Involvement of hippocampal nitric oxide in spatial learning in the rat

Neurobiology of Learning and Memory

Volumn 90, Issue 2, 2008, Pages 413-419

  Majlessi, Nahid ^a   Choopani, Samira ^a   Bozorgmehr, Tahereh ^a   Azizi, Zahra ^a  

^a PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Hippocampus; Morris water maze; Nitric oxide; Spatial learning

Indexed keywords

ARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; HISTOLOGY; LEARNING; MALE; MAZE TEST; NONHUMAN; RAT; SENSORIMOTOR CORTEX; SPATIAL DISCRIMINATION;

ANIMALS; ESCAPE REACTION; HIPPOCAMPUS; MALE; MAZE LEARNING; MENTAL RECALL; MOTIVATION; NEURONAL PLASTICITY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; ORIENTATION; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR; REACTION TIME;

EID: 48549086812     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2008.04.010     Document Type: Article

References (62)

1. Antonov I., Ha T., Antonova I., Moroz L.L., and Hawkins R.D. Role of nitric oxide in classical conditioning of siphon withdrawal in aplysia. The Journal of Neuroscience 27 (2007) 10993-11002
2. Arancio O., Kiebler M., Lee C.J., Lev-Ram V., Tsien R.T., Kandel E.R., et al. Nitric oxide acts directly in the pre-synaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87 (1996) 1025-1035
3. Bannerman D.M., Chapman P.F., Kelly P.A., Butcher S.P., and Morris R.G. Inhibition of nitric oxide synthase does not impair spatial learning. The Journal of Neuroscience 14 (1994) 7404-7414
4. Bannerman D.M., Chapman P.F., Kelly P.A., Butcher S.P., and Morris R.G. Inhibition of nitric oxide synthase does not prevent the induction of long-term potentiation in vivo. The Journal of Neuroscience 14 (1994) 7415-7425
5. Bernabeu R., de Stein M.L., 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
6. Bliss T.V.P., and Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
7. Blokland A., de Vente J., Prickaerts J., Honig W., Markerink-van Ittersun M., and Steinbusch H. Local inhibition of hippocampal nitric oxide synthase does not impair place learning in the morris water escape task in rats. The European Journal of Neuroscience 11 (1999) 223-232
8. Blokland A., Prickaerts J., Honig W., and de Vente J. State-dependent impairment in object recognition after hippocampal nos inhibition. Neuroreport 9 (1998) 4205-4208
9. Böhme G.A., Bon C., Lemaire M., Reibaud M., Piot O., Stutzmann J.M., et al. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. Proceedings of the National Academy of Sciences of the United States of America 90 (1993) 9191-9194
10. Bon C., Böhme G.A., Doble A., Stutzmann J.M., and Blanchard J.C. A role for nitric oxide in long-term potentiation. The European Journal of Neuroscience 4 (1992) 420-424
11. Bon C.L.M., and Garthwaite J. On the role of nitric oxide in hippocampal long-term potentiation. The Journal of Neuroscience 23 (2003) 1941-1948
12. Bredt D.S. Endogenous nitric oxide synthesis: Biological functions and pathophysiology. Free Radical Research 31 (1999) 577-596
13. Chapman P.F., Atkins C.M., Allen M.T., Haley J.E., and Steinmetz J.E. Inhibition of nitric oxide synthesis impairs two different forms of learning. Neuroreport 3 (1992) 567-570
14. Devan B.D., Pistell P.J., Daffin Jr. L.W., Nelson C.M., Duffy K.B., Bowker J.L., et al. Sildenafil citrate attenuates a complex maze impairment induced by intracerebroventricular infusion of the nos inhibitor N omega-nitro-l-arginine methyl ester. European Journal of Pharmacology 563 (2007) 134-140
15. Du W., Weiss H., and Harvey J.A. Associative learning is enhanced by selective neuronal nitric oxide synthase inhibitors and retarded by a nitric oxide donor in the rabbit. Psychopharmacology 150 (2000) 264-271
16. Edwards T.M., and Rickard N.S. New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes. Neuroscience and Biobehavioral Reviews 31 (2007) 413-425
17. 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
18. Hawkins R.D., Son H., and Arancio O. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Progress in Brain Research 118 (1998) 155-172
