Influence of nitric oxide on morphine-induced amnesia and interactions with dopaminergic receptor agents

Physiology and Behavior

Volumn 88, Issue 1-2, 2006, Pages 124-131

  Rezayof, Ameneh ^a   Amini, Rana ^a   Rassouli, Yassaman ^a   Zarrindast, Mohammad Reza ^b,c,d  

^a UNIVERSITY OF TEHRAN   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c INSTITUTE FOR STUDIES IN THEORETICAL PHYSICS AND MATHEMATICS IPM   (Iran)

^d Institute for Cognitive Science Studies   (Iran)

Author keywords

Dopaminergic agents; l Arginine; l NAME; Morphine; Mouse; Passive avoidance learning

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; APOMORPHINE; ARGININE; DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR AFFECTING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; MORPHINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; SULPIRIDE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; LEARNING; MALE; MEMORY; MEMORY DISORDER; MOUSE; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; TASK PERFORMANCE;

EID: 33646950302     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2006.03.017     Document Type: Article

References (82)

1. Gallagher M., Rapp P.R., and Fanelli R.J. Opiate antagonist facilitation of time-dependent memory processes: dependence upon intact norepinephrine function. Brain Res 347 (1985) 284-290
2. Canli T., Cook R.G., and Miczek K.A. Opiate antagonists enhance the working memory of rats in the radial maze. Pharmacol Biochem Behav 36 (1990) 521-525
3. Braida D., Gori E., and Sala M. Relationship between morphine and etonitazene-induced working memory impairment and analgesia. Eur J Pharmacol 271 (1994) 497-504
4. Bodnar R.J., and Klein G.E. Endogenous opiates and behavior: 2003. Peptides 25 (2004) 2205-2256
5. Nishimura M., Shiigi Y., and Kaneto H. State dependent and/or direct memory retrieval by morphine in mice. Psychopharmacology 100 (1990) 27-30
6. Ragozzino M.E., and Gold P.E. Task-dependent effects of intra-amygdala morphine injections: attenuation by intra-amygdala glucose injections. J Neurosci 14 (1994) 7478-7485
7. Homayoun H., Khavandgar S., and Zarrindast M.R. Morphine state-dependent learning: interactions with alpha2-adrenoceptors and acute stress. Behav Pharmacol 14 (2003) 41-48
8. Izquierdo I. Effect of naloxone and morphine on various forms of memory in the rat: possible role of engogenous opiate mechanisms in memory consolidation. Psychopharmacology 66 (1979) 199-203
9. Spain J.W., and Newsom G.C. Chronic opioids impair acquisition of both radial maze and Y-maze choice escape. Psychopharmacology 105 (1991) 101-106
10. Sala M., Braida D., Leone M.P., Calcaterra P., Frattola D., and Gori E. Chronic morphine affects working memory during treatment and withdrawal in rats: possible residual long-term impairment. Behav Pharmacol 5 (1994) 570-580
11. Zarrindast M.R., Jafari M.R., Shafaghi B., and Djahanguiri B. Influence of potassium channel modulators on morphine state-dependent memory of passive avoidance. Behav Pharmacol 15 (2004) 103-110
12. Zarrindast M.R., and Rezayof A. Morphine state-dependent learning: sensitization and interactions with dopamine receptors. Eur J Pharmacol 497 (2004) 197-204
13. Jafari-Sabet M., Zarrindast M.R., Rezayat M., Rezayof A., and Djahangiri B. The influence of NMDA receptor agonist and antagonist on morphine state-dependent memory of passive avoidance in mice. Life Sci 78 (2005) 157-163
14. White N.M. Addictive drugs as reinforces: multiple partial actions on memory systems. Addiction 91 (1996) 921-949
