Involvement of nitric oxide-dependent pathways of dorsolateral periaqueductal gray in the effects of ethanol in rats submitted to the elevated plus-maze test

Behavioural Brain Research

Volumn 153, Issue 2, 2004, Pages 341-349

  Morato, Gina Struffaldi ^a   Ortiga, Roberta Moura ^a   Ferreira, Vania Maria Moraes ^a,b  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b FEDERAL UNIVERSITY OF PARÁ   (Brazil)

Author keywords

Anxiety; Elevated plus maze; Ethanol; Nitric oxide; Periaqueductal gray

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 7 NITROINDAZOLE; 8 BROMO CYCLIC GMP; ALCOHOL; GUANYLATE CYCLASE INHIBITOR; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE INHIBITOR; NITROPRUSSIDE SODIUM;

ANXIETY; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; EXPLORATORY BEHAVIOR; MALE; MAZE TEST; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; TRANQUILIZING ACTIVITY;

ANIMALS; AROUSAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; EXPLORATORY BEHAVIOR; FEAR; INJECTIONS, INTRAPERITONEAL; MALE; MAZE LEARNING; NEURAL PATHWAYS; NITRIC OXIDE; ORIENTATION; PERIAQUEDUCTAL GRAY; RATS; RATS, WISTAR; REACTION TIME;

EID: 3242686861     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2003.12.010     Document Type: Article

References (76)

