Activation of the Nitric-Oxide System in Nucleus Accumbens Inhibits the Nicotine Reversal Effects upon Ethanol-Induced Amnesia

Document Type : Original Articles

Authors

1 Department of Biology, Faculty of Basic Sciences, Islamic Azad University, Lahijan Branch, Lahijan

2 Department of Biology, Faculty of Basic Sciences, Islamic Azad University, Ardabil branch, Ardabil

3 Young Researchers’ Club, Islamic Azad University, Shahr-e-Rey Branch, Tehran, Iran

4 Department of Neuroscience, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences

Abstract

The present study investigated the possible involvement of the nucleus accumbens’ (NAc) nitric oxide system in nicotine's reversal effect upon ethanol-induced amnesia. The hypothesis was tested through ethanol state-dependent memory assessment in adult male Wistar rats. Bilateral chronic cannulae were implanted in the NAc and the animals were trained in a step-through type inhibitory avoidance memory task.  The step-through latency was examined 24 h after animals’ training. The pre-training or pre-test intraperitoneal (i.p.) injection of ethanol (0.9 g/kg) decreased the step-through latency, indicating an amnesic effect of the drug. Meanwhile, the pre-test administration of ethanol (0.6 and 0.9 g/kg) could reverse the pre-training ethanol (0.9 g/kg)-induced amnesia, suggesting a state-dependent effect. Similar to ethanol, the pre-test intra-NAc microinjection of nicotine (0.25 and 0.5 µg/rat) alone or nicotine (0.1, 0.25 and 0.5 µg/mouse, intra-NAc) in combination with an ineffective dose of ethanol (0.3 g/kg) could significantly reverse the (pre-training) ethanol-induced memory impairment. The ethanol (0.9 g/kg)-induced amnesia was similarly prevented following the pre-test intra-NAc administration of a nitric oxide synthase (NOS) inhibitor, L-NAME (0.4 and 0.8 µg/rat). Of note, the co-administration of L-NAME (0.04 and 0.08 µg/rat, intra-NAc) with an ineffective dose of nicotine (0.1 µg/rat, intra- NAc) could significantly potentiate the memory-improving effect of nicotine on ethanol-induced amnesia and resembled the effects of pre-test administration of a higher dose of nicotine. Furthermore, while the pre-test intra-NAc injection of L-NAME impaired the memory retrieval by itself, the pre-test intra-NAc administration of L-arginine, a nitric oxide precursor (0.3 and 0.6 µg/rat, intra-NAc), did not exert any effect either alone or in combination with an effective dose of nicotine (0.5 µg/rat, intra-NAc)  on pre-training ethanol-induced memory impairment. Our findings indicated a possible role of the nucleus accumbens’ nitric oxide system in the improving effects of nicotine on ethanol-induced amnesia and the related state-dependent learning. 

