Activation of neurons containing the enzyme nitric oxide synthase following exposure to an elevated plus maze

Brain Research Bulletin

Volumn 69, Issue 4, 2006, Pages 347-355

  Beijamini, Vanessa ^a   Guimarães, Francisco Silveira ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Anxiety; c Fos; Elevated plus maze; NADPH diaphorase

Indexed keywords

NITRIC OXIDE SYNTHASE; PROTEIN C FOS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; EVALUATION; FEAR; HISTOCHEMISTRY; HYPOTHALAMUS NUCLEUS; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; MALE; MAMMILLARY BODY; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; STATISTICAL SIGNIFICANCE; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS;

ANIMALS; ANXIETY; BRAIN; FEAR; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR;

EID: 33646032088     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2006.02.006     Document Type: Article

References (92)

1. Adamec R.E., Sayin U., and Brown A. The effects of corticotrophin releasing factor (CRF) and handling stress on behavior in the elevated plus-maze test of anxiety. J. Psychopharmacol. 5 (1991) 175-186
2. Aguilera G. Corticotropin releasing hormone, receptor regulation and stress response. Trends Endocrinol. Metab. 9 (1998) 329-336
3. Amir S., Rackover M., and Funk D. Blockers of nitric oxide synthase inhibit stress activation of c-Fos expression in the neurons of the hypothalamic paraventricular nucleus in the rat. Neuroscience 77 (1997) 623-627
4. Asano Y. Characteristics of open field behavior of Wistar and Sprague-Dawley rats. Jikken Dobutsu 35 (1986) 505-508
5. Asanuma M., Ogawa N., Hirata H., Chou H., Tanaka K., and Mori A. Opposite effects of rough and gentle handling with repeated saline administration on c-fos mRNA expression in the rat brain. J. Neural Transm. Gen. Sect. 90 (1992) 163-169
6. Bandler R., and Shipley M.T. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?. Trends Neurosci. 17 (1994) 379-389
7. Bernard J.K., and Bandler R. Parallel circuits for emotional coping behaviour: new pieces in the puzzle. J. Comp. Neurol. 401 (1998) 429-436
8. Berrino L., Pizzirusso A., Maione S., Vitagliano S., D'Amico M., and Rossi F. Hypothalamic paraventricular nucleus involvement in the pressor response to N-methyl-d-aspartic acid in the periaqueductal grey matter. Naunyn Schmiedebergs Arch. Pharmacol. 353 (1996) 157-160
9. Bertoglio L.J., and Carobrez A.P. Behavioral profile of rats submitted to session 1-session 2 in the elevated plus-maze during diurnal/nocturnal phases and under different illumination conditions. Behav. Brain Res. 132 (2002) 135-143
10. Blanchard D.C., Li C.I., Hubbard D., Markham C.M., Yang M., Takahashi L.K., and Blanchard R.J. Dorsal premammillary nucleus differentially modulates defensive behaviors induced by different threat stimuli in rats. Neurosci. Lett. 345 (2003) 145-148
11. Brett R.R., and Pratt J.A. Limitations of the elevated plus-maze test for assessing the effects of chronic benzodiazepine administration. Br. J. Pharmacol. 96 (1989) 313
12. Carobrez A.P., and Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: The elevated plus-maze model 20 years on. Neurosci. Biobehav. Rev. 29 (2005) 1193-1205
13. Carobrez A.P., Teixeira K.V., and Graeff F.G. Modulation of defensive behavior by periaqueductal gray NMDA/glycine-B receptor. Neurosci. Biobehav. Rev. 25 (2001) 697-709
14. Carrive P. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav. Brain Res. 58 (1993) 27-47