15. McBride W.J., Murphy J.M., and Ikemoto S. Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav Brain Res 101 (1999) 129-152
16. Sigala S., Missale C., and Spano P. Opposite effects of dopamine D2 and D3 receptors on learning and memory in the rat. Eur J Pharmacol 336 (1997) 107-112
17. Tzschentke T.M., and Schmidt W.J. Interactions of MK-801 and GYKI 52466 with morphine and amphetamine in place preference conditioning and behavioural sensitization. Behav Brain Res 84 (1997) 99-107
18. Beninger R.J., and Miller R. Dopamine D1-like receptors and reward-related incentive learning. Neurosci Biobehav Rev 22 (1998) 335-345
19. Adriani W., Felici A., Sargolini F., Roullet P., Usiello A., Oliverio A., et al. N-Methyl-d-aspartate and dopamine receptor involvement in the modulation of locomotor activity and memory processes. Exp Brain Res 123 (1998) 52-59
20. Cai Z., Xiao F., Lee B., Paul I.A., and Rhodes P.G. Prenatal hypoxia-ischemia alters expression and activity of nitric oxide synthase in the young rat brain and causes learning deficits. Brain Res Bull 49 (1999) 359-365
21. Hawkins R.D., Son H., and Arancio O. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118 (1998) 155-172
22. Prast H., and Philippu A. Nitric oxide as modulator of neuronal function. Prog Neurobiol 64 (2001) 51-68
23. Kolesnikov Y.A., Pick C.G., and Pasternak G.W. NG-Nitro-l-arginine prevents morphine tolerance. Eur J Pharmacol 221 (1992) 399-400
24. Xu X., Boshoven W., Lombardo B., and Spranger J. Comparison of the amnestic effects of NMDA receptor antagonist MK-801 and nitric oxide synthase inhibitors: l-NAME and l-NOARG in goldfish. Behav Neurosci 112 (1998) 892-899
25. Kivastik T., Rutkauskaite J., and Zharkovsky A. Nitric oxide synthesis inhibition attenuates morphine-induced place preference. Pharmacol Biochem Behav 53 (1996) 1013-1015
26. Biala G., and Langwinski R. Rewarding properties of some drugs studied by place preference conditioning. Pol J Pharmacol 48 (1996) 425-430
27. Zarrindast M.R., Karami M., Sepehri H., and Sahraei H. Influence of nitric oxide on morphine-induced conditioned place preference in the rat central amygdala. Eur J Pharmacol 453 (2002) 81-89
28. Gholami A., Haeri-Rohani A., Sahraie H., and Zarrindast M.R. Nitric oxide mediation of morphine-induced place preference in the nucleus accumbens of rat. Eur J Pharmacol 449 (2002) 269-277
29. Karami M., Zarrindast M.R., Sepehri H., and Sahraie H. Sulpiride injections into the medial septum reverse the influence of intra-medial septum injection of l-arginine on expression of place conditioning-induced by morphine in rats. Brain Res 976 (2003) 30-40
30. Cuellar B., Fernandez A.P., Lizasoain I., Moro M.A., Lorenzo P., Bentura M.L., et al. Up-regulation of neuronal NO synthase immunoreactivity in opiate dependence and withdrawal. Psychopharmacology 148 (2000) 66-73
31. Lysle D.T., and How T. Endogenous opioids regulate the expression of inducible nitric oxide synthase by splenocytes. J Pharmacol Exp Ther 288 (1999) 502-508
32. O'Dell T., Huang P.L., Dawson T.M., Dinerman J.L., Snyder S.H., Kandel E.R., et al. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265 (1994) 542-546
33. Kantor D.B., Lanzrien M., Stary J.S., Sandoval G.M., Smith W.B., Sullivan B.M., et al. A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science 274 (1996) 1744-1748
34. Wilson R.I., Yanovsky J., Godecke A., Stevens D.R., Schrader J., and Haas H.L. Endothelial nitric oxide synthase and LTP. Nature 386 (1997) 338
35. Fujiyama F., and Masuko S. 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
36. Hidaka S., and Totterdell S. 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
