Effects of nitric oxide synthase inhibition on spatial discrimination learning and central DA2 and mACh receptors

Pharmacology Biochemistry and Behavior

Volumn 81, Issue 1, 2005, Pages 32-40

  Koylu, Ersin O ^a   Kanit, Lutfiye ^a   Taskiran, Dilek ^a   Dagci, Taner ^a   Balkan, Burcu ^a   Pogun, Sakire ^a  

^a EGE UNIVERSITY   (Turkey)

Author keywords

Brain; Place learning; Rat; Receptor regulation; Water maze

Indexed keywords

DOPAMINE 2 RECEPTOR; MUSCARINIC RECEPTOR; N(G) NITROARGININE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; QUINUCLIDINYL BENZILATE; SODIUM CHLORIDE; SPIPERONE; TRITIUM;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CHOLINERGIC SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; ENZYME INHIBITION; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; REGULATORY MECHANISM; SPATIAL DISCRIMINATION; SPATIAL MEMORY;

ANIMALS; DISCRIMINATION LEARNING; ENZYME INHIBITORS; MALE; MAZE LEARNING; NITRIC OXIDE SYNTHASE; NITROARGININE; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D2; RECEPTORS, MUSCARINIC; SPATIAL BEHAVIOR;

RODENTIA;

EID: 19444379213     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2005.02.008     Document Type: Article

References (92)