15. Ceccatelli S., Villar M.J., Goldstein M., and Hokfelt T. Expression of c-Fos immunoreactivity in transmitter-characterized neurons after stress. Proc. Natl. Acad. Sci. 86 (1989) 9569-9573
16. Celada P., Casanovas J.M., Paez X., and Artigas F. Control of serotonergic neurons in the dorsal raphe nucleus by the lateral hypothalamus. Brain Res. 932 (2002) 79-90
17. Costa A., Trainer P., Besser M., and Grossman A. Nitric oxide modulates the release of corticotropin-releasing hormone from the rat hypothalamus in vitro. Brain Res. 605 (1993) 187-192
18. Cullinan W.E., Herman J.P., Battaglia D.F., Akil H., and Watson S.J. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64 (1995) 477-505
19. Dawson G.R., and Tricklebank M.D. Use of elevated plus-maze in the search for novel anxiolytic agents. Trends Pharmacol. Sci. 16 (1995) 33-36
20. Decker M.W., Curzon P., and Brioni J.D. Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety and locomotor activity in rats. Neurobiol. Learn. Mem. 64 (1995) 156-168
21. De Oliveira R.W., and Guimarães F.S. Anxiolytic effect of methylene blue microinjected into the dorsal periaqueductal gray matter. Braz. J. Med. Biol. Res. 32 (1999) 1529-1532
22. De Oliveira R.W., Del Bel E.A., and Guimarães F.S. Effects of excitatory amino acids and nitric oxide on flight behavior elicited from the dorsal periaqueductal gray. Neurosci. Biobehav. Rev. 25 (2001) 679-685
23. De Oliveira R.W., Del-Bel E.A., Mamede-Rosa M.L., Padovan C.M., Deakin J.F., and Guimarães F.S. Expression of neuronal nitric oxide synthase mRNA in stress-related brain areas after restraint stress. Neurosci. Lett. 289 (2000) 123-126
24. De Oliveira R.W., Forestiero D., Manfrim C.M., and Guimarães F.S. Anxiolytic effect induced by nitric oxide synthase inhibitors microinjected at medial amygdala of rats. Psychopharmacology 184 (2006) 166-172
25. Duncan G.E., Knapp D.J., and Breese G.R. Neuroanatomical characterization of Fos induction in rat behavioral models of anxiety. Brain Res. 713 (1996) 76-91
26. Dunn R.W., Reed T.A., Copeland P.D., and Frye C.A. The nitric oxide synthase inhibitor 7-nitroindazole displays enhanced anxiolytic efficacy without tolerance in rats following subchronic administration. Neuropharmacology 37 (1998) 899-904
27. Eroglu L., and Caglayan B. Anxiolytic and antidepressant properties of methylene blue in animal models. Pharmacol. Res. 36 (1997) 381-385
28. Falter U., Gower A.J., and Gobert J. Resistance of baseline activity in the elevated plus-maze to exogenous influences. Behav. Pharmacol. 3 (1992) 123-128
29. Faria M.S., Muscara M.N., Moreno J.R.H., Teixeira A.S., Dias H.B., De Oliveira B., Graeff F.G., and De Nucci G. Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test. Eur. J. Pharmacol. 323 (1997) 37-43
30. Fernandez-Teruel A., Escorihuela R.M., Boix F., and Tobena A. Effects of different handling stimulation procedures and benzodiazepines on two-way active avoidance acquisition in rats. Pharmacol. Res. 24 (1991) 1273-1282
31. File S.E. Behavioral detection of anxiolytic action. In: Elliott J.M., Heal D.J., and Marsden C.A. (Eds). Experimental Approaches to Anxiety and Depression (1992), John Wiley & Sons Ltd., New York 25-44
32. Graeff F.G., Guimarães F.S., Andrade R.G.S., and Deakin J.F.W. Role of 5-HT in stress, anxiety and depression. Pharmacol. Biochem. Behav. 54 (1996) 129-14146]