Keywords

References

  1. Bien TH, Burge R. Smoking and drinking: a review of the literature. Int J Addict. 1990;25(12):1429-54.
  2. Batel P, Pessione F, Maitre C, Rueff B. Relationship between alcohol and tobacco dependencies among alcoholics who smoke. Addiction. 1995;90(7):977-80.
  3. Larsson A, Engel JA. Neurochemical and behavioral studies on ethanol and nicotine interactions. Neurosci Biobehav Rev. 2004;27(8):713-20.
  4. Rezayof A, Sharifi K, Zarrindast MR, Rassouli Y. Modulation of ethanol state-dependent learning by dorsal hippocampal NMDA receptors in mice. Alcohol. 2008;42(8):667-74.
  5. Rezayof A, Shirazi-Zand Z, Zarrindast MR, Nayer-Nouri T. Nicotine improves ethanol-induced memory impairment: the role of dorsal hippocampal NMDA receptors. Life Sci. 2010;86(7-8):260-6.
  6. Rezayof A, Zare-Chahoki A, Zarrindast MR, Rassouli Y. Inhibition of dorsal hippocampal nitric oxide synthesis potentiates ethanol-induced state-dependent memory in mice. Behav Brain Res. 2010;209(2):189-95.
  7. Raoufi N, Piri M, Moshfegh A, Shahin MS. Nicotine improves ethanol-induced impairment of memory: possible involvement of nitric oxide in the dorsal hippocampus of mice. Neuroscience. 2012.
  8. Rezayof A, Alijanpour S, Zarrindast MR, Rassouli Y. Ethanol state-dependent memory: involvement of dorsal hippocampal muscarinic and nicotinic receptors. Neurobiol Learn Mem. 2008;89(4):441-7.
  9. Melchior CL, Glasky AJ, Ritzmann RF. A low dose of ethanol impairs working memory in mice in a win-shift foraging paradigm. Alcohol. 1993;10(6):491-3.
  10. Matthews DB, Simson PE, Best PJ. Acute ethanol impairs spatial memory but not stimulus/response memory in the rat. Alcohol Clin Exp Res. 1995;19(4):902-9.
  11. Chin VS, Van Skike CE, Berry RB, Kirk RE, Diaz-Granados J, Matthews DB. Effect of acute ethanol and acute allopregnanolone on spatial memory in adolescent and adult rats. Alcohol. 2011;45(5):473-83.
  12. Berry RB, Matthews DB. Acute ethanol administration selectively impairs spatial memory in C57BL/6J mice. Alcohol. 2004;32(1):9-18.
  13. Nakagawa Y, Iwasaki T. Involvement of benzodiazepine/GABA-A receptor complex in ethanol-induced state-dependent learning in rats. Brain Res. 1995;686(1):70-6.
  14. Nakagawa Y, Iwasaki T. Ethanol-induced state-dependent learning is mediated by 5-hydroxytryptamine3 receptors but not by N-methyl-D-aspartate receptor complex. Brain Res. 1996;706(2):227-32.
  15. Larsson A, Svensson L, Soderpalm B, Engel JA. Role of different nicotinic acetylcholine receptors in mediating behavioral and neurochemical effects of ethanol in mice. Alcohol. 2002;28(3):157-67.
  16. Narahashi T, Aistrup GL, Marszalec W, Nagata K. Neuronal nicotinic acetylcholine receptors: a new target site of ethanol. Neurochem Int. 1999;35(2):131-41.
  17. Lowe G. State-dependent learning effects with a combination of alcohol and nicotine. Psychopharmacology (Berl). 1986;89(1):105-7.
  18. Gould TJ, Collins AC, Wehner JM. Nicotine enhances latent inhibition and ameliorates ethanol-induced deficits in latent inhibition. Nicotine Tob Res. 2001;3(1):17-24.
  19. Gulick D, Gould TJ. Interactive effects of ethanol and nicotine on learning in C57BL/6J mice depend on both dose and duration of treatment. Psychopharmacology (Berl). 2008;196(3):483-95.
  20. Tracy HA, Jr., Wayner MJ, Armstrong DL. Nicotine blocks ethanol and diazepam impairment of air righting and ethanol impairment of maze performance. Alcohol. 1999;18(2-3):123-30.
  21. Dawson DA. Drinking as a risk factor for sustained smoking. Drug Alcohol Depend. 2000;59(3):235-49.
  22. Shim I, Kim HT, Kim YH, Chun BG, Hahm DH, Lee EH, et al. Role of nitric oxide synthase inhibitors and NMDA receptor antagonist in nicotine-induced behavioral sensitization in the rat. Eur J Pharmacol. 2002;443(1-3):119-24.