1. T. Abekawa, T. Ohmori, and T. Koyama Effect of no synthesis inhibition on striatal dopamine release and stereotyped behavior induced by a single administration of methamphetamine Prog Neuropsychopharmacol Biol Psychiatry 21 1997 831 838
2. D.M. Bannerman, P.F. Chapman, P.A. Kelly, S.P. Butcher, and R.G. Morris Inhibition of nitric oxide synthase does not impair spatial learning J Neurosci 14 1994 7404 7414
3. M.G. Baxter, D.J. Bucci, L.K. Gorman, R.G. Wiley, and M. Gallagher Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats Behav Neurosci 109 1995 714 722
4. J. Berger-Sweeney, S. Heckers, M.M. Mesulam, R.G. Wiley, D.A. Lappi, and M. Sharma Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis J Neurosci 14 1994 4507 4519
5. H.J. Bidmon, J. Wu, N. Palomero-Gallagher, E. Oermann, B. Mayer, and A. Schleicher Different nitric oxide synthase inhibitors cause rapid and differential alterations in the ligand-binding capacity of transmitter receptors in the rat cerebral cortex Anat Anz 181 1999 345 351
6. A. Blokland, J. de Vente, J. Prickaerts, W. Honig, M. Markerink-van Ittersum, and H. Steinbusch Local inhibition of hippocampal nitric oxide synthase does not impair place learning in the Morris water escape task in rats Eur J Neurosci 11 1999 223 232
7. G.A. Bohme, C. Bon, M. Lemaire, M. Reibaud, O. Piot, and J.M. Stutzmann Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats Proc Natl Acad Sci U S A 90 1993 9191 9194
8. J.F. Bowyer, P. Clausing, B. Gough, W. Slikker Jr., and R.R. Holson Nitric oxide regulation of methamphetamine-induced dopamine release in caudate/putamen Brain Res 699 1995 62 70
9. R.W. Brown, M.T. Bardo, D.D. Mace, S.B. Phillips, and P.J. Kraemer d-amphetamine facilitation of Morris water task performance is blocked by eticlopride and correlated with increased dopamine synthesis in the prefrontal cortex Behav Brain Res 114 2000 135 143
10. P.F. Chapman, C.M. Atkins, M.T. Allen, J.E. Haley, and J.E. Steinmetz Inhibition of nitric oxide synthesis impairs two different forms of learning NeuroReport 3 1992 567 570
11. S. Demirgoren, and S. Pogun Effects of nitric oxide on Morris Water Maze performance in rats: correlation with cGMP levels L. Packer K.W.A. Wirtz Signaling Mechanisms-From Transcription Factors to Oxidative Stress NATO ASI Series, Series H 1995 Springer-Verlag New York 271 277
12. E. Dere, C. Frisch, M.A. De Souza Silva, A. Godecke, J. Schrader, and J.P. Huston Unaltered radial maze performance and brain acetylcholine of the endothelial nitric oxide synthase knockout mouse Neuroscience 107 2001 561 570
13. E. Elvander, P.A. Schott, J. Sandin, B. Bjelke, J. Kehr, and T. Yoshitake Intraseptal muscarinic ligands and galanin: influence on hippocampal acetylcholine and cognition Neuroscience 126 2004 541 557
14. B.J. Everitt, and T.W. Robbins Central cholinergic systems and cognition Annu Rev Psychol 48 1997 649 684
15. C. Frisch, E. Dere, M.A. Silva, A. Godecke, J. Schrader, and J.P. Huston Superior water maze performance and increase in fear-related behavior in the endothelial nitric oxide synthase-deficient mouse together with monoamine changes in cerebellum and ventral striatum J Neurosci 20 2000 6694 6700
16. F. Fujiyama, and S. Masuko Association of dopaminergic terminals and neurons releasing nitric oxide in the rat striatum: an electron microscopic study using NADPH-diaphorase histochemistry and tyrosine hydroxylase immunohistochemistry Brain Res Bull 40 1996 121 127
17. S.J. Getting, J. Segieth, S. Ahmad, C.S. Biggs, and P.S. Whitton Biphasic modulation of GABA release by nitric oxide in the hippocampus of freely moving rats in vivo Brain Res 717 1996 196 199
18. B. Givens, and M. Sarter Modulation of cognitive processes by transsynaptic activation of the basal forebrain Behav Brain Res 84 1997 1 22
19. S.B. Glickstein, P.R. Hof, and C. Schmauss Mice lacking dopamine D2 and D3 receptors have spatial working memory deficits J Neurosci 22 2002 5619 5629
20. 3H]-dopamine from striatal slices NeuroReport 3 1992 409 412
21. R.D. Hawkins, H. Son, and O. Arancio Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus Prog Brain Res 118 1998 155 172