37. Hiramatsu M., Sasaki M., and Kameyama T. Effects of dynorphine A-(1-13) on carbon monoxide-induced delayed amnesia in mice studied in step-down type passive avoidance task. Eur J Pharmacol 282 (1995) 185-191
38. Khavandgar S., Homayoun H., Torkaman-Boutorabi A., and Zarrindast M.R. The effects of adenosine receptor agonists and antagonists on morphine state-dependent memory of passive avoidance. Neurobiol Learn Mem 78 (2002) 390-405
39. Jellestad F.K., and Bakke H.K. Passive avoidance after ibotenic acid and radio frequency lesions in the rat amygdala. Physiol Behav 34 (1985) 299-305
40. Izquierdo I., Medina J.H., Vianna M.R.M., Izquierdo L.A., and Barros D.M. Separate mechanisms for short- and long-term memory. Behav Brain Res 103 (1999) 1-11
41. Gallagher M., and Kapp B.S. Manipulation of opiate activity in the amygdala alters memory processes. Life Sci 23 (1978) 1973-1977
42. Bruins Slot L.A., and Colpaert F.C. Opiates states of memory: receptor mechanisms. J Neurosci 19 (1999) 10520-10529
43. Bruins Slot L.A., and Colpaert F.C. Recall rendered dependent on an opiate state. Behav Neurosci 113 (1999) 337-344
44. Guarna M., Ghelardini C., Galeotti N., Bartolini A., Noli L., Neri C., et al. Effects of endogenous morphine deprivation on memory retention of passive avoidance learning in mice. Int J Neuropsychopharmacol 7 (2004) 311-319
45. Itoh J., Ukai M., and Kameyama T. Dynorphin A-(1-13) potently improves the impairment of spontaneous alternation performance induced by the mu-selective opioid receptor agonist DAMGO in mice. J Pharmacol Exp Ther 269 (1994) 15-21
46. Ukai M., Takada A., Sasaki Y., and Kameyama T. Stimulation of delta1- and delta2-opioid receptors produces amnesia in mice. Eur J Pharmacol 29 (1997) 1-6
47. Galeotti N., Ghelardini C., and Bartolini A. Differential prevention of morphine amnesia by antisense oligodeoxynucleotides directed against various Gi-protein alpha subunits. Br J Pharmacol 133 (2001) 267-274
48. Law P.Y., Wong Y.H., and Loh H.H. Mutational analysis of the structure and function of opioid receptors. Biopolymers 51 (1999) 440-455
49. Law P.Y., Wong Y.H., and Loh H.H. Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40 (2000) 389-430
50. Wang J.H., Ko G.Y., and Kelly P.T. Cellular and molecular bases of memory: synaptic and neuronal plasticity. J Clin Neurophysiol 14 (19971) 264-293
51. Zorumski C.F., and Izumi Y. Modulation of LTP induction by NMDA receptor activation and nitric oxide release. Prog Brain Res 118 (1998) 173-182
52. Yanagihara D., and Kondo I. Nitric oxide plays a key role in adaptive control of locomotion in cat. Proc Natl Acad Sci U S A 93 (1996) 13292-13297
53. Qiang M., Chen Y.C., Wang R., Wu F.M., and Qiao J.T. 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
54. Telegdy G., and Kokavszky R. The role of nitric oxide in passive avoidance learning. Neuropharmacology 36 (1997) 1583-1587
55. Kendrick K.M., Guevara-Guzman R., Zorrilla J., Hinton M.R., Broad K.D., Mimmack M., et al. Formation of olfactory memories mediated by nitric oxide. Nature 388 (1997) 670-674
56. Holscher 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. Learn Mem 2 (1996) 267-278
57. Okere C.O., Kaba H., and Higuchi T. Formation of an olfactory recognition memory in mice: reassessment of the role of nitric oxide. Neuroscience 71 (1996) 349-354
58. 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
59. 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. Neurobiol Learn Mem 63 (1995) 113-115