33. Grahn R.E., Watkins L.R., and Maier S.F. Impaired escape performance and enhanced conditioned fear in rats following exposure to an uncontrollable stressor are mediated by glutamate and nitric oxide in the dorsal raphe nucleus. Behav. Brain. Res. 112 (2000) 33-41
34. Guimarães F.S., Beijamini V., Moreira F.A., Aguiar D.C., and De Luca A.C.B. Role of nitric oxide on brain regions related to defensive reactions. Neurosci. Biobehav. Rev. 29 (2005) 1313-1322
35. Guimarães F.S., Carobrez A.P., De Aguiar J.C., and Graeff F.G. Anxiolytic effect in the elevated plus-maze of the NMDA receptor antagonist AP7 microinjected into the dorsal periaqueductal gray. Psychopharmacology 103 (1991) 91-94
36. Guimarães F.S., De Aguiar J.C., Del Bel E.A., and Ballejo G.O. Anxiolytic effect of nitric oxide synthase inhibitors microinjected into the dorsal central grey. Neuroreport 5 (1994) 1929-1932
37. Handa R.J., Nunley K.M., and Bollnow M.R. Induction of c-fos mRNA in the brain and anterior pituitary gland by a novel environment. Neuroreport 4 (1993) 1079-1082
38. Handley S.L., and Mithani S. Effects of alpha-adrenoceptors agonists and antagonists in a maze-exploration of fear-motivated behaviour. Naunyn Schmiedebergs Arch. Pharmacol. 324 (1984) 1-5
39. Harbuz M.S., and Lightman S.L. Stress and the HPA axis: acute, chronic and immune interactions. J. Endocrinol. 134 (1992) 327-339
40. Hinks G.L., Brown P., Field M., Poat J.A., and Hughes J. The anxiolytics CI-988 and chlordiazepoxide fail to reduce immediate early gene mRNA stimulation following exposure to the rat elevated X-maze. Eur. J. Pharmacol. 312 (1996) 153-161
41. Hope B.T., Michael G.J., Knigge K.M., and Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. 88 (1991) 2811-2814
42. Iwata J., LeDoux J.E., and Reis D.J. Destruction of intrinsic neurons in the lateral hypothalamus disrupts the classical conditioning of autonomic but not behavioral emotional responses in the rat. Brain Res. 368 (1986) 161-166
43. Jahng J.W., Lee J.H., Lee S., Lee J.Y., Kim G.T., Houpt T.A., and Kim D.G. N(omega)-nitro-l-arginine methyl ester attenuates lithium-induced c-Fos, but not conditioned taste aversion, in rats. Neurosci. Res. 50 (2004) 485-492
44. Johnson M.D., and Ma P.M. Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain. J. Comp. Neurol. 332 (1993) 391-406
45. Kerr J.E., Beck S.G., and Handa R.J. Androgens selectively modulate C-fos messenger RNA induction in the rat hippocampus following novelty. Neuroscience 74 (1996) 757-766
46. Kjelstrup K.G., Tuvnes F.A., Steffenach H.A., Murison R., Moser E.I., and Moser M.B. Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. 99 (2002) 10825-10830
47. Krukoff T.L., and Khalili P. Stress-induced activation of nitric oxide-producing neurons in the rat brain. J. Comp. Neurol. 377 (1997) 509-519
48. Lee S., Kim C.K., and Rivier C. Nitric oxide stimulates ACTH secretion and the transcription of the genes encoding for NGFI-B, corticotropin-releasing factor, corticotropin-releasing factor receptor type 1, and vasopressin in the hypothalamus of the intact rat. J. Neurosci. 19 (1997) 7640-7647
49. Lee H.S., Kim M.A., Valentino R.J., and Waterhouse B.D. Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res. 963 (2003) 57-71
50. Lino De Oliveira C., Guimarães F.S., and Del Bel E.A. Effects of L-NOARG on plus-maze performance in rats. Pharmacol. Biochem. Behav. 56 (1997) 55-59
51. Lister R. Ethologically-based animal models of anxiety disorders. Pharmacol. Ther. 46 (1990) 321-340
