Systemic administration of a nitric oxide synthase inhibitor impairs fear sensitization in the plus-maze

Neurobiology of Learning and Memory

Volumn 90, Issue 2, 2008, Pages 455-459

  Sakae, Diana Yae ^a   Pereira, Lenir Orlandi ^a   da Cunha, Isabel Cristina ^a,b   de Lima, Thereza Christina Monteiro ^a   Paschoalini, Marta Aparecida ^a   Faria, Moacir Serralvo ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSITY OF SOUTHERN SANTA CATARINA   (Brazil)

Author keywords

Fear; l NAME; Nitric oxide; Plus maze; Rat

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONTROLLED STUDY; ENZYME SYNTHESIS; FEAR; LOCOMOTION; MALE; MAZE TEST; NONHUMAN; RAT; SPATIAL DISCRIMINATION; TIME PERCEPTION;

ANIMALS; AROUSAL; ASSOCIATION LEARNING; DOSE-RESPONSE RELATIONSHIP, DRUG; FEAR; MALE; MAZE LEARNING; MENTAL RECALL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; RATS; RATS, WISTAR; REACTION TIME;

EID: 48549097397     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2008.05.007     Document Type: Article

References (53)

1. Akar F.Y., Ulak G., Tanyeri P., Erden F., Utkan T., and Gacar N. 7-Nitroindazole, a neuronal nitric oxide synthase inhibitor, impairs passive-avoidance and elevated plus-maze memory performance in rats. Pharmacology, Biochemistry and Behavior 87 (2007) 434-443
2. Almeida S.S., Garcia R.A., and De Oliveira L.M. Effects of early protein malnutrition and repeated testinfo upon locomotor and exploratory behaviors in the elevated plus-maze. Physiology and Behavior 54 (1993) 749-752
3. Bernabeu R., Levi de Stein M., Fin C., Izquierdo I., and Medina J.H. Role of hippocampal NO in the acquisition and consolidation of inhibitory avoidance learning. Neuroreport 6 (1995) 1498-1500
4. Calixto A.V., Duarte F.S., Moraes C.K.L., Faria M.S., and De Lima T.C.M. Nitric oxide involvement and neural substrates of the conditioned and innate fear as evaluated in the T-maze test in rats. Behavioural Brain Research 189 (2008) 341-349
5. Calixto A.V., Vandressen N., Nucci G., Moreno Jr. H., and Faria M.S. Nitric oxide may underlie learned fear in the elevated T-maze. Brain Research Bulletin 55 (2001) 37-42
6. DaCunha I.C., José R.F., OrlandiPereira L., Pimenta J.A., OliveiradeSouza I.A., Reiser R., et al. The role of nitric oxide in the emotional learning of rats in the plus-maze. Physiology and Behavior 84 (2005) 351-358
7. Dal-Cól M.L.C., OrlandiPereira L., Rosa V.P., Calixto A.V., Carobrez A.P., and Faria M.S. Lack of midazolam-induced anxiolysis in the plus-maze Trial2 is dependent on the length of Trial 1. Pharmacology, Biochemistry and Behavior 74 (2003) 395-400
8. Dawson G.R., Crawford S.P., Stanhope K.J., Iversen S.D., and Tricklebank M.D. One-trial tolerance to the effects of chlordiazepoxide on the elevated plus maze may be due to locomotor habituation, not repeated drug exposure. Psychopharmacology 113 (1994) 570-572
9. De Oliveira C.L., Del-Bel E.A., and Guimarães F.S. Effects of l-NOARG on plus-maze performance in rats. Pharmacology, Biochemistry and Behavior 56 (1997) 55-59
10. De Oliveira R.W., Del-Bel E.A., and Guimarães F.S. Behavioral and c-fos expression changes induced by nitric oxide donors microinjected into the dorsal periaqueductal gray. Brain Research Bulletin 51 (2000) 457-464
11. 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
12. Eroglu L., and Caglayan B. Anxiolytic and antidepressant properties of methylene blue in animal models. Pharmacological Research 36 (1997) 381-385
13. Eskiocak S., Gozen A.S., Taskiran A., Kilic A.S., Eskiocak M., and Gulen S. Effect of psychological stress on the l-arginine-nitric oxide pathway and semen quality. Brazilian Journal of Medical and Biological Research 39 (2006) 581-588
14. Faria M.S., Muscará M.N., Moreno Jr. H., Teixeira S.A., Dias H.B., De Oliveira B., et al. Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test. European Journal of Pharmacology 323 (1997) 37-43