22. C. Heim, W. Kolasiewicz, T. Kurz, and K.H. Sontag Behavioral alterations after unilateral 6-hydroxydopamine lesions of the striatum. Effect of alpha-tocopherol Pol J Pharmacol 53 2001 435 448
23. S. Hidaka, and S. Totterdell Ultrastructural features of the nitric oxide synthase-containing interneurons in the nucleus accumbens and their relationship with tyrosine hydroxylase-containing terminals J Comp Neurol 431 2001 139 154
24. C. Holscher, L. McGlinchey, R. Anwyl, and M.J. Rowan 7-Nitro indazole, a selective neuronal nitric oxide synthase inhibitor in vivo, impairs spatial learning in the rat Learn Mem 2 1996 267 278
25. E.P. Huang Synaptic plasticity: a role for nitric oxide in LTP Curr Biol 7 1997 R141 R143
26. L. Kanit, D. Taskiran, O.A. Yilmaz, B. Balkan, S. Demirgoren, and J.J. Furedy Sexually dimorphic cognitive style in rats emerges after puberty Brain Res Bull 52 2000 243 248
27. L. Kanit, E.O. Koylu, G. Yararbas, J.J. Furedy, and S. Pogun The effect of nitric oxide synthase inhibition on cognitive ability and strategies employed for place learning in the water maze: sex differences Brain Res Bull 62 2003 151 159
28. T. Kano, M. Shimizu-Sasamata, P.L. Huang, M.A. Moskowitz, and E.H. Lo Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo Neuroscience 86 1998 695 699
29. K.M. Kendrick, R. Guevara-Guzman, J. Zorrilla, M.R. Hinton, K.D. Broad, and M. Mimmack Formation of olfactory memories mediated by nitric oxide Nature 388 1997 670 674
30. J.S. Kim, and E.D. Levin Nicotinic, muscarinic and dopaminergic actions in the ventral hippocampus and the nucleus accumbens: effects on spatial working memory in rats Brain Res 725 1996 231 240
31. J.P. Kiss, E.C. Hennings, G. Zsilla, and E.S. Vizi A possible role of nitric oxide in the regulation of dopamine transporter function in the striatum Neurochem Int 34 1999 345 350
32. A.E. Kline, J.L. Massucci, D.W. Marion, and C.E. Dixon Attenuation of working memory and spatial acquisition deficits after a delayed and chronic bromocriptine treatment regimen in rats subjected to traumatic brain injury by controlled cortical impact J Neurotrauma 19 2002 415 425
33. R.D. Lees, P. Slater, and D.S. SW Nitric oxide does not modulate kainate receptor binding in human brain Neurosci Lett 233 1997 133 136
34. O. Lehmann, F. Bertrand, H. Jeltsch, M. Morer, C. Lazarus, and B. Will 5,7-DHT-induced hippocampal 5-HT depletion attenuates behavioural deficits produced by 192 IgG-saporin lesions of septal cholinergic neurons in the rat Eur J Neurosci 15 2002 1991 2006
35. I. Lena, H. Dh tel, C. Garbay, and V. Dauge Involvement of D2 dopamine receptors in the opposing effects of two CCK-B agonists in a spatial recognition memory task: role of the anterior nucleus accumbens Psychopharmacology (Berlin) 153 2001 170 179
36. E.D. Levin, and J.E. Rose Acute and chronic nicotinic interactions with dopamine systems and working memory performance Ann N Y Acad Sci 757 1995 245 252
37. S. Li, W.K. Cullen, R. Anwyl, and M.J. Rowan Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty Nat Neurosci 6 2003 526 531
38. Y. Liu Nitric oxide influences dopaminergic processes Adv Neuroimmunol 6 1996 259 264
39. 3H]norepinephrine release: I. The role of glutamate J Pharmacol Exp Ther 275 1995 7 13
40. G. Lonart, J. Wang, and K.M. Johnson Nitric oxide induces neurotransmitter release from hippocampal slices Eur J Pharmacol 220 1992 271 272
41. 3H]dopamine release from striatal slices J Neurosci Res 35 1993 192 198
42. A. Mattsson, S.O. Ogren, and L. Olson Facilitation of dopamine-mediated locomotor activity in adult rats following cholinergic denervation Exp Neurol 174 2002 96 108
43. M.K. Meffert, B.A. Premack, and H. Schulman Nitric oxide stimulates Ca(2+)-independent synaptic vesicle release Neuron 12 1994 1235 1244
44. A. Mele, M. Avena, P. Roullet, E. De Leonibus, S. Mandillo, and F. Sargolini Nucleus accumbens dopamine receptors in the consolidation of spatial memory Behav Pharmacol 15 2004 423 431