19. Hawkins R.D., Zhuo M., and Arancio O. Nitric oxide and carbon monoxide as possible retrograde messengers in hippocampal long-term potentiation. In: Takagi H., Toda N., and Hawkins R.D. (Eds). Nitric oxide: Roles in neuronal communication and neurotoxicity (1994), Japan Scientific Societies Press, Tokyo 129-147
20. Hölscher C., Canevari L., and Richter-Levin G. Inhibitors of pla2 and no synthase cooperate in producing amnesia of a spatial task. Neuroreport 6 (1995) 730-732
21. Hölscher C., McGlinchey L., Anwyl R., and Rowan M.J. 7-Nitro indazole, a selective neuronal nitric oxide synthase inhibitor in vivo, impairs spatial learning in the rat. Learning & Memory 2 (1996) 267-278
22. Hölscher C., and Rose S.P. An inhibitor of nitric oxide synthesis prevents memory formation in the chick. Neuroscience Letters 145 (1992) 165-167
23. Hölscher C., and Rose S.P.R. Inhibiting synthesis of the putative retrograde messenger nitric oxide results in amnesia in a passive avoidance task in the chick. Brain Research 619 (1993) 189-194
24. Huang A.M., and Lee E.H. Role of hippocampal nitric oxide in memory retention in rats. Pharmacology, Biochemistry, and Behavior 50 (1995) 327-332
25. Johnson D.M., Baker J.D., and Azorlosa J.L. Acquisition, extinction, and reinstatement of Pavlovian fear conditioning: The roles of the NMDA receptor and nitric oxide. Brain Research 857 (2000) 66-70
26. Katzoff A., Ben-Gedalya T., and Susswein A.J. Nitric oxide is necessary for multiple memory processes after learning that a food is inedible in aplysia. The Journal of Neuroscience 22 (2002) 9581-9594
27. Kirchner L., Weitzdoerfer R., Hoeger H., Url A., Schmidt P., Engelmann M., et al. Impaired cognitive performance in neuronal nitric oxide synthase knockout mice is associated with hippocampal protein derangements. Nitric Oxide: Biology and Chemistry/Official Journal of the Nitric Oxide Society 11 (2004) 316-330
28. Kopf S.R., and Baratti C.M. Enhancement of the post-training cholinergic tone antagonizes the impairment of retention induced by a nitric oxide synthase inhibitor in mice. Neurobiology of Learning and Memory 65 (1996) 207-212
29. Kopf S.R., Benton R.S., Kalfin R., Giovannini M.G., and Pepeu G. NO synthesis inhibition decreases cortical ACh release and impairs retention of a conditioned response. Brain Research 894 (2001) 141-144
30. Koylu E.O., Kanit L., Taskiran D., Dagci T., Balkan B., and Pogun S. Effects of nitric oxide synthase inhibition on spatial discrimination learning and central DA2 and mACh receptors. Pharmacology, Biochemistry, and Behavior 81 (2005) 32-40
31. Majlessi N., Kadkhodaee M., Parviz M., and Naghdi N. Serotonin depletion in rat hippocampus attenuates l-NAME-induced spatial learning deficits. Brain Research 963 (2003) 244-251
32. Majlessi N., and Naghdi N. Impaired spatial learning in the Morris water maze induced by serotonin reuptake inhibitors in rats. Behavioural Pharmacology 13 (2002) 237-242
33. Malen P.L., and Chapman P.F. Nitric oxide facilitates long-term potentiation, but not long-term depression. The Journal of Neuroscience 17 (1997) 2645-2651
34. Matsumoto Y., Unoki S., Aonuma H., and Mizunami M. Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory. Learning & Memory 13 (2006) 35-44
35. Mogensen J., Wörtwein G., Hasman A., Nielsen P., and Wang Q. Functional and neurochemical profile of place learning after l-nitro-arginine in the rat. Neurobiology of Learning and Memory 63 (1995) 54-65
36. Morris R.G.M. Synaptic plasticity and learning: Selective impairment of learning and blockage of long-term potentiation in vivo by N-methyl-d-aspartate receptor antagonist AP5. The Journal of Neuroscience 9 (1989) 3040-3057
37. Morris R. Theories of hippocampal function. In: Morris R., Anderson P., Bliss T., Amaral D., and O'Keefe J. (Eds). The hippocampus book (2007), Oxford University Press, New York 581-713
38. Müller U. Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16 (1996) 541-549
39. Noda Y., Yamada K., and Nabeshima T. Role of nitric oxide in the effect of aging on spatial memory in rats. Behavioural Brain Research 83 (1997) 153-158
