Involvement of dorsal hippocampal and medial septal nicotinic receptors in cross state-dependent memory between WIN55, 212-2 and nicotine or ethanol in mice

Neuroscience

Volumn 245, Issue , 2013, Pages 61-73

  Alijanpour, S ^a   Rezayof, A ^a  

^a UNIVERSITY OF TEHRAN   (Iran)

Author keywords

Dorsal hippocampus; Ethanol; Medial septum; Memory retrieval; Nicotine; WIN55, 212 2

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ALCOHOL; MECAMYLAMINE; NICOTINE; NICOTINIC RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CHOLINERGIC SYSTEM; CONTROLLED STUDY; CROSS STATE DEPENDENT MEMORY; DOSE RESPONSE; EXPERIMENTAL TEST; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HISTOLOGY; MALE; MEMORY; MEMORY DISORDER; MOUSE; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; SEPTUM PELLUCIDUM;

ANIMALS; AVOIDANCE LEARNING; BENZOXAZINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; HIPPOCAMPUS; MALE; MEMORY; MICE; MICROINJECTIONS; MORPHOLINES; NAPHTHALENES; NICOTINE; RECEPTORS, NICOTINIC; SEPTUM OF BRAIN;

EID: 84877904409     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.04.030     Document Type: Article

References (95)