45. A. Meulemans, J.P. Mothet, A. Schirar, P. Fossier, L. Tauc, and G. Baux A nitric oxide synthase activity is involved in the modulation of acetylcholine release in Aplysia ganglion neurons: a histological, voltammetric and electrophysiological study Neuroscience 69 1995 985 995
46. N. Milivojevic, K. Babic, D. Milatovic, W.D. Dettbarn, D. Sket, and M. Zivin N-tert-butyl-alpha-phenylnitrone, a free radical scavenger with anticholinesterase activity does not improve the cognitive performance of scopolamine-challenged rats Int J Dev Neurosci 19 2001 319 325
47. E. Miyoshi, S. Wietzikoski, M. Camplessei, R. Silveira, R.N. Takahashi, and C. Da Cunha Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions Brain Res Bull 58 2002 41 47
48. Y. Morot Gaudry-Talarmain, N. Moulian, F.A. Meunier, B. Blanchard, D. Angaut-Petit, and L. Faille Nitric oxide and peroxynitrite affect differently acetylcholine release, choline acetyltransferase activity, synthesis, and compartmentation of newly formed acetylcholine in Torpedo marmorata synaptosomes Nitric Oxide 1 1997 330 345
49. R. Morris Developments of a water-maze procedure for studying spatial learning in the rat J Neurosci Methods 11 1984 47 60
50. J.P. Mothet, P. Fossier, A. Schirar, L. Tauc, and G. Baux Opposite effects of nitric oxide on identified inhibitory and excitatory cholinergic synapses of Aplysia californica Physiol Res 45 1996 177 183
51. J.P. Mothet, P. Fossier, L. Tauc, and G. Baux Opposite actions of nitric oxide on cholinergic synapses: which pathways? Proc Natl Acad Sci U S A 93 1996 8721 8726
52. M.R. Mukhtarov, F. Vyskocil, A.K. Urazaev, and E.E. Nikolsky Non-quantal acetylcholine release is increased after nitric oxide synthase inhibition Physiol Res 48 1999 315 317
53. M.R. Mukhtarov, A.K. Urazaev, E.E. Nikolsky, and F. Vyskocil Effect of nitric oxide and NO synthase inhibition on nonquantal acetylcholine release in the rat diaphragm Eur J Neurosci 12 2000 980 986
54. T. Myhrer Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks Brain Res Brain Res Rev 41 2003 268 287
55. J. Myslivecek, J. Hassmannova, J. Barcal, J. Safanda, and V. Zalud Inhibitory learning and memory in newborn rats influenced by nitric oxide Neuroscience 71 1996 299 312
56. C.O. Okere, H. Kaba, and T. Higuchi Formation of an olfactory recognition memory in mice: reassessment of the role of nitric oxide Neuroscience 71 1996 349 354
57. M.G. Packard, and N.M. White Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists Behav Neurosci 105 1991 295 306
58. C.L. Peterson, M.A. Thompson, D. Martin, and J.V. Nadler Modulation of glutamate and aspartate release from slices of hippocampal area CA1 by inhibitors of arachidonic acid metabolism J Neurochem 64 1995 1152 1160
59. S. Pogun, and M.J. Kuhar Regulation of neurotransmitter reuptake by nitric oxide Ann N Y Acad Sci 738 1994 305 315
60. S. Pogun, S. Demirgoren, F.Z. Kutay, and B. Okur Learning induces changes in the central cholinergic system of the rat in a sexually dimorphic pattern Int J Psychophysiol 13 1992 17 23
61. S. Pogun, L. Kanit, and B.E. Okur Learning-induced changes in D2 receptors of rat brain are sexually dimorphic Pharmacol Biochem Behav 43 1992 71 75
62. 3H]dopamine uptake Brain Res 641 1994 83 91
63. 3H-glutamate transport in synaptosomes Synapse 18 1994 21 26
64. H. Prast, and A. Philippu Nitric oxide as modulator of neuronal function Prog Neurobiol 64 2001 51 68
65. M.A. Prendergast, J.J. Buccafusco, and A.V. Terry Jr. Nitric oxide synthase inhibition impairs spatial navigation learning and induces conditioned taste aversion Pharmacol Biochem Behav 57 1997 347 352
66. M. Qiang, Y.C. Chen, R. Wang, F.M. Wu, and J.T. Qiao Nitric oxide is involved in the formation of learning and memory in rats: studies using passive avoidance response and Morris water maze task Behav Pharmacol 8 1997 183 187
67. A. Reif, A. Schmitt, S. Fritzen, S. Chourbaji, C. Bartsch, and A. Urani Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour Eur J Neurosci 20 2004 885 895
68. E. Salemme, S. Diano, P. Maharajan, and V. Maharajan Nitric oxide, a neuronal messenger. Its role in the hippocampus neuronal plasticity Riv Biol 89 1996 87 107