40. O'Dell T.J., Hawkins R.D., Kandel E.R., and Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: Evidence for nitric oxide as a possible early retrograde messenger. Proceedings of the National Academy of Sciences of the United States of America 88 (1991) 11285-11289
41. Ohno M., Yamamoto T., and Watanabe S. Deficits in working memory following inhibition of hippocampal nitric oxide synthesis in the rat. Brain Research 632 (1993) 36-40
42. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 2nd ed. (1986), Academic Press, Orlando
43. Pitsikas N. Effects of scopolamine and l-NAME on rats' performance in the object location test. Behavioural Brain Research 179 (2007) 294-298
44. Prendergast M.A., Buccafusco J.J., and Terry Jr. A.V. Nitric oxide synthase inhibition impairs spatial navigation learning and induces conditioned taste aversion. Pharmacology, Biochemistry, and Behavior 57 (1997) 347-352
45. Rickard N.S., and Gibbs M.E. Effects of nitric oxide inhibition on avoidance learning in the chick are lateralized and localized. Neurobiology of Learning and Memory 79 (2003) 252-256
46. Rickard N.S., and Gibbs M.E. Hemispheric dissociation of the involvement of NOS isoforms in memory for discriminated avoidance in the chick. Learning & Memory 10 (2003) 314-318
47. Rickard N.S., Gibbs M.E., and Ng K.T. Inhibition of the endothelial isoform of nitric oxide synthase impairs long-term memory formation in the chick. Learning & Memory 6 (1999) 458-466
48. Samama B., and Boehm N. Inhibition of nitric oxide synthase impairs early olfactory associative learning in newborn rats. Neurobiology of Learning and Memory 71 (1999) 219-231
49. Schmidt H.H.H.W., Hofmann H., Ogilvie P., Sennefelder H., and Weinberg R.J. Biochemistry and regulation of nitric oxide synthase. In: Takagi H., Toda N., and Hawkins R.D. (Eds). Nitric oxide: Roles in neuronal communication and neurotoxicity (1994), Japan Scientific Societies Press, Tokyo 3-18
50. Segieth J., Pearce B., Fowler L., and Whitton P.S. Regulatory role of nitric oxide over hippocampal 5-HT release in vivo. Naunyn-Schmiedeberg's Archives of Pharmacology 363 (2001) 302-306
51. Shen Y., Specht S.M., De Saint Ghislain I., and Li R. The hippocampus: A biological model for studying learning and memory. Progress in Neurobiology 44 (1994) 485-496
52. Sullivan B.M., Wong S., and Schuman E.M. Modification of hippocampal synaptic proteins by nitric oxide-stimulated ADP ribosylation. Learning & Memory 3 (1997) 414-424
53. Tan S.E. Roles of hippocampal nitric oxide and calcium/calmodulin-dependent protein kinase II in inhibitory avoidance learning in rats. Behavioural Pharmacology 18 (2007) 29-38
54. Teyke T. Nitric oxide, but not serotonin, is involved in acquisition of food-attraction conditioning in the snail Helix pomatia. Neuroscience Letters 206 (1996) 29-32
55. Tobin J.R., Gorman L.K., Baxter M.G., and Traystman R.J. Nitric oxide synthase inhibition does not impair visual or spatial discrimination learning. Brain Research 694 (1995) 177-182
56. Wegener G., Volke V., and Rosenberg R. Endogenous nitric oxide decreases hippocampal levels of serotonin and dopamine in vivo. British Journal of Pharmacology 130 (2000) 575-580
57. Yamada K., Noda Y., Nakayama S., Komori Y., Sugihara H., Hasegawa T., et al. Role of nitric oxide in learning and memory and in monoamine metabolism in the rat brain. British Journal of Pharmacology 115 (1995) 852-858
58. Yildirim M., and Marangoz C. Effects of nitric oxide on passive avoidance learning in rats. The International Journal of Neuroscience 114 (2004) 597-606
59. Yildiz Akar F., 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
60. Yun H.Y., Dawson V.L., and Dawson T.M. Glutamate-stimulated calcium activation of Ras/Erk pathway mediated by nitric oxide. Diabetes Research and Clinical Practice 45 (1999) 113-115
61. Zhuo M., Laitinen J.T., Li X.C., and Hawkins R.D. On the respective roles of nitric oxide and carbon monoxide in long-term potentiation in the hippocampus. Learning & Memory 6 (1999) 63-76
62. 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