  23. Sahraei H, Falahi M, Zarrindast MR, Sabetkasaei M, Ghoshooni H, Khalili M. The effects of nitric oxide on the acquisition and expression of nicotine-induced conditioned place preference in mice. Eur J Pharmacol. 2004;503(1-3):81-7.
  24. Schilstrom B, Mameli-Engvall M, Rawal N, Grillner P, Jardemark K, Svensson TH. Nitric oxide is involved in nicotine-induced burst firing of rat ventral tegmental area dopamine neurons. Neuroscience. 2004;125(4):957-64.
  25. Piri M, Zarrindast MR. Nitric oxide in the ventral tegmental area is involved in retrieval of inhibitory avoidance memory by nicotine. Neuroscience. 2011.
  26. Tayfun Uzbay I, Oglesby MW. Nitric oxide and substance dependence. Neurosci Biobehav Rev. 2001;25(1):43-52.
  27. Loh HH, Liu HC, Cavalli A, Yang W, Chen YF, Wei LN. mu Opioid receptor knockout in mice: effects on ligand-induced analgesia and morphine lethality. Brain Res Mol Brain Res. 1998;54(2):321-6.
  28. Martin JL, Itzhak Y. 7-Nitroindazole blocks nicotine-induced conditioned place preference but not LiCl-induced conditioned place aversion. Neuroreport. 2000;11(5):947-9.
  29. Khavandgar S, Homayoun H, Zarrindast MR. The effect of L-NAME and L-arginine on impairment of memory formation and state-dependent learning induced by morphine in mice. Psychopharmacology (Berl). 2003;167(3):291-6.
  30. Qiang M, Chen YC, Wang R, Wu FM, Qiao JT. 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. 1997;8(2-3):183-7.
  31. Telegdy G, Kokavszky R. The role of nitric oxide in passive avoidance learning. Neuropharmacology. 1997;36(11-12):1583-7.
  32. Zarrindast MR, Shendy MM, Ahmadi S. Nitric oxide modulates state dependency induced by lithium in an inhibitory avoidance task in mice. Behav Pharmacol. 2007;18(4):289-95.
  33. Choopani S, Moosavi M, Naghdi N. Involvement of nitric oxide in insulin induced memory improvement. Peptides. 2008;29(6):898-903.
  34. Kendrick KM, Guevara-Guzman R, Zorrilla J, Hinton MR, Broad KD, Mimmack M, et al. Formation of olfactory memories mediated by nitric oxide. Nature. 1997;388(6643):670-4.
  35. Majlessi N, Kadkhodaee M, Parviz M, Naghdi N. Serotonin depletion in rat hippocampus attenuates L-NAME-induced spatial learning deficits. Brain Res. 2003;963(1-2):244-51.
  36. Yamada K, Noda Y, Hasegawa T, Komori Y, Nikai T, Sugihara H, et al. The role of nitric oxide in dizocilpine-induced impairment of spontaneous alternation behavior in mice. J Pharmacol Exp Ther. 1996;276(2):460-6.
  37. Blokland A, Prickaerts J, Honig W, de Vente J. State-dependent impairment in object recognition after hippocampal NOS inhibition. Neuroreport. 1998;9(18):4205-8.
  38. Ingram DK, Spangler EL, Kametani H, Meyer RC, London ED. Intracerebroventricular injection of N omega-nitro-L-arginine in rats impairs learning in a 14-unit T-maze. Eur J Pharmacol. 1998;341(1):11-6.
  39. Fin C, da Cunha C, Bromberg E, Schmitz PK, Bianchin M, Medina JH, et al. Experiments suggesting a role for nitric oxide in the hippocampus in memory processes. Neurobiol Learn Mem. 1995;63(2):113-5.
  40. Piri M, Zarrindast MR. Nitric oxide in the ventral tegmental area is involved in retrieval of inhibitory avoidance memory by nicotine. Neuroscience. 2011;175:154-61.
  41. Zarrindast MR, Piri M, Nasehi M, Ebrahimi-Ghiri M. Nitric oxide in the nucleus accumbens is involved in retrieval of inhibitory avoidance memory by nicotine. Pharmacol Biochem Behav. 2012;101(1):166-73.
  42. Blokland A, de Vente J, Prickaerts J, Honig W, Markerink-van Ittersum M, Steinbusch H. Local inhibition of hippocampal nitric oxide synthase does not impair place learning in the Morris water escape task in rats. Eur J Neurosci. 1999;11(1):223-32.
  43. Bannerman DM, Chapman PF, Kelly PA, Butcher SP, Morris RG. Inhibition of nitric oxide synthase does not impair spatial learning. J Neurosci. 1994;14(12):7404-14.