69. C. Sandi, C. Venero, and C. Guaza Decreased spontaneous motor activity and startle response in nitric oxide synthase inhibitor-treated rats Eur J Pharmacol 277 1995 89 97
70. N.T. Sandor, A. Brassai, A. Puskas, and B. Lendvai Role of nitric oxide in modulating neurotransmitter release from rat striatum Brain Res Bull 36 1995 483 486
71. M. Sarter, and J.P. Bruno Cognitive functions of cortical acetylcholine: toward a unifying hypothesis Brain Res Brain Res Rev 23 1997 28 46
72. H. Schulman Nitric oxide: a spatial second messenger Mol Psychiatry 2 1997 296 299
73. S.M. Sequeira, A.F. Ambrosio, J.O. Malva, A.P. Carvalho, and C.M. Carvalho Modulation of glutamate release from rat hippocampal synaptosomes by nitric oxide Nitric Oxide 1 1997 315 329
74. B. Setlow, and J.L. McGaugh D2 dopamine receptor blockade immediately post-training enhances retention in hidden and visible platform versions of the water maze Learn Mem 7 2000 187 191
75. S. Sigala, C. Missale, and P. Spano Opposite effects of dopamine D2 and D3 receptors on learning and memory in the rat Eur J Pharmacol 336 1997 107 112
76. M. Spatz, Y. Yasuma, A. Strasser, N. Kawai, D. Stanimirovic, and R. McCarron Modulation of striatal dopamine release in cerebral ischemia by l-arginine Neurochem Res 20 1995 491 496
77. R. Tatchum-Talom, R. Schulz, J.R. McNeill, and F.H. Khadour Upregulation of neuronal nitric oxide synthase in skeletal muscle by swim training Am J Physiol Heart Circ Physiol 279 2000 H1757 H1766
78. G. Telegdy, and R. Kokavszky The role of nitric oxide in passive avoidance learning Neuropharmacology 36 1997 1583 1587
79. E.M. Torres, T.A. Perry, A. Blockland, L.S. Wilkinson, R.G. Wiley, and D.A. Lappi Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system Neuroscience 63 1994 95 122
80. A.H. Tran, R. Tamura, T. Uwano, T. Kobayashi, M. Katsuki, and G. Matsumoto Altered accumbens neural response to prediction of reward associated with place in dopamine D2 receptor knockout mice Proc Natl Acad Sci U S A 99 2002 8986 8991
81. T.Y. Turner, and M.R. Soliman Effects of zinc on spatial reference memory and brain dopamine (D1) receptor binding kinetics in rats Prog Neuropsychopharmacol Biol Psychiatry 24 2000 1203 1217
82. E.S. Vizi Role of high-affinity receptors and membrane transporters in nonsynaptic communication and drug action in the central nervous system Pharmacol Rev 52 2000 63 89
83. T.J. Walsh, R.M. Kelly, K.D. Dougherty, R.W. Stackman, R.G. Wiley, and C.L. Kutscher Behavioral and neurobiological alterations induced by the immunotoxin 192-IgG-saporin: cholinergic and non-cholinergic effects following i.c.v. injection Brain Res 702 1995 233 245
84. J.H. Wang, G.Y. Ko, and P.T. Kelly Cellular and molecular bases of memory: synaptic and neuronal plasticity J Clin Neurophysiol 14 1997 264 293
85. N.M. White, and M. Viaud Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats Behav Neural Biol 55 1991 255 269
86. N.M. White, M.G. Packard, and J. Seamans Memory enhancement by post-training peripheral administration of low doses of dopamine agonists: possible autoreceptor effect Behav Neural Biol 59 1993 230 241
87. A. Wilkerson, and E.D. Levin Ventral hippocampal dopamine D1 and D2 systems and spatial working memory in rats Neuroscience 89 1999 743 749
88. K. Yamada, M. Hiramatsu, Y. Noda, T. Mamiya, M. Murai, and T. Kameyama Role of nitric oxide and cyclic GMP in the dizocilpine-induced impairment of spontaneous alternation behavior in mice Neuroscience 74 1996 365 374
89. H.I. Yamamura, and S.H. Snyder Muscarinic cholinergic binding in rat brain Proc Natl Acad Sci U S A 71 1974 1725 1729
90. D. Yanagihara, and I. Kondo Nitric oxide plays a key role in adaptive control of locomotion in cat Proc Natl Acad Sci U S A 93 1996 13292 13297
91. S.N. Yang, C.B. Huang, C.H. Yang, M.C. Lai, W.F. Chen, and C.L. Wang Impaired SynGAP expression and long-term spatial learning and memory in hippocampal CA1 area from rats previously exposed to perinatal hypoxia-induced insults: beneficial effects of A68930 Neurosci Lett 371 2004 73 78
92. C.F. Zorumski, and Y. Izumi Modulation of LTP induction by NMDA receptor activation and nitric oxide release Prog Brain Res 118 1998 173 182