Inhibition of dorsal hippocampal nitric oxide synthesis potentiates ethanol-induced state-dependent memory in mice

Behavioural Brain Research

Volumn 209, Issue 2, 2010, Pages 189-195

  Rezayof, Ameneh ^a   Zare Chahoki, Ameneh ^a   Zarrindast, Mohammad Reza ^b,c,d   Rassouli, Yassaman ^a  

^a Statistics and Computer Science   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c INSTITUTE FOR RESEARCH IN FUNDAMENTAL SCIENCES IPM   (Iran)

^d INSTITUTE FOR COGNITIVE SCIENCE STUDIES   (Iran)

Author keywords

ETOH; l Arginine; l NAME; Mouse; Passive avoidance learning

Indexed keywords

ALCOHOL; ARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

AMNESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL MOUSE; HIPPOCAMPUS; LOCOMOTION; MALE; MEMORY; MEMORY DISORDER; MICROINJECTION; MOUSE; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; STATE DEPENDENT MEMORY; SYNTHESIS;

ANALYSIS OF VARIANCE; ANIMALS; ARGININE; AVOIDANCE LEARNING; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ETHANOL; HIPPOCAMPUS; MALE; MEMORY; MICE; MICROINJECTIONS; MOTOR ACTIVITY; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; REACTION TIME;

EID: 77649238813     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.01.027     Document Type: Article

References (72)