15. File S.E. Behavioural detection of anxiolytic action. In: Elliot J.M., Heal C.A., and Marsden C.A. (Eds). Experimental approaches to anxiety and depression (1992), Elsevier, Amsterdam 25-44
16. File S.E. The interplay of learning and anxiety in the elevated plus-maze. Behavioural Brain Research 58 (1993) 199-202
17. File S.E., Gonzalez L.E., and Gallant R. Role of the basolateral nucleus of the amygdala in the formation of a phobia. Neuropsychopharmacology 19 (1998) 397-405
18. Fin C., Da Cunha C., Bromberg E., Schmitz P.K., Bianchin M., Medina J.H., et al. Experiments suggesting a role for nitric oxide in the hippocampus in memory processes. Neurobiology of Learning and Memory 63 (1995) 113-115
19. Ghizoni D.M., João L.M., Moratelli Neto L., Da Cunha I.C., OrlandiPereira L., Borges F.R.M., et al. The effects of metabolic stress and vagotomy on emotional learning in an animal model of anxiety. Neurobiology of Learning and Memory 86 (2006) 107-116
20. Godinho M.A.A., Meneghini L., Lucinda A.M., Borges F.R.M., Sakae D.Y., Marino Neto J., et al. An approach to evaluate the ability of rats to discriminate different levels of illumination in the plus maze test: Effects of scopolamine. Behavioural Brain Research 181 (2007) 86-94
21. Goldblatt H., Lynch J., Hanzal R.F., and Summerville W.W. Studies on experimental hypertension. The production persistent elevation of systolic blood pressure by means of renal ischemia. Journal of Experimental Medicine 59 (1934) 347-356
22. Griebel G., Rodgers R.J., Perrault G., and Sanger D.J. Risk assessment behaviour: Evaluation of utility in the study of 5-HT-related drugs in the rat elevated plus-maze test. Pharmacology, Biochemistry and Behavior 57 (1997) 817-827
23. Handley S.L., and Mithani S. Effects of α2-adrenoceptor agonists and antagonists in a maze exploration model of fear-motivated behaviour. Naunyn Schimiedeberg's Archives of Pharmacology 327 (1984) 1-5
24. Holmes A., and Rodgers R.J. Responses of Swiss Webster mice to repeated plus-maze experience: Further evidence for a qualitative shift in emotional state?. Pharmacology Biochemistry and Behavior 60 (1998) 473-488
25. Hölscher C. Nitric oxide, the enigmatic neuronal messenger: Its role in synaptic plasticity. Trends in Neurosciences 20 (1997) 298-303
26. Kaya B., Unal S., Karabulut A.B., and Turkoz Y. Altered diurnal variation of nitric oxide production in patients with panic disorder. Tohoku Journal of Experimental Medicine 204 (2004) 147-154
27. Krukoff T.L., and Khalili P. Stress-induced activation of nitric oxide-producing neurons in the rat brain. Journal of Comparative Neurology 377 (1997) 509-519
28. Lamprea M.R., Cardenas F.P., Silveira R., Morato S., and Walsh T.J. Dissociation of memory and anxiety in a repeated elevated plus maze paradigm: Forebrain cholinergic mechanisms. Behavioural Brain Research 117 (2000) 97-105
29. Lee C., and Rodgers R.J. Antinociceptive effects of the elevated plus-maze: Influence of the opiate receptor manipulations. Psychopharmacology 102 (1990) 507-513
30. Lister R.G. Ethologically-based animal models of anxiety disorders. Pharmacology and Therapeutics 46 (1990) 321-340
31. Moncada S., Palmer R.M., and Higgs E.A. Nitric oxide: Physiology pathology and pharmacology. Pharmacological Reviews 43 (1991) 109
32. Orlandi Pereira L., Da Cunha I.C., Marino Neto J., Paschoalini M.A., and Faria M.S. The gradient of luminosity between open/enclosed arms, and not the absolute level of lux, predicts the behaviour of rats in the plus maze. Behavioural Brain Research 159 (2005) 55-61
33. Ottoni E.B. EthoLog2.2: A tool for the transcription and timing of behaviour observation sessions. Behavior Research Methods, Instruments, & Computers 32 (2000) 446-449
