefrontal cortex lesions on anxiety-like behaviour in restrained and non-restrained rats. Behav Brain Res 2009, 201(2):338-342.
30. Viana M.B., Zangrossi H., Onusic G.M. 5-HT1A receptors of the lateral septum regulate inhibitory avoidance but not escape behavior in rats. Pharmacol Biochem Behav 2008, 89:360-366.
31. Tye K.M., Prakash R., Kim S.Y., Fenno L.E., Grosenick L., Zarabi H., et al. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 2011, 471(7338):358-362.
32. Ledoux J.E. Fear and the brain: where have we been, and where are we going. Biol Psychiatry 1998, 44:1229-1238.
33. Ledoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184.
34. Charney D.S., Drevets W.C. Neurobiological basis of anxiety disorders. Neuropsychopharmacology: the fifth generation of progress 2002, 901-930. Lippincott Williams & Wilkins, Philadelphia. K.L. Davis, D.S. Charney, J.T. Coyle, C. Nemeroff (Eds.).
35. Hasler G., Fromm S., Alvarez R.P., Luckenbaugh D.A., Drevets W.C., Grillon C. Cerebral blood flow in immediate and sustained anxiety. J Neurosci 2007, 27(23):6313-6319.
36. Sah P., Faber E.S.L., Lopez De Armentia M., Power J. The amygdaloid complex: anatomy and physiology. Physiol Rev 2003, 83(3):803-834.
37. Davis M., Myers K.M. The role of glutamate and gamma-aminobutyric acid in fear extinction: clinical implications for exposure therapy. Biol Psychiatry 2002, 52(10):998-1007.
38. Davis M. Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am Psychol 2006, 61(8):741-756.
39. Ongür D., Price J.L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 2000, 10(3):206-219.
40. Zangrossi H., Viana M.B., Graeff F.G. Anxiolytic effect of intra-amygdala injection of midazolam and 8-hydroxy-2-(di-n-propylamino)tetralin in the elevated T-maze. Eur J Pharmacol 1999, 369(3):267-270.
41. Bueno C.H., Zangrossi H., Viana M.B. The inactivation of the basolateral nucleus of the rat amygdala has an anxiolytic effect in the elevated T-maze and light/dark transition tests. Braz J Med Biol Res 2005, 38(11):1697-1701.
42. Deakin J.F., Graeff F.G. 5-HT and mechanisms of defense. J Psychopharmachol (Berl) 1991, 5(1991):305-315.
43. Graeff F.G., Guimarães F.S., De Andrade T.G., Deakin J.F. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 1996, 54(1):129-141.
44. Graeff F.G., Zangrossi H. The dual role of serotonin in defense and the mode of action of antidepressants on generalized anxiety and panic disorders. Cent Nerv Syst Agents Med Chem 2010, 10(3):207-217.
45. Etkin A., Prater K.E., Schatzberg A.F., Menon V., Greicius M.D. Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch Gen Psychiatry 2009, 66(12):1361-1372.
46. Canteras N. The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol Biochem Behav 2002, 71:481-491.
47. Silveira M.C.L., Graeff F.G. Defense reaction elicited by microinjection of kainic acid into the medial hypothalamus of the rat: antagonism by a GABAA receptor agonist. Behav Neural Biol 1992, 57(3):226-232.
48. Shekhar A., Keim S.R. The circumventricular organs form a potential neural pathway for lactate sensitivity: implications for panic disorder. J Neurosci 1997, 17(24):9726-9735.
49. 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.
50. Santos J.M., Macedo C.E., Brandão M.L. Gabaergic mechanisms of hypothalamic nuclei in the expression of conditioned fear. Neurobiol Lear Mem 2008, 560-568.
51. Hess W.R., Brugger M. Das subkortikale Zentrum der affektiven abwehrreacktion. Helv Physiol Pharmacol Acta 1943, 1:33-52.
52. Fernandez de Molina A., Hunsperger R.W. Organization of the subcortical system governing defense and flight reactions in the cat. J Physiol 1962, 160:200-213.
53. Panksepp J. Aggression elicited by electrical stimulation of the hypothalamus in albino rats. Physiol Behav 1971, 6(4):321-329.
54. Bailey T.W., DiMicco J.A. Chemical stimulation of the dorsomedial hypothalamus elevates plasma ACTH in conscious rats. Am J Physiol Regul Integr Comp Physiol 2001, 280(1):R8-R15.
55. 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. Eur J Pharmacol 1985, 117(2):149-158.
56. Bueno C.H., Zangrossi H., Viana M.B. GABA/benzodiazepine receptors in the ventromedial hypothalamic nucleus regulate both anxiety and panic-related defensive responses in the elevated T-maze. Brain Res Bull 2007, 74(1-3):134-141.
57. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72(1):165-229.
58. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J., Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 2005, 8(4):233-246.
59. Lowry C.A., Hale M.W., Evans A.K., Heerkens J., Staub D.R., Gasser P.J., et al. Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 2008, 1148:86-94.
60. Andrade R. Serotonergic regulation of neuronal excitability in the prefrontal cortex. Neuropharmacology 2011, 61(3):382-386.
61. 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.).
62. Jacquet Y.F., Squires R.F. Excitatory amino acids: role in morphine excitation in rat periaqueductal gray. Behav Brain Res 1988, 31(1):85-88.
63. Fanselow M.S. Neural organization of the behaviour system responsible for fear. Psychol Bull Rev 1994, 1:429-438.
64. 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.).
65. 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 Res 1995, 57:181-191.
66. Bueno C.H., Zangrossi H., Nogueira R.L., Soares V.P., Viana M.B. Panicolytic-like effect induced by the stimulation of GABAA and GABAB receptors in the dorsal periaqueductal grey of rats. Eur J Pharmacol 2005, 516(3):239-246.