1. Alijanpour S., Rezayof A., Zarrindast M.R. Dorsal hippocampal cannabinoid CB1 receptors mediate the interactive effects of nicotine and ethanol on passive avoidance learning in mice. Addict Biol 2013, 18(2):241-251.
2. Arias-Carrión O., Stamelou M., Murillo-Rodríguez E., Menéndez-González M., Pöppel E. Dopaminergic reward system: a short integrative review. Int Arch Med 2010, 3:24.
3. Azam L., Winzer-Serhan U., Leslie F.M. Co-expression of alpha7 and beta2 nicotinic acetylcholine receptor subunit mRNAs within rat brain cholinergic neurons. Neuroscience 2003, 119(4):965-977.
4. Balerio G.N., Aso E., Berrendero F., Murtra P., Maldonado R. Delta9-tetrahydrocannabinol decreases somatic and motivational manifestations of nicotine withdrawal in mice. Eur J Neurosci 2004, 20(10):2737-2748.
5. Balerio G.N., Aso E., Maldonado R. Role of the cannabinoid system in the effects induced by nicotine on anxiety-like behaviour in mice. Psychopharmacology (Berl) 2006, 184(3-4):504-513.
6. Basavarajappa B.S., Ninan I., Arancio O. Acute ethanol suppresses glutamatergic neurotransmission through endocannabinoids in hippocampal neurons. J Neurochem 2008, 107(4):1001-1013.
7. Bhatti A.S., Aydin C., Oztan O., Ma Z., Hall P., Tao R., Isgor C. Effects of a cannabinoid receptor (CB) 1 antagonist AM251 on behavioral sensitization to nicotine in a rat model of novelty-seeking behavior: correlation with hippocampal 5HT. Psychopharmacology (Berl) 2009, 203(1):23-32.
8. Bird C.M., Burgess N. The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 2008, 9(3):182-194.
9. Bondi M.W., Drake A.I., Grant I. Verbal learning and memory in alcohol abusers and polysubstance abusers with concurrent alcohol abuse. J Int Neuropsychol Soc 1998, 4(4):319-328.
10. Bramness J.G., Khiabani H.Z., Mørland J. Impairment due to cannabis and ethanol: clinical signs and additive effects. Addiction 2010, 105(6):1080-1087.
11. Calandreau L., Jaffard R., Desmedt A. Dissociated roles for the lateral and medial septum in elemental and contextual fear conditioning. Learn Mem 2007, 14(6):422-429.
12. Clarke R.B., Adermark L. Acute ethanol treatment prevents endocannabinoid-mediated long-lasting disinhibition of striatal output. Neuropharmacology 2010, 58(4-5):799-805.
13. Clark R.E., Broad N.J., Squire L.R. Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life. Hippocampus 2005, 15(3):340-346.
14. Clarke J.R., Rossato J.I., Moniteiro S., Bevilaqua L.R., Izquierdo I., Cammarota M. Posttraining activation of CB1 cannabinoid receptors in the CA1 region of the dorsal hippocampus impairs object recognition long-term memory. Neurobiol Learn Mem 2008, 90(2):374-381.
15. Cohen C., Kodas E., Griebel G. CB1 receptor antagonists for the treatment of nicotine addiction. Pharmacol Biochem Behav 2005, 81(2):387-395.
16. Dableh L.J., Yashpal K., Henry J.L. Physiological evidence of a postsynaptic inhibition of the tail flick reflex by a cannabinoid receptor agonist. Eur J Pharmacol 2009, 602(1):36-40.
17. Da Cunha C., Wolfman C., Huang C.H., Walz R., Koya R., Bianchin M., Medina J.H., Izquierdo I. Effect of post-training injections of flumazenil into the amygdala, hippocampus and septum on retention of habituation and of inhibitory avoidance in rats. Braz J Med Biol Res 1991, 24(3):301-306.
18. Dani J.A., Bertrand D. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 2007, 47(1):699-729.
19. Dani J.A., Harris R.A. Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat Neurosci 2005, 8(11):1465-1470.
20. Davies M. The role of GABAA receptors in mediating the effects of alcohol in the central nervous system. J Psychiatry Neurosci 2003, 28(4):263-274.
21. de Bruin N.M., Lange J.H., Kruse C.G., Herremans A.H., Schoffelmeer A.N., van Drimmelen M., De Vries T.J. SLV330, a cannabinoid CB(1) receptor antagonist, attenuates ethanol and nicotine seeking and improves inhibitory response control in rats. Behav Brain Res 2011, 217(2):408-415.
22. De Fiebre N.C., De Fiebre C.M. α7 Nicotinic acetylcholine receptor knockout selectively enhances ethanol-, but not β-amyloid-induced neurotoxicity. Neurosci Lett 2005, 373(1):42-47.