1. Goodwin D.W. Alcohol amnesia. Addiction 90 (1995) 315-317
2. Hartzler B., and Fromme K. Fragmentary and en bloc blackouts: similarity and distinction among episodes of alcohol-induced memory loss. J Stud Alcohol 64 (2003) 547-550
3. White A.M. What happened? Alcohol, memory blackouts, and the brain. Alcohol Res Health 27 (2003) 186-196
4. Weitemier A.Z., and Ryabinin A.E. Alcohol-induced memory impairment in trace fear conditioning: a hippocampus-specific effect. Hippocampus 13 (2003) 305-315
5. Matthews D.B., and Silvers J.R. The use of acute ethanol administration as a tool to investigate multiple memory systems. Neurobiol Learn Mem 82 (2004) 299-308
6. Gold P.E. The many faces of amnesia. Learn Mem 13 (2006) 506-514
7. White A.M., and Swartzwelder H.S. Hippocampal function during adolescence: a uniqe target of ethanol effects. Ann N Y Acad Sci 1021 (2004) 206-220
8. Fujii S., Yamazaki Y., Sugihara T., and Wakabayashi I. Acute and chronic ethanol exposure differentially affect induction of hippocampal LTP. Brain Res 1211 (2008) 13-21
9. Hendricson A.W., Thomas M.P., Lippmann M.J., and Morrisett R.A. Suppression of L-type voltage-gated calcium channel-dependent synaptic plasticity by ethanol: analysis of miniature synaptic currents and dendritic calcium transients. J Pharmacol Exp Ther 307 (2003) 550-558
10. Silvers J.M., Tokunaga S., Berry R.B., White A.M., and Matthews D.B. Impairments in spatial learning and memory: ethanol, allopregnanolone, and the hippocampus. Brain Res Rev 43 (2003) 275-284
11. Costa E.T., Ferreira V.M., and 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
12. Contestabile A. Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells. Progr Neurobiol 84 (2008) 317-328
13. Feil R., and Kleppisch T. NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol. 184 (2008) 529-560
14. Pepicelli O., Raiteri M., and Fedele E. The NOS/sGC pathway in the rat central nervous system: a microdialysis overview. Neurochem Int 45 (2004) 787-797
15. Wu G., and Morris Jr. S.M. Arginine metabolism: nitric oxide and beyond. Biochem J 336 (1998) 1-17
16. Hara S., Mukai T., Kurosaki K., Mizukami H., Kuriiwa F., and Endo T. Different response to exogenous l-arginine in nitric oxide production between hippocampus and striatum of conscious rats: a microdialysis study. Neurosci Lett 366 (2004) 302-307
17. Hemish J., Nakaya N., Mittal V., and Enikolopov G. Nitric oxide activates diverse signaling pathways to regulate gene expression. J Biol Chem 278 (2003) 42321-42329
18. Domek-Łopacińska K., and Strosznajder J.B. Cyclic GMP metabolism and its role in brain physiology. J Physiol Pharmacol 56 (2005) 15-34
19. Christopherson K.S., Hillier B.J., Lim W.A., and Bredt D.S. PSD-95 assembles a ternary complex with the N-methyl-d-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 274 (1999) 27467-27473
20. Bowyer J.F., Clausing P., Gough B., Slikker Jr. W., and Holson R.R. Nitric oxide regulation of methamphetamine-induced dopamine release in caudate putamen. Brain Res 699 (1995) 62-70
21. Sandor N.T., Brassai A., Puskas A., and Lendvai B. Role of nitric oxide in modulating neurotransmitter release from rat striatum. Brain Res Bull 36 (1995) 483-486
22. Getting S.J., Segieth J., Ahmad S., Biggs C.S., and Whitton P.S. Biphasic modulation of GABA release by nitric oxide in the hippocampus of freely moving rats in vivo. Brain Res 717 (1996) 196-199
23. Ledo A., Frade J., Barbosa R.M., and Laranjinha J. Nitric oxide in brain: diffusion, targets and concentration dynamics in hippocampal subregions. Mol Aspects Med 25 (2004) 75-89
24. Kleppisch T., and Feil R. cGMP signalling in the mammalian brain: role in synaptic plasticity and behaviour. Handb Exp Pharmacol 191 (2009) 549-579
25. Holscher C. Nitrix oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 20 (1997) 298-303
26. Feil R., and Kleppisch T. NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 184 (2008) 529-560
27. Llansola M., Hernandez-Viadel M., Erceg S., Montoliu C., and Felipo V. Increasing the function of the glutamate-nitric oxide-cyclic guanosine monophosphate pathway increases the ability to learn a Y-maze task. J Neurosci Res 87 (2009) 2351-2355
28. Piedrafita B., Cauli O., Montoliu C., and Felipo V. The function of the glutamate-nitric oxide-cGMP pathway in brain in vivo and learning ability decrease in parallel in mature compared with young rats. Learn Mem 14 (2007) 248-254
29. Shulz D.E., Sosnik R., Ego V., Haidarliu S., and Ahissar E. A neuronal analogue of state-dependent learning. Nature 403 (2000) 549-553
30. Rezayof A., Motevasseli T., Rassouli Y., and Zarrindast M.R. Dorsal hippocampal dopamine receptors are involved in mediating ethanol state-dependent learning. Life Sci 80 (2007) 285-292
31. Zarrindast M.R., Bananej M., Khalilzadeh A., Fazli-Tabaei S., Haeri-Rohani A., and Rezayof A. Influence of intracerebroventricular administration of dopaminergic drugs on morphine state-dependent memory in the step-down passive avoidance test. Neurobiol Learn Mem 86 (2006) 286-292
32. Zarrindast M.R., Jafari-Sabet M., Rezayat M., Djahanguiri B., and Rezayof A. Involvement of NMDA receptors in morphine state-dependent learning in mice. Int J Neurosci 116 (2006) 1-13
33. Nakagawa Y., and Iwasaki T. Involvement of benzodiazepine/GABA-A receptor complex in ethanol-induced state-dependent learning in rats. Brain Res 686 (1995) 70-76
34. Nakagawa Y., and Iwasaki T. EtOH-induced state-dependent learning is mediated by 5-hydroxytryptamine3 receptors but not by N-methyl-d-aspartate receptor complex. Brain Res 706 (1996) 227-232