1. Adams M.L., Meyer E.R., Sewing B.N., Cicero T.J. Effects of nitric oxide-related agents on alcohol narcosis. Alcohol. Clin. Exp. Res. 18:1994;969-975
2. Ahern G.P., Klyachkob V.A., Jackson M.B. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. TINS. 25:2002;510-517
3. Alabadi J.A., Thibault J.-L., Pinard E., Seylaz J., Lasbennes F. 7-Nitroindazole, a selective inhibitor of nNOS, increases hippocampal extracellular glutamate concentration in status epilepticus induced by kainic acid in rats. Brain Res. 839:1999;305-312
4. Albin R.L., Makowiec R.L., Hollingsworth Z., Dure L.S. 4th, Penney J.B., Young A.B. Excitatory amino acid binding sites in the periaqueductal gray of the rat. Neurosci. Lett. 118:1990;112-115
5. Amir S. N-Methyl-D-aspartate receptor-mediated signaling in the supraoptic nucleus involves activation of a nitric oxide-dependent pathway. Brain Res. 645:1994;330-334
6. Baretta I.P., Assreuy J., De Lima T.C. Nitric oxide involvement in the anxiogenic-like effect of substance P. Behav. Brain Res. 121:2001;199-205
7. Behbehani M.M. Functional characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 46:1995;575-605
8. Bertoglio L.J., Carobrez A.P. Anxiolytic effects of ethanol and phenobarbital are abolished in test-experienced rats submitted to the elevated plus maze. Pharmacol. Biochem. Behav. 73:2002;963-969
9. Bie B.H., Zhao Z.Q. Nitric oxide inhibits GABA-evoked current in dorsal root ganglion neuron via PKG-dependent pathway. Brain Res. Bull. 55:2001;335-339
10. Blanchard R.J., Magee L., Veniegas R., Blanchard D.C. Alcohol and anxiety: ethopharmacological approaches. Prog. Neuropsychopharmacol. Biol. Psych. 17:1993;171-182
11. Brandao M.L., de Aguiar J.C., Graeff F.G. GABA mediation of the anti-aversive action of minor tranquilizers. Pharmacol. Biochem. Behav. 16:1982;397-402
12. Bredt D., Snyder S.H. Isolation of nitric oxide synthase a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA. 87:1990;682-685
13. Carobrez A.P., Teixeira K.V., Graeff F.G. Modulation of defensive behavior by periaqueductal gray NMDA/glycine-B receptor. Neurosci. Biobehav. Rev. 25:2001;697-709
14. Carrive P., Schmitt P., Karli P. Flight induced by microinjection of D-tubocurarine or alpha-bungarotoxin into medial hypothalamus or periaqueductal gray matter: cholinergic or GABAergic mediation? Behav. Brain Res. 22:1986;233-248
15. Coop C.F., McNaughton N., Warnock K., Laverty R. Effects of ethanol and Ro 15-4513 in an electrophysiological model of anxiolytic action. Neuroscience. 35:1990;669-674
16. Costa E.T., Ferreira V.M., Valenzuela C.F. Evidence that nitric oxide regulates the acute effects of ethanol on rat N-methyl-D-aspartate receptors in vitro. Neurosci. Lett. 343:2003;41-44
17. De Oliveira R.M.W., Del Bel E.A., Guimarães F.S. Effects of excitatory amino acids and nitric oxide on flight behavior elicited from the dorsolateral periaqueductal gray. Neurosci. Behav. Rev. 25:2001;679-685
18. Del Bel E.A., Guimarães F.S. Sub-chronic inhibition of nitric-oxide synthesis modifies haloperidol-induced catalepsy and the number of NADPH-diaforase neurons in mice. Psychopharmacology. 147:2000;356-361
19. Dodd P.R., Beckmann A.M., Davidson M.S., Wilce P.A. Glutamate-mediated transmission, alcohol, and alcoholism. Neurochem. Int. 37:2000;509-533
20. Dudek B.C., Maio A., Phillips T.J., Perrone M. Naturalistic behavioral assessment of anxiolytic properties of benzodiazepines and ethanol in mice. Neurosci. Lett. 63:1986;265-270
21. Dunn R.W., Reed T.A., Copeland P.D., 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
22. East S.J., Garthwaite J. NMDA receptor activation in rat hippocampus induces cyclic GMP formation though the L-arginine-nitric oxide pathway. Neurosci. Lett. 123:1991;17-19
23. Fadda F., Rossetti Z.L. Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog. Neurobiol. 56:1998;385-431
24. Ferreira V.M., Morato G.S. D-cycloserine blocks the effects of ethanol and HA-966 in rats tested in the elevated plus-maze. Alcohol. Clin. Exp. Res. 21:1997;1638-1642
25. Ferreira V.M.M., Valenzuela C.F., Morato G.S. Role of nitric oxide-dependent pathways in ethanol-induced anxiolytic effects in rats. Alcohol. Clin. Exp. Res. 23:1999;1898-1904
26. Forstermann U., Closs E.I., Pollock J.S., Nakane M., Schwarz P., Gath I., et al. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension. 23:1994;1121-1131
27. Garthwaite J., Boulton C.L. Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57:1995;683-706
28. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. TINS. 14:1991;60-67
29. Graeff F.G., Silveira M.C., Nogueira R.L., Audi E.A., Oliveira R.M. Role of the amygdala and periaqueductal gray in anxiety and panic. Behav. Brain Res. 58:1993;123-131
30. Graeff F.G. Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals. Braz. J. Med. Biol. Res. 27:1994;811-829
31. Graeff F.G. Role of 5-HT in defensive behavior and anxiety. Rev. Neurosci. 4:1993;181-211
32. Graeff FG. Brain defense system and anxiety. In: Roth M, Burrows GD, Noyes R, editors. Handbook of anxiety. Amsterdam: Elsevier; 1990. p. 307-54.
33. Guimarães A.P., Guimarães F.S., Prado W.A. Modulation of carbachol-induced antinociception from the rat periaqueductal gray. Brain Res. Bull. 51:2000;471-478
34. Guimarães F.S., Carobrez A.P., De Aguiar J.C., 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
35. Guimarães F.S., de Aguiar J.C., Del Bel E.A., Ballejo G. Anxiolytic effect of nitric oxide synthase inhibitors microinjected into the dorsal central gray. NeuroReport. 5:1994;1929-1932
36. Handley S.L., Mithani S. Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of 'fear'-motivated behaviour. Naunyn Schmiedeberg's Arch. Pharmacol. 327:1984;1-5
37. Hoffman M. A new role for gases: neurotransmission. Science. 252:1991;1788
38. -. Neuron. 24:1999;461-469
39. Knych E.T. The role of endothelium in tolerance to ethanol-induced contraction of the rat aorta. Alcohol. Clin. Exp. Res. 11:1987;112-117
40. Krystal J.H., Petrakis I.L., Mason G., Trevisan L., D'Souza D.C. N-Methyl-D-aspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol. Ther. 99:2003;79-94