23. Dougherty D.M., Marsh D.M., Moeller F.G., Chokshi R.V., Rosen V.C. Effects of moderate and high doses of alcohol on attention, impulsivity, discriminability, and response bias in immediate and delayed memory task performance. Alcohol Clin Exp Res 2000, 24(11):1702-1711.
24. Drever B.D., Riedel G., Platt B. The cholinergic system and hippocampal plasticity. Behave Brain Res 2011, 221(2):505-514.
25. Easton A., Douchamps V., Eacott M., Lever C. A specific role for septohippocampal acetylcholine in memory?. Neuropsychologia 2012, 50(13):3156-3168.
26. Elvander-Tottie E., Eriksson T.M., Sandin J., Ogren S.O. 5-HT(1A) and NMDA receptors interact in the rat medial septum and modulate hippocampal-dependent spatial learning. Hippocampus 2009, 19(12):1187-1198.
27. Ericson M., Molander A., Löf E., Engel J.A., Söderpalm B. Ethanol elevates accumbal dopamine levels via indirect activation of ventral tegmental nicotinic acetylcholine receptors. Eur J Pharmacol 2003, 467(1-3):85-93.
28. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 2007, Elsevier/Academic Press, San Diego. 3rd ed.
29. 3-mediated indirect suppression through endocannabinoid signaling. Eur J Neurosci 2004, 19(10):2682-2692.
30. Gamaleddin I., Wertheim C., Zhu A.Z., Coen K.M., Vemuri K., Makryannis A., Goldberg S.R., Le Foll B. Cannabinoid receptor stimulation increases motivation for nicotine and nicotine seeking. Addict Biol 2012, 17(1):47-61.
31. Ghiasvand M., Rezayof A., Zarrindast M.R., Ahmadi S. Activation of cannabinoid CB1 receptors in the central amygdala impairs inhibitory avoidance memory consolidation via NMDA receptors. Neurobiol Learn Mem 2011, 96(2):333-338.
32. Gulick D., Gould T.J. 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):483-495.
33. Gutierrez T., Nackley A.G., Neely M.H., Freeman K.G., Edwards G.L., Hohmann A.G. Effects of neurotoxic destruction of descending noradrenergic pathways on cannabinoid antinociception in models of acute and tonic nociception. Brain Res 2003, 987(2):176-185.
34. Hanchar H.J., Dodson P.D., Olsen R.W., Otis T.S., Wallner M. Alcohol-induced motor impairment caused by increased extrasynaptic GABA(A) receptor activity. Nat Neurosci 2005, 8(3):339-345.
35. Hansen H.H., Krutz B., Sifringer M., Stefovska V., Bittigau P., Pragst F., Marsicano G., Lutz B., Ikonomidou C. Cannabinoids enhance susceptibility of immature brain to ethanol neurotoxicity. Ann Neurol 2008, 64(1):42-52.
36. Hasselmo M.E. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 2006, 16(6):710-715.
37. Hyman S.E. Addiction: a disease of learning and memory. Am J Psychiatry 2005, 162(8):1414-1422.
38. Jafari M.R., Golmohammadi S., Ghiasvand F., Zarrindast M.R., Djahanguiri B. Influence of nicotinic receptor modulators on CB2 cannabinoid receptor agonist (JWH133)-induced antinociception in mice. Behav Pharmacol 2007, 18(7):691-697.
39. Jeltsch H., Bertrand F., Galani R., Lazarus C., Schimchowitsch S., Cassel J.C. Intraseptal injection of the 5-HT1A/5-HT7 agonist 8-OH-DPAT and working memory in rats. Psychopharmacology (Berl) 2004, 175(1):37-46.
40. Kanju P.M., Parameshwaran K., Sims-Robinson C., Uthayathas S., Josephson E.M., Rajakumar N., Dhanasekaran M., Suppiramaniam V. Selective cholinergic depletion in medial septum leads to impaired long term potentiation and glutamatergic synaptic currents in the hippocampus. PLoS One 2012, 7(2):e31073.
41. Khajehpour L., Rezayof A., Zarrindast M.R. Involvement of dorsal hippocampal nicotinic receptors in the effect of morphine on memory retrieval in passive avoidance task. Eur J Pharmacol 2008, 584(2-3):343-351.
42. Kim J., Isokawa M., Ledent C., Alger B.E. Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 2002, 22(23):10182-10191.
43. Kim S.M., Frank L.M. Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLoS One 2009, 4(5):e5494.
44. Larsson A., Engel J.A. Neurochemical and behavioral studies on ethanol and nicotine interactions. Neurosci Biobehav Rev 2004, 27(8):713-720.
45. Le Foll B., Goldberg S.R. Rimonabant, a CB1 antagonist, blocks nicotine-conditioned place preferences. Neuroreport 2004, 15(13):2139-2143.
46. Lemos J.I., Takahashi R.N., Morato G.S. Effects of SR141716 and WIN55,212-2 on tolerance to ethanol in rats using the acute and rapid procedures. Psychopharmacology (Berl) 2007, 194(2):139-149.