52. Marquez C., Nadal R., and Armario A. Responsiveness of the hypothalamic-pituitary-adrenal axis to different novel environments is a consistent individual trait in adult male outbred rats. Psychoneuroendocrinology 30 (2005) 179-187
53. Martinez M., Phillips P.J., and Herbert J. Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur. J. Neurosci. 10 (1998) 20-33
54. Matsumoto T.M., Nakane M., Pollock J.S., Kuk J.E., and Forstermann U.T.M. A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci. Lett. 155 (1993) 61-64
55. McHugh S.B., Deacon R.M., Rawlins J.N., and Bannerman D.M. Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav. Neurosci. 118 (2004) 63-78
56. McNaughton N., and Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci. Biobehav. Rev. 28 (2004) 285-305
57. Molchanov M.L., and Guimarães F.S. Anxiolytic-like effects of AP7 injected into the dorsolateral or ventrolateral columns of the periaqueductal gray of rats. Psychopharmacology 160 (2002) 30-38
58. Montgomery K.C. The relation between fear induced by novel stimulation and exploratory behaviour. J. Comp. Neurol. 48 (1955) 254-260
59. Morgan J.I., and Curran T. Role of ion flux in the control of c-fos expression. Nature 322 (1986) 552-555
60. Morrow B.A., Redmond A.J., Roth R.H., and Elsworth J.D. The predator odor, TMT, displays a unique, stress-like pattern of dopaminergic and endocrinological activation in the rat. Brain Res. 864 (2000) 146-151
61. Netto C.F., and Guimarães F.S. Anxiogenic effect of cholecystokinin in the dorsal periaqueductal gray. Neuropsychopharmacology 29 (2004) 101-107
62. Ohl F. Testing for anxiety. Clin. Neurosci. Res. 3 (2003) 233-238
63. Onstott D., Mayer B., and Beitz A.J. Nitric oxide synthase immunoreactive neurons anatomically define a longitudinal dorsolateral column within the midbrain periaqueductal gray of the rat: analysis using laser confocal microscopy. Brain Res. 610 (1993) 3317-3324
64. Padovan C.M., and Guimarães F.S. Restraint-induced hypoactivity in an elevated plus-maze. Braz. J. Med. Biol. Res. 33 (2000) 79-83
65. Papa M., Pellicano M.P., Cerbone A., Lamberti-D'Mello C., Menna T., Buono C., Giuditta A., Welzl H., and Sadile A.G. Immediate early genes and brain DNA remodelling in the Naples high- and low-excitability rat lines following exposure to a spatial novelty. Brain Res. Bull. 37 (1995) 111-118
66. Papa M., Pellicano M.P., Welzl H., and Sadile A.G. Distributed changes in c-Fos and c-Jun immunoreactivity in the rat brain associated with arousal and habituation to novelty. Brain Res. Bull. 32 (1993) 509-515
67. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. third ed. (1997), Academic Press, New York
68. Pellow S., Chopin P., File S.E., and Briley M. Validation of open-closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14 (1985) 149-167
69. Pellow S., and File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 24 (1986) 525-529
70. Quock R.M., and Nguyen E. Possible involvement of nitric oxide in chlordiazepoxide-induced anxiolysis in mice. Life Sci. 51 (1992) L255-L260
71. Rex A., Thomas H., Hortnagl H., Voits M., and Fink H. Behavioural and microdialysis study after neurotoxic lesion of the dorsal raphe nucleus in rats. Pharmacol. Biochem. Behav. 74 (2003) 587-593
72. Rivier C. Role of gaseous neurotransmitters in the hypothalamic-pituitary-adrenal axis. Ann. N.Y. Acad. Sci. 933 (2001) 254-264
73. Rodgers R.J., Cao B.J., Dalvi A., and Holmes A. Animal models of anxiety: an ethological perspective. Braz. J. Med. Biol. Res. 30 (1997) 289-304