41. Langen B., Dietze S., Fink H. Acute effect of ethanol on anxiety and 5-HT in the prefrontal cortex of rats. Alcohol. 27:2002;135-141
42. Marras R.A., Martins A.P., Del Bel E.A., Guimarães F.S. L-NOARG, an inhibitor of nitric oxide synthase, induces catalepsy in mice. NeuroReport. 7:1995;158-160
43. Molchanov M.L., 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
44. Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol. Rev. 43:1991;109-142
45. Monti J.M., Hantos H., Ponzoni A., Monti D., Banchero P. Role of nitric oxide in sleep regulation: effects of L-NAME, an inhibitor of nitric oxide synthase, on sleep in rats. Behav. Brain Res. 100:1999;197-205
46. Monzon M.E., Varas M.M., De Barioglio S.R. Anxiogenesis induced by nitric oxide synthase inhibition and anxiolytic effect of melanin-concentrating hormone (MCH) in rat brain. Peptides. 22:2001;1043-1047
47. Moreira FA, Molchanov ML, Guimarães FS. Ionotropic glutamate-receptor antagonists inhibit the aversive effects of nitric oxide donor injected into the dorsolateral periaqueductal gray of rats. Psychopharmacology (Berl) 2004;171:199-203.
48. Murad F. Cellular signaling with nitric oxide and cyclic GMP. Braz J. Med. Biol Res. 32:1999;1317-1327
49. Naassila M., Beauge F.J., Sebire N., Daoust M. Intracerebroventricular injection of antisense oligos to nNOS decreases rat ethanol intake. Pharmacol. Biochem. Behav. 67:2000;629-636
50. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. USA. 88:1991;11285-11289
51. Oliveira R.M.W., Del Bel E.A., Mamede-Rosa M.L., Padovan C.M., Deakin J.F.W., Guimarães F.S. Expression of neuronal nitric oxide synthase mRNA in stress-related brain areas after restraint in rats. Neurosci. Lett. 289:2000;123-126
52. Oliveira R.W., Del Bel E.A., Guimarães F.S. Behavioral and c-fos expression changes induced by nitric oxide donors microinjected into the dorsal periaqueductal gray. Brain Res. Bull. 51:2000;457-464
53. Oliveira R.W., Guimarães F.S. Anxiolytic effect of methylene blue microinjected into the dorsal periaqueductal gray matter. Braz J. Med. Biol. Res. 32:1999;1529-1532
54. Onstott D., Mayer B., 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;317-324
55. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. San Diego: Academic Press; 1997.
56. 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. 14:1985;149-167
57. Peoples R.W., Li C., Weight F.F. Lipid versus protein theories of alcohol action in the nervous system. Annu. Rev. Pharmacol. Toxicol. 36:1996;185-201
58. Pontieri V., Venezuela M.K., Scavone C., Michelini C. Role of endogenous nitric oxide in the nucleus tratus solitarii on baroreflex control of heart rate in spontaneously hypertensive rats. J. Hypertens. 16:1998;1993-1999
59. Prast H., Tran M.H., Fischer H., Philippu A. Nitric oxide-induced release of acetylcholine in the nucleus accumbens: role of cyclic GMP, glutamate, and GABA. J. Neurochem. 71:1998;266-273
60. Rezvani A.H., Grady D.R., Peek A.E., Pucilowski O. Inhibition of nitric oxide synthesis attenuates alcohol consumption in two strains of alcohol-preferring rats. Pharmacol. Biochem. Behav. 50:1995;265-270
61. Russo A.S., Guimarães F.S., De Aguiar J.C., Graeff F.G. Role of benzodiazepine receptors located in the dorsal periaqueductal grey of rats in anxiety. Psychopharmacology. 110:1993;198-202
62. Schmitt M.L., Coelho W., Lopes-de-Souza A.S., Guimarães F.S., Carobrez A.P. Anxiogenic-like effect of glycine and D-serine microinjected into dorsal periaqueductal gray matter of rats. Neurosci. Lett. 189:1995;93-96
63. Schuman E.M., Madison D.V. Nitric oxide and synaptic function. Annu. Rev. Neurosci. 17:1994;153-183
64. Southam E., Garthwaite J. Comparative effects of some nitric oxide donors on cyclic GMP levels in rat cerebellar slices. Neurosci. Lett. 130:1991;107-111
65. Southam E., Garthwaite J. The nitric oxide-cyclic GMP signaling pathway in rat brain. Neuropharmacology. 32:1993;1267-1277
66. Spanagel R., Siegmund S., Cowen M., Schroff K.C., Schumann G., Fiserova M., et al. The neuronal nitric oxide synthase gene is critically involved in neurobehavioral effects of alcohol. J. Neurosci. 22:2002;8676-8683
67. Tabakoff B, Hellevuo K, Hoffman PL. Alcohol. In: Schuster CR, Gust SW, Kuhar M.J. editors. Handbook of experimental pharmacology: pharmacological aspects of drugs dependence. Berlin, Germany: Springer-Verlag; 1996. p. 373-458.
68. Tanaka T., Saito H., Matsuki N. Endogenous nitric oxide inhibits NMDA- and kainate-responses by a negative feedback system in rat hippocampal neurons. Brain Res. 631:1993;72-76
69. Teixeira K.V., Carobrez A.P. Effects of glycine or (+/-)-3-amino-1- hydroxy-2-pyrrolidone microinjections along the rostrocaudal axis of the dorsal periaqueductal gray matter on rats' performance in the elevated plus-maze task. Behav. Neurosci. 113:1999;196-203
70. Uzbay I.T., Erden B.F., Tapanyigit E.E., Kayaalp S.O. Nitric oxide synthase inhibition attenuates signs of ethanol withdrawal in rats. Life Sci. 61:1997;2197-2209
71. Volke V., Koks S., Vasar E., Bourin M., Bradwejn J., Mannisto P.T. Inhibition of nitric oxide synthase causes anxiolytic-like behavior in an elevated plus-maze. NeuroReport. 6:1995;1413-1416
72. Wall M.J. Endogenous nitric oxide modulates GABAergic transmission to granule cells in adult rat cerebellum. Eur. J. Neurosci. 18:2003;869-878
73. Wazlawik E, Morato GS. Influence of drugs acting on nitric oxide-dependent pathways on ethanol tolerance in rats. Psychopharmacology (Berl) 2003;170:343-50.
74. Wazlawik E., Morato G.S. Effects of intracerebroventricular administration of 7-nitroindazole on tolerance to ethanol. Brain Res. Bull. 57:2002;165-170
75. Yang L., Long C., Evans M.S., Faingold C. Ethanol withdrawal results in aberrant membrane properties and synaptic responses in periaqueductal gray neurons associated with seizure susceptibility. Brain Res. 957:2002;99-108
76. Zhuo M., Small A.S., Kandel E.R., Hawkins R.D. Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science. 260:1993;1946-1950