34. 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. Journal of Neuroscience Methods 14 (1985) 149-167
35. Podhorna J., and Brown R.E. Inhibition of nitric oxide synthase reduces ultrasonic vocalizations of rat pups. European Journal of Pharmacology 382 (1999) 143-150
36. Podhorna J., and Brown R.E. Interactions between N-methyl-d-aspartate and nitric oxide in the modulation of ultrasonic vocalizations of infant rats. European Journal of Pharmacology 408 (2000) 265-271
37. Prast H., and Philippu A. Nitric oxide as a modulator of neuronal function. Progress in Neurobiology 64 (2001) 51-56
38. Quirk G.J., Russo G.K., Barron J.L., and Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. Journal of Neurosciences 20 (2000) 6225-6231
39. Rodgers R.J., and Cole J.C. The elevated plus-maze: Pharmacology, methodology and ethology. In: Cooper S.J., and Hendrie C.A. (Eds). Ethology and psychopharmacology (1994), John Wiley and Sons, Ltd., Chichester 9-44
40. Rodgers R.J., Johnson N.J.T., Cole J.C., Dewar C.V., Kidd G.R., and Kimpson P.H. Plus-maze retest profile in mice: Importance of initial stages of trial 1 and response to post-trial cholinergic receptor blockade. Pharmacology, Biochemistry and Behavior 54 (1996) 41-50
41. Rodgers O.J., Lee C., and Shepherd J.K. Effects of diazepam on behavioral and antinociceptive responses to the elevated plus-maze in male mice depend upon treatment regimen and prior maze experience. Psychopharmacology 106 (1992) 102-110
42. Rodgers R.J., and Shepherd J.K. Influence of prior maze experience on behavior and response to diazepam in the elevated plus-maze and light/dark tests of anxiety in mice. Psychopharmacology 113 (1993) 237-242
43. Rosa V.P., Vandresen N., Calixto A.V., Kovaleski D.F., and Faria M.S. Temporal analysis of the rat's behavior in the plus-maze: Effect of midazolam. Pharmacology, Biochemistry and Behavior 67 (2000) 177-182
44. Setem J., Pinheiro A.P., Motta V.A., Morato S., and Cruz A.P.M. Ethopharmacological analysis of 5-HT ligands on the rat elevated plus-maze. Pharmacology, Biochemistry and Behavior 62 (1999) 515-521
45. Spolidório P.C., Echeverry M.B., Iyomasa M., Guimarães F.S., and Del-Bel E.A. Anxiolytic effects induced by inhibition of the nitric-oxide-cGMP pathway in the rat dorsal hippocampus. Psychopharmacology (Berlin) 195 (2007) 183-192
46. Treit D., Menard J., and Royan C. Anxiogenic stimuli in the elevated plus-maze. Pharmacology Biochemistry and Behavior 44 (1993) 463-469
47. Vale A.L., Green S., Montgomery A.M., and Shafi S. The nitric oxide synthesis inhibitor l-NAME produces anxiogenic-like effects in the rat elevated plus-maze test, but not in the social interaction test. Journal of Psychopharmacology 12 (1998) 268-272
48. Vincent S.R. Nitric oxide: A radical neurotransmitter in the central nervous system. Progress in Neurobiology 42 (1994) 129-160
49. Vincent S.R., and Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46 (1992) 755-784
50. Volke V., Soosaar A., Koks S., Bourin M., Mannisto P.T., and Vasar E. 7-Nitroindazole, a nitric oxide synthase inhibitor, has anxiolytic-like properties in exploratory models of anxiety. Psychopharmacology (Berlin) 131 (1997) 399-405
51. Volke V., Soosaar A., Koks S., Vasar E., and Mannisto P.T. l-Arginine abolishes the anxiolytic-like effect of diazepam in the elevated plus-maze test in rats. European Journal of Pharmacology 351 (1998) 287-290
52. Yildiz F., Ulak G., Erden B.F., and Gacar N. Anxiolytic-like effects of 7-nitroindazole in the rat plus-maze test. Pharmacology, Biochemistry and Behavior 65 (2000) 199-202
53. Zou L.B., Yamada K., Tanaka T., Kameyama T., and Nabeshima T. Nitric oxide synthase inhibitors impair reference memory formation in a radial arm maze task in rats. Neuropharmacology 37 (1998) 323-330