47. Madroñal N., Gruart A., Valverde O., Espadas I., Moratalla R., Delgado-García J.M. Involvement of cannabinoid CB1 receptor in associative learning and in hippocampal CA3-CA1 synaptic plasticity. Cereb Cortex 2012, 22(3):550-566.
48. Manseau F., Danik M., Williams S. A functional glutamatergic neurone network in the medial septum and diagonal band area. J Physiol 2005, 566:865-884.
49. McCool B.A. Ethanol modulation of synaptic plasticity. Neuropharmacology 2011, 61(7):1097-1108.
50. McKee S.A., Harrison E.L., O'malley S.S., Krishnan-Sarin S., Shi J., Tetrault J.M., Picciotto M.R., Petrakis I.L., Estevez N., Balchunas E. Varenicline reduces alcohols elf-administration in heavy-drinking smokers. Biol Psychiatry 2009, 66(2):185-190.
51. Medina K.L., Shear P.K., Schafer J., Armstrong T.G., Dyer P. Cognitive functioning and length of abstinence in polysubstance dependent men. Arch Clin Neuropsychol 2004, 19(2):245-258.
52. Merritt L.L., Martin B.R., Walters C., Lichtman A.H., Damaj M.I. The endogenous cannabinoid system modulates nicotine reward and dependence. J Pharmacol Exp Ther 2008, 326(2):483-492.
53. Nestor L., Roberts G., Garavan H., Hester R. Deficits in learning and memory: parahippocampal hyperactivity and frontocortical hypoactivity in cannabis users. Neuroimage 2008, 40(3):1328-1339.
54. Nyiri G., Szabadits E., Cserep C., Mackie K., Shigemoto R., Freund T.F. GABAB and CB1 cannabinoid receptor expression identifies two types of septal cholinergic neurons. Eur J Neurosci 2005, 21(11):3034-3042.
55. Okada K., Okaichi H. Functional cooperation between the hippocampal subregions and the medial septum in unreinforced and reinforced spatial memory tasks. Behav Brain Res 2010, 209(2):295-304.
56. Pamplona F.A., Takahashi R.N. WIN 55212-2 impairs contextual fear conditioning through the activation of CB1 cannabinoid receptors. Neurosci Lett 2006, 397(1-2):88-92.
57. Parfitt G.M., Campos R.C., Barbosa A.K., Koth A.P., Barros D.M. Participation of hippocampal cholinergic system in memory persistence for inhibitory avoidance in rats. Neurobiol Learn Mem 2012, 97(2):183-188.
58. Picciotto M.R., Caldarone B.J., King S.L., Zachariou V. Nicotinic receptors in the brain: links between molecular biology and behavior. Neuropsychopharmacology 2000, 22(5):451-465.
59. Pisanu A., Acquas E., Fenu S., Di Chiara G. Modulation of Delta(9)-THC-induced increase of cortical and hippocampal acetylcholine release by mu opioid and D(1) dopamine receptors. Neuropharmacology 2006, 50(6):661-670.
60. Placzek A.N., Zhang T.A., Dani J.A. Nicotinic mechanisms influencing synaptic plasticity in the hippocampus. Acta Pharmacol Sin 2009, 30(6):752-760.
61. Polissidis A., Chouliara O., Galanopoulos A., Marselos M., Papadopoulou-Daifoti Z., Antoniou K. Behavioural and dopaminergic alterations induced by a low dose of WIN 55,212-2 in a conditioned place preference procedure. Life Sci 2009, 85(5-6):248-254.
62. Polissidis A., Galanopoulos A., Naxakis G., Papahatjis D., Papadopoulou-Daifoti Z., Antoniou K. The cannabinoid CB1 receptor biphasically modulates motor activity and regulates dopamine and glutamate release region dependently. Int J Neuropsychopharmacol 2013, 16(2):393-403.
63. Raoufi N., Piri M., Moshfegh A., Shahin M.S. Nicotine improves ethanol-induced impairment of memory: possible involvement of nitric oxide in the dorsal hippocampus of mice. Neuroscience 2012, 219:82-91.
64. Rezayof A., Alijanpour S., Zarrindast M.R., Rassouli Y. Ethanol state-dependent memory: involvement of dorsal hippocampal muscarinic and nicotinic receptors. Neurobiol Learn Mem 2008, 89(4):441-447.
65. Rezayof A., Ghandipour M., Nazari-Serenjeh F. Effect of co-injection of arachydonilcyclopropylamide and ethanol on conditioned place preference in rats. Physiol Behav 2012, 107(3):301-308.
66. Rezayof A., Shirazi-Zand Z., Zarrindast M.R., Nayer-Nouri T. Nicotine improves ethanol-induced memory impairment: the role of dorsal hippocampal NMDA receptors. Life Sci 2010, 86(7-8):260-266.
67. Roberto M., Cruz M., Bajo M., Siggins G.R., Parsons L.H., Schweitzer P. The endocannabinoid system tonically regulates inhibitory transmission and depresses the effect of ethanol in central amygdala. Neuropsychopharmacology 2010, 35(9):1962-1972.