60. West A.R., and Galloway M.P. Inhibition of glutamate reuptake potentiates endogenous nitric oxide-facilitated dopamine efflux in the rat striatum: an in vivo microdialysis study. Neurosci Lett 230 (1997) 21-24
61. Schulman H. Nitric oxide: a spatial second messenger. Mol Psychiatry 2 (1997) 296-299
62. Steckler T., Oliveira A.F., Van Dyck C., Van Craenendonck H., Mateus A.M., Langlois X., et al. Metabotropic glutamate receptor 1 blockade impairs acquisition and retention in a spatial Water maze task. Behav Brain Res 164 (2005) 52-60
63. Antzoulatos E.G., and Byrne J.H. Learning insights transmitted by glutamate. Trends Neurosci 27 (2004) 555-560
64. Zhao M.G., Toyoda H., Lee Y.S., Wu L.J., Ko S.W., Zhang X.H., et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47 (2005) 859-872
65. Shohamy D., Myers C.E., Grossman S., Sage J., and Gluck M.A. The role of dopamine in cognitive sequence learning: evidence from Parkinson's disease. Behav Brain Res 156 (2005) 191-199
66. Jay T.M. Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 69 (2003) 375-390
67. Baratti C.M., and Kopf S.R. A nitric oxide synthase inhibitor impairs memory storage in mice. Neurobiol Learn Mem 65 (1996) 197-201
68. Calixto A.V., Vandresen N., de Nucci G., Moreno H., and Faria M.S. Nitric oxide may underlie learned fear in the elevated T-maze. Brain Res Bull 55 (2001) 37-42
69. Khavandgar S., Homayoun H., and Zarrindast M.R. The effect of l-NAME and l-arginine on impairment of memory formation and state dependent learning induced by morphine in mice. Psychopharmacology 167 (2003) 291-296
70. Estall L.B., Grant S.J., and Cicala J.A. Inhibition of nitric oxide (NO) production selectively impairs learning and memory in the rat. Pharmacol Biochem Behav 46 (1993) 959-962
71. Ohno M., Yamamoto T., and Watanabe S. Deficits in working memory following inhibition of hippocampal nitric oxide synthesis in the rat. Brain Res 632 (1993) 36-40
72. Suzuki Y., Ikari H., Hayashi T., and Iguchi A. Central administration of a nitric oxide synthase inhibitor impairs spatial memory in spontaneous hypertensive rats. Neurosci Lett 207 (1996) 105-108
73. Prendergast M.A., Buccafusco J.J., and Terry A.V. Nitric oxide synthase inhibition impairs spatial navigation learning and induces conditioned taste aversion. Pharmacol Biochem Behav 57 (1997) 347-352
74. Cai Z., Hutchins J.B., and Rhodes P.G. Intrauterine hypoxia-ischemia alters nitric oxide synthase expression and activity in fetal and neonatal rat brains. Dev Brain Res 109 (1998) 265-269
75. Myslivecek J., Hassmannova J., Barcal J., Safanda J., and Zalud V. Inhibitory learning and memory in newborn rats influenced by nitric oxide. Neurosci 71 (1996) 299-312
76. Wilkerson A., and Levin E.D. Ventral hippocampal dopamine D1 and D2 systems and spatial working memory in rats. Neuroscience 89 (1999) 743-749
77. Seamans J.K., Floresco S.B., and Phillips A.G. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J Neurosci 18 (1998) 1613-1621
78. Izquierdo I., Medina J.H., Izquierdo L.A., Barros D.M., de Souza M.M., and Mello e Souza T. Short- and long-term memory are differentially regulated by monoaminergic systems in the rat brain. Neurobiol Learn Mem 69 (1998) 219-224
79. Rezayof A., Zarrindast M.R., Sahraei H., and Haeri-Rohani A. Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 17 (2003) 415-423
80. Koob G.F. Dopamine, addiction and reward. Semin Neurosci 4 (1992) 139-146
81. Liu Y. Nitric oxide influences dopaminergic processes. Adv Neuroimmunol 6 (1996) 259-264
82. Strasser A., McCarron R.M., Ishii H., Stanimirovic D., and Spatz M. l-Arginine induces dopamine release from the striatum in vivo. NeuroReport 5 (1994) 2298-2300