  44. Bohme GA, Bon C, Lemaire M, Reibaud M, Piot O, Stutzmann JM, et al. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. Proc Natl Acad Sci U S A. 1993;90(19):9191-4.
  45. Izquierdo I, Bevilaqua LR, Rossato JI, Bonini JS, Medina JH, Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 2006;29(9):496-505.
  46. Lisman JE, Grace AA. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron. 2005;46(5):703-13.
  47. Zahm DS, Heimer L. Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol. 1990;302(3):437-46.
  48. Kalivas PW, Churchill L, Klitenick MA. GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience. 1993;57(4):1047-60.
  49. Steffensen SC, Svingos AL, Pickel VM, Henriksen SJ. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci. 1998;18(19):8003-15.
  50. Gracy KN, Pickel VM. Ultrastructural localization and comparative distribution of nitric oxide synthase and N-methyl-D-aspartate receptors in the shell of the rat nucleus accumbens. Brain Res. 1997;747(2):259-72.
  51. Afanas'ev I, Ferger B, Kuschinsky K. The associative type of sensitization to d-amphetamine is expressed as an NO-dependent dramatic increase in extracellular dopamine in the nucleus accumbens. Naunyn Schmiedebergs Arch Pharmacol. 2000;362(3):232-7.
  52. Oorschot DE. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical disector methods. J Comp Neurol. 1996;366(4):580-99.
  53. Ahmadi S, Zarrindast MR, Nouri M, Haeri-Rohani A, 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. 2007;88(3):352-8.
  54. Azizbeigi R, Ahmadi S, Babapour V, Rezayof A, Zarrindast MR. Nicotine restores morphine-induced memory deficit through the D1 and D2 dopamine receptor mechanisms in the nucleus accumbens. J Psychopharmacol. 2011;25(8):1126-33.
  55. Rezayof A, Motevasseli T, Rassouli Y, Zarrindast MR. Dorsal hippocampal dopamine receptors are involved in mediating ethanol state-dependent memory. Life Sci. 2007;80(4):285-92.
  56. Schilstrom B, Nomikos GG, Nisell M, Hertel P, Svensson TH. N-methyl-D-aspartate receptor antagonism in the ventral tegmental area diminishes the systemic nicotine-induced dopamine release in the nucleus accumbens. Neuroscience. 1998;82(3):781-9.
  57. Schilstrom B, Svensson HM, Svensson TH, Nomikos GG. Nicotine and food induced dopamine release in the nucleus accumbens of the rat: putative role of alpha7 nicotinic receptors in the ventral tegmental area. Neuroscience. 1998;85(4):1005-9.
  58. Paxinos G, & Watson, C. The rat brain in stereotaxic coordinatesed r, editor. San Diego: Academic Press; 1997.
  59. Azami NS, Piri M, Oryan S, Jahanshahi M, Babapour V, Zarrindast MR. Involvement of dorsal hippocampal alpha-adrenergic receptors in the effect of scopolamine on memory retrieval in inhibitory avoidance task. Neurobiol Learn Mem. 2010;93(4):455-62.
  60. Nasehi M, Piri M, Jamali-Raeufy N, Zarrindast MR. Influence of intracerebral administration of NO agents in dorsal hippocampus (CA1) on cannabinoid state-dependent memory in the step-down passive avoidance test. Physiol Behav. 2010;100(4):297-304.
  61. Zarrindast MR, Eidi M, Eidi A, Oryan S. Effects of histamine and opioid systems on memory retention of passive avoidance learning in rats. Eur J Pharmacol. 2002;452(2):193-7.
  62. Zarrindast MR, Farajzadeh Z, Rostami P, Rezayof A, Nourjah P. Involvement of the ventral tegmental area (VTA) in morphine-induced memory retention in morphine-sensitized rats. Behav Brain Res. 2005;163(1):100-6.
  63. Davis JA, Kenney JW, Gould TJ. Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning. J Neurosci. 2007;27(40):10870-7.
  64. Manago F, Castellano C, Oliverio A, Mele A, De Leonibus E. Role of dopamine receptors subtypes, D1-like and D2-like, within the nucleus accumbens subregions, core and shell, on memory consolidation in the one-trial inhibitory avoidance task. Learn Mem. 2009;16(1):46-52.