35. Rezayof A., Alijanpour S., Zarrindast M.R., and Rassouli Y. Ethanol state-dependent memory: Involvement of dorsal hippocampal muscarinic and nicotinic receptors. Neurobiol Learn Mem 89 (2008) 441-447
36. Rezayof A., Sharifi Kh, Zarrindast M.R., and Rassouli Y. Modulation of ethanol state-dependent learning by dorsal hippocampal NMDA receptors in mice. Alcohol 42 (2008) 667-674
37. 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. Pharmacol Biochem Behav 81 (2005) 32-40
38. Edwards T.M., and Rickard N.S. New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes. Neurosci Biobehav Rev 31 (2006) 413-425
39. Jellestard F.K., and Bakke H.K. Passive avoidance after ibotenic acid and radio frequency lesions in the rat. 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. Paxinos G., and Franklin K.B.J. The mouse brain in stereotaxic coordinates. 2nd ed. (2001), Academic Press, New York
42. Roohbakhsh A., Hajizadeh Moghaddam A., Massoudi R., and Zarrindast M.R. Role of dorsal hippocampal cannabinoid receptors and nitric oxide in anxiety like behaviours in rats using the elevated plus-maze test. Clin Exp Pharmacol Physiol 34 (2007) 223-229
43. Colpaert F.C. Amnesic trace locked into the benzodiazepine state of memory. Psychopharmacology 102 (1990) 28-36
44. Carlezone J.R., Mendrek A., and Wise R.A. MK-801 disrupts the expression but not the development of bromocriptine sensitization: a state-dependency interpretation. Synapse 20 (1995) 1-9
45. Lowe G. State-dependent learning effects with a combination of alcohol and nicotine. Psychopharmacology (Berl) 89 (1986) 105-107
46. Duka T., Weissenborn R., and Dienes Z. State-dependent effects of alcohol on recollective experience, familiarity and awareness of memories. Psychopharmacology (Berl) 153 (2001) 295-306
47. Khajehpour L., Rezayof A., and Zarrindast M.R. Involvement of dorsal hippocampal nicotinic receptors in the effect of morphine on memory retrieval in passive avoidance task. Eur J Pharmacol 584 (2008) 343-351
48. White A.M., Matthews D.B., and Best P.J. Ethanol, memory, and hippocampal function: a review of recent findings. Hippocampus 10 (2000) 88-93
49. 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
50. 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
51. Naassila M., Ledent C., and Daoust M. Low ethanol sensitivity and increased ethanol consumption in mice lacking adenosine A2A receptors. J Neurosci 22 (2002) 10487-10493
52. Maas J.W., Vogt S.K., Chan G.C., Pineda V.V., Storm D.R., and Muglia L.J. Calcium-stimulated adenylyl cyclases are critical modulators of neuronal ethanol sensitivity. J Neurosci 25 (2005) 4118-4126
53. Adams M.L., Meyer E.R., Sewing B.N., and Cicero T.J. Effects of nitric oxide-related agents on alcohol narcosis. Alcohol Clin Exp Res 18 (1994) 969-975
54. Ferreira V.M.M., Valenzuela C.F., and Morato G.S. Role of nitric oxide-dependent pathways in ethanol-induced anxiolytic effects in rats. Alcohol Clin Exp Res 23 (1999) 1898-1904
55. Rossetti Z.L., and Crespi F. Inhibition of nitric oxide release in vivo by ethanol. Alcohol Clin Exp Res 28 11 (2004 Nov) 1746-1751
56. Wazlawik E., and Morato G.S. Influence of drugs acting on nitric oxide-dependent pathways on ethanol tolerance in rats. Psychopharmacology (Berl) 170 (2003) 343-350
57. 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
58. Deng X.S., and Deitrich R.A. Ethanol metabolism and effects: nitric oxide and its interaction. Curr Clin Pharmacol 2 (2007) 145-153
59. Syapin P.J. Alcohol and nitric oxide production by cells of the brain. Alcohol 16 (1998) 159-165
60. Guix F.X., Uribesalgo I., Coma M., and Munoz F.J. The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76 (2005) 126-152
61. Hendricson A.W., Miao C.L., Lippmann M.J., and Morrisett R.A. Ifenprodil and ethanol enhance NMDA receptor-dependent long-term depression. J Pharmacol Exp Ther 301 (2002) 938-944
62. Hendricson A.W., Sibbald J.R., and Morrisett R.A. Ethanol alters the frequency, amplitude, and decay kinetics of Sr2+-supported, asynchronous NMDAR mEPSCs in rat hippocampal slices. J Neurophysiol 91 (2004) 2568-2577
63. Krystal J.H., Petrakis I.L., Limoncelli D., Webb E., Gueorgueva R., D'Souza1 D.C., et al. Altered NMDA glutamate receptor antagonist response in recovering ethanol-dependent patients. Neuropsychopharmacology 28 (2003) 2020-2028
64. Baratti S.R., and Kopf A. A nitric oxide synthase inhibitor impairs memory storage in mice. Neurobiol Learn Mem 65 (1996) 197-201
65. Telegdy G., and Kokavszky R. The role of nitric oxide in passive avoidance learning. Neuropharmacology 36 (1997) 1583-1587
66. 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
67. Majlessi N., Choopani S., Bozorgmehr T., and Azizi Z. Involvement of hippocampal nitric oxide in spatial learning in the rat. Neurobiol Learn Mem 90 (2008) 413-419
68. 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
69. 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 Res 894 (2001) 141-144
70. Rezayof A., Darbandi N., and Zarrindast M.R. Nicotinic acetylcholine receptors of the ventral tegmental area are involved in mediating morphine-state-dependent learning. Neurobiol Learn Mem 90 (2008) 255-260
71. Ahmadi S., Zarrindast M.R., Nouri M., Haeri-Rohani A., and Rezayof A. N-Methyl-D-aspartate receptors in the ventral tegmental area are involved in retrieval of inhibitory avoidance memory by nicotine. Neurobiol Learn Mem 88 (2007) 352-358
72. 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. Neurobiol Learn Mem 65 (1996) 207-212