67. Lim L.W., Blokland A., Visser-Vandewalle V., Vlamings R., Sesia T., Steinbusch H., et al. High-frequency stimulation of the dorsolateral periaqueductal gray and ventromedial hypothalamus fails to inhibit panic-like behaviour. Behav Brain Res 2008, 193(2):197-203.
68. Grove G., Coplan J.D., Hollander E. The neuroanatomy of 5-HT dysregulation and panic disorder. J Neuropsychiatry Clin Neurosci 1997, 9(2):198-207.
69. Sullivan G.M., Coplan J.D., Kent J.M., Gorman J.M. The noradrenergic system in pathological anxiety: a focus on panic with relevance to generalized anxiety and phobias. Biol Psychiatry 1999, 46(9):1205-1218.
70. Singewald N., Sharp T. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 2000, 98(4):759-770.
71. Szabo S.T., de Montigny C., Blier P. Progressive attenuation of the firing activity of locus ceruleus noradrenergic neurons by sustained administration of selective serotonin reuptake inhibitors. Int J Neuropsychopharmacol 2000, 3(1):1-11.
72. Gallego X., Murtra P., Zamalloa T., Canals J.M., Pineda J., Amador-Arjona A., et al. Increased opioid dependence in a mouse model of panic disorder. Front Behav Neurosci 2010, 3:60.
73. España R.A., Berridge C.W. Organization of noradrenergic efferents to arousal-related basal forebrain structures. J Comp Neurol 2006, 496(5):668-683.
74. Redmond D.E. The possible role of locus ceruleus noradrenergic activity in anxiety-panic. Clin Neuropharmacol 1986, 9(Suppl. 4):40-42.
75. Nutt D.J. Altered central alpha 2-adrenoceptor sensitivity in panic disorder. Arch Gen Psychiatry 1989, 46(2):165-169.
76. Gurguis G.N., Uhde T.W. Effect of yohimbine on plasma homovanillic acid in panic disorder patients and normal controls. Biol Psychiatry 1990, 28(4):292-296.
77. Protopopescu X., Pan H., Tuescher O., Cloitre M., Goldstein M., Engelien A., et al. Increased brainstem volume in panic disorder: a voxel-based morphometric study. Neuroreport 2006, 17(4):361-363.
78. Newman A.E., Soma K.K. Corticosterone and dehydroepiandrosterone in songbird plasma and brain: effects of season and acute stress. Eur J Neurosci 2009, 29(9):1905-1914.
79. Busnardo C., Tavares R.F., Resstel L.B., Elias L.L., Correa F.M. Paraventricular nucleus modulates autonomic and neuroendocrine responses to acute restraint stress in rats. Auton Neurosci 2010, 158(1-2):51-57.
80. Sterrenburg L., Gaszner B., Boerrigter J., Santbergen L., Bramini M., Roubos E.W., et al. Sex-dependent and differential responses to acute restraint stress of corticotropin-releasing factor-producing neurons in the rat paraventricular nucleus, central amygdala, and bed nucleus of the stria terminalis. J Neurosci Res 2012, 90(1):179-192.
81. 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. Braz J Med Biol Res 2011, 44(10):1048-1053.
82. Klein D.F. False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch Gen Psychiatry 1993, 50(4):306-317.
83. 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.
84. Graeff F.G. Anxiety, panic and the hypothalamic-pituitary-adrenal axis. Rev Bras Psiquiatr 2007, 29(Suppl. 1):S3-S6.
85. Graeff F.G., Garcia-Leal C., Del-Ben C.M., Guimarães F.S. Does the panic attack activate the hypothalamic-pituitary-adrenal axis?. An Acad Bras Cienc 2005, 77(3):477-491.
86. 2 inhalation study. Am J Psychiatry 2006, 163(4):738-740.
87. 2 challenge induced HPA axis activation in panic. Int J Neuropsychopharmacol 2007, 10(6):797-804.
88. Lanfumey L., Mongeau R., Cohen-Salmon C., Hamon M. Corticosteroid-serotonin interactions in the neurobiological mechanisms of stress-related disorders. Neurosc Biobehav Rev 2008, 32:1174-1184.
89. Härfstrand A., Fuxe K., Cintra A., Agnati L.F., Zini I., Wikström A.C., et al. Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc Natl Acad Sci U S A 1986, 83(24):9779-9783.
90. 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. J Steroid Biochem 1987, 27(1-3):159-170.
91. 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. Neurosci Res 1996, 26:235-269.
92. Pei Q., Zetterström T., Fillenz M. Tail pinch-induced changes in the turnover and release of dopamine and 5-hydroxytryptamine in different brain regions of the rat. Neuroscience 1990, 35(1):133-138.
93. Clement H.W., Schäfer F., Ruwe C., Gemsa D., Wesemann W. Stress-induced changes of extracellular 5-hydroxyindoleacetic acid concentrations followed in the nucleus raphe dorsalis and the frontal cortex of the rat. Brain Res 1993, 614(1-2):117-124.
94. Inoue T., Tsuchiya K., Koyama T. Regional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain. Pharmacol Biochem Behav 1994, 49(4):911-920.
95. Maswood S., Barter J.E., Watkins L.R., Maier S.F. Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res 1998, 783(1):115-120.
96. Grahn R.E., Will M.J., Hammack S.E., Maswood S., McQueenMB, Watkins L.R., et al. Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 1999, 826(1):35-43.
97. Greenwood B.N., Foley T.E., Day H.E., Campisi J., Hammack S.H., Campeau S., et al. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 2003, 23(7):2889-2898.