  65. Ahmadi S, Zarrindast MR, Haeri-Rohani A, Rezayof A, Nouri M. Nicotine improves morphine-induced impairment of memory: possible involvement of N-methyl-D-aspartate receptors in the nucleus accumbens. Dev Neurobiol. 2007;67(8):1118-27.
  66. Criswell HE, Simson PE, Duncan GE, McCown TJ, Herbert JS, Morrow AL, et al. Molecular basis for regionally specific action of ethanol on gamma-aminobutyric acidA receptors: generalization to other ligand-gated ion channels. J Pharmacol Exp Ther. 1993;267(1):522-37.
  67. Yang X, Criswell HE, Breese GR. Action of ethanol on responses to nicotine from cerebellar interneurons and medial septal neurons: relationship to methyllycaconitine inhibition of nicotine responses. Alcohol Clin Exp Res. 1999;23(6):983-90.
  68. Marszalec W, Aistrup GL, Narahashi T. Ethanol-nicotine interactions at alpha-bungarotoxin-insensitive nicotinic acetylcholine receptors in rat cortical neurons. Alcohol Clin Exp Res. 1999;23(3):439-45.
  69. Wonnacott S. Presynaptic nicotinic ACh receptors. Trends Neurosci. 1997;20(2):92-8.
  70. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science. 1995;269(5231):1692-6.
  71. Harooni HE, Naghdi N, Sepehri H, Rohani AH. The role of hippocampal nitric oxide (NO) on learning and immediate, short- and long-term memory retrieval in inhibitory avoidance task in male adult rats. Behav Brain Res. 2009;201(1):166-72.
  72. Baratti CM, Boccia MM, Blake MG, Acosta GB. Reactivated memory of an inhibitory avoidance response in mice is sensitive to a nitric oxide synthase inhibitor. Neurobiol Learn Mem. 2008;89(4):426-40.
  73. Pitsikas N, Rigamonti AE, Bonomo SM, Cella SG, Muller EE. Molsidomine antagonizes L-NAME-induced acquisition deficits in a recognition memory task in the rat. Pharmacol Res. 2003;47(4):311-5.
  74. Cobb BL, Ryan KL, Frei MR, Guel-Gomez V, Mickley GA. Chronic administration of L-NAME in drinking water alters working memory in rats. Brain Res Bull. 1995;38(2):203-7.
  75. Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE, et al. The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci. 1997;9(3):354-81.
  76. Johnson SW, Mercuri NB, North RA. 5-hydroxytryptamine1B receptors block the GABAB synaptic potential in rat dopamine neurons. J Neurosci. 1992;12(5):2000-6.
  77. Leone P, Pocock D, Wise RA. Morphine-dopamine interaction: ventral tegmental morphine increases nucleus accumbens dopamine release. Pharmacol Biochem Behav. 1991;39(2):469-72.
  78. Olmstead MC, Franklin KB. The development of a conditioned place preference to morphine: effects of microinjections into various CNS sites. Behav Neurosci. 1997;111(6):1324-34.
  79. Olmstead MC, Franklin KB. The development of a conditioned place preference to morphine: effects of lesions of various CNS sites. Behav Neurosci. 1997;111(6):1313-23.
  80. Manzanedo C, Aguilar MA, Rodriguez-Arias M, Minarro J. Effects of dopamine antagonists with different receptor blockade profiles on morphine-induced place preference in male mice. Behav Brain Res. 2001;121(1-2):189-97.
  81. Hefco V, Yamada K, Hefco A, Hritcu L, Tiron A, Nabeshima T. Role of the mesotelencephalic dopamine system in learning and memory processes in the rat. Eur J Pharmacol. 2003;475(1-3):55-60.
  82. Seamans JK, Floresco SB, Phillips AG. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J Neurosci. 1998;18(4):1613-21.
  83. Myhrer T. 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. 2003;41(2-3):268-87.
  84. Di Chiara G. Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol. 2000;393(1-3):295-314.
  85. Yang Y, Cao J, Xiong W, Zhang J, Zhou Q, Wei H, et al. Both stress experience and age determine the impairment or enhancement effect of stress on spatial memory retrieval. J Endocrinol. 2003;178(1):45-54.
Journal of Advanced Medical Sciences and Applied Technologies
Volume 2, Issue 1 - Serial Number 1
6
March 2016
Pages 151-161

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