74. Salomé N., Salchner P., Viltart O., Sequeira H., Wigger A., Landgraf R., and Singewald N. Neurobiological Correlates of High (HAB) Versus Low Anxiety-Related Behavior (LAB): Differential Fos Expression in HAB and LAB Rats. Biol. Psychiatry 55 (2004) 715-723
75. Schenberg L.C., Bittencourt A.S., Sudré E.C.M., and Vargas L.C. Modeling panic attacks. Neurosci. Biobehav. Rev. 25 (2001) 647-659
76. Schmitt U., and Hiemke C. Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling. Pharmacol. Biochem. Behav. 59 (1998) 807-811
77. Schuman E.M., Meffert M.K., Schulman H., and Madison D.V. An ADP-ribosiltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc. Natl. Acad. Sci. 91 (1994) 111958-111962
78. Sharp F.R., Sagar S.M., Hicks K., Lowenstein D., and Hisanaga K. c-fos mRNA, Fos, and Fos-related antigen induction by hypertonic saline and stress. J. Neurosci. 11 (1991) 2321-2331
79. Silveira M.C.L., Graeff F.G., and Sandner G. Regional distribution of Fos-like immunoreactivity in the rat brain after exposure to fear-inducing stimuli. Braz. J. Med. Biol. Res. 27 (1994) 1077-1081
80. Silveira M.C.L., Sandner G., and Graeff F.G. Induction of Fos immunoreactivity in the brain by exposure to the elevated plus-maze. Behav. Brain Res. 56 (1993) 115-118
81. Sommer W., Möller C., Wiklund L., Thorsell A., Rimondini R., Nissbrandt H., and Heilig M. Local 5,7-dihydroxytryptamine lesions of rat amygdala: Release of punished drinking, unaffected plus-maze behavior and ethanol consumption. Neuropsychopharmacology 24 (2001) 430-440
82. Swanson L.H., and Petrovich G.D. What is the amygdala?. Trends Neurosci. 21 (1998) 323-331
83. Treit D., and Menard J. Dissociations among the anxiolytic effects of septal, hippocampal, and amygdaloid lesions. Behav. Neurosci. 111 (1997) 653-658
84. Treit D., Pesold C., and Rotzinger S. Dissociating the anti-fear effects of septal and amygdala lesions using two pharmacologically validated models of rat anxiety. Behav. Neurosci. 107 (1993) 770-785
85. Treit D., Robinson A., Rotzinger S., and Pesold C. Anxiolytic effects of serotonergic interventions in the shock-probe burying test and the elevated plus-maze test. Behav. Brain Res. 31 (1993) 23-34
86. Vincent S.R., and Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46 (1992) 755-784
87. Volke V., Soosaar A., Koks S., Bourin M., and Mannisto P.T. Inhibition of nitric oxide synthase causes anxiolytic-like behaviour in an elevated plus-maze. Neuroreport 6 (1995) 1413-1416
88. Wang Q.P., Guan J.L., and Nakai Y. Distribution and synaptic relations of NOS neurons in the dorsal raphe nucleus: a comparison to 5-HT neurons. Brain Res. Bull. 37 (1995) 177-187
89. Watanabe Y., Stone E., and McEwen B.S. Induction and habituation of c-fos and zif/268 by acute and repeated stressors. Neuroreport 5 (1994) 1321-1324
90. Wiley J.L., Cristello A.F., and Balster R.L. Effects of site-selective NMDA receptor antagonists in an elevated plus-maze model of anxiety in mice. Eur. J. Pharmacol. 294 (1995) 101-107
91. Wotherspoon G., Albert M., Rattray M., and Priestley J.P. Serotonin and NADPH-diaphorase in the dorsal raphe nucleus of the adult rat. Neurosci. Lett. 173 (1994) 31-36
92. Yao S.T., Gouraud S., Paton P.F., and Murphy D. Water deprivation increases the expression of neuronal nitric oxide synthase (nNOS) but not orexin-A in the lateral hypothalamic area of the rat. J. Comp. Neurol. 490 (2005) 180-193