68. Robinson L., Hinder L., Pertwee R.G., Riedel G. Effects of D9-THC and WIN-55,212-2 on place preference in the water maze in rats. Psychopharmacology 2003, 166(1):40-50.
69. Ron D., Wang J. The NMDA receptor and alcohol addiction. Biology of the NMDA receptor 2009, CRC Press, Boca Raton, FL. A.M. Van Dongen (Ed.).
70. Rubio S.E., Vega-Flores G., Martínez A., Bosch C., Pérez-Mediavilla A., del Río J., Gruart A., Delgado-García J.M., Soriano E., Pascual M. Accelerated aging of the GABAergic septohippocampal pathway and decreased hippocampal rhythms in a mouse model of Alzheimer's disease. FASEB 2012, 26(11):4458-4467.
71. Schlicker E., Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 2001, 22(11):565-572.
72. Shulz D.E., Sosnik R., Ego V., Haidarliu S., Ahissar E. A neuronal analogue of state-dependent learning. Nature 2000, 403(6769):549-553.
73. Söderpalm B., Ericson M., Olausson P., Blomqvist O., Engel J.A. Nicotinic mechanisms involved in the dopamine activating and reinforcing properties of ethanol. Behav Brain Res 2000, 113(1-2):85-96.
74. Solinas M., Schema M., Tanda G., Wertheim C.E., Fratta W., Goldberg S.R. Nicotinic facilitation of Delta9-tetrahydrocannabinol discrimination involves endogenous anandamide. J Pharmacol Exp Ther 2007, 321(3):1127-1134.
75. Solinas M., Yasar S., Goldberg S.R. Endocannabinoid system involvement in brain reward processes related to drug abuse. Pharmacol Res 2007, 56(5):393-405.
76. Steensland P., Simms J.A., Holgate J., Richards J.K., Bartlett S.E. Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, selectively decreases ethanol consumption and seeking. Proc Natl Acad Sci U S A 2007, 104(30):12518-12523.
77. Tribollet E., Bertrand D., Marguerat A., Raggenbass M. Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 2004, 124(2):405-420.
78. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 1998, 83(2):393-411.
79. Tzavara E.T., Wade M., Nomikos G.G. Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J Neurosci 2003, 23(28):9374-9384.
80. Ujfalussy B., Kiss T. How do glutamatergic and GABAergic cells contribute to synchronization in the medial septum?. J Comput Neurosci 2006, 21(3):343-357.
81. Valjent E., Mitchell J.M., Besson M.J., Caboche J., Maldonado R. Behavioural and biochemical evidence for interactions between Delta9-tetrahydrocannabinol and nicotine. Br J Pharmacol 2002, 135(2):564-578.
82. Vengeliene V., Bilbao A., Molander A., Spanagel R. Neuropharmacology of alcohol addiction. Br J Pharmacol 2008, 154(2):299-315.
83. Vega-Flores G, Rubio SE, Jurado-Parras MT, Gómez-Climent MA, Hampe CS, Manto M, Soriano E, Pascual M, Gruart A, Delgado-García JM (2013) The GABAergic septohippocampal pathway is directly involved in internal processes related to operant reward learning. Cereb Cortex, in press.
84. Vinod K.Y., Yalamanchili R., Thanos P.K., Vadasz C., Cooper T.B., Volkow N.D., Hungund B.L. Genetic and pharmacological manipulations of the CB(1) receptor alter ethanol preference and dependence in ethanol preferring and nonpreferring mice. Synapse 2008, 62(8):574-581.
85. Viveros M.P., Marco E.M., Llorente R., Lamota L. The role of the hippocampus in mediating emotional responses to nicotine and cannabinoids: a possible neural substrate for functional interactions. Behav Pharmacol 2007, 18(5-6):375-389.
86. Warnault V., Houchi H., Barbier E., Pierrefiche O., Vilpoux C., Ledent C., Daoust M., Naassila M. The lack of CB1 receptors prevents neuroadaptations of both NMDA and GABA(A) receptors after chronic ethanol exposure. J Neurochem 2007, 102(3):741-752.
87. Wise R.A. Neurobiology of addiction. Curr Opin Neurobiol 1996, 6(2):243-251.
88. Wise L.E., Thorpe A.J., Lichtman A.H. Hippocampal CB1 receptors mediate the memory impairing effects of δ9-tetrahydrocannabinol. Neuropsychopharmacology 2009, 34(9):2072-2080.
89. Yesilyurt O., Dogrul A., Gul H., Seyrek M., Kusmez O., Ozkan Y., Yildiz O. Topical cannabinoid enhances topical morphine antinociception. Pain 2003, 105(1-2):303-308.
90. Zarrindast M.R., Rezayof A. Morphine state-dependent learning: sensitization and interactions with dopamine receptors. Eur J Pharmacol 2004, 497(2):197-204.
91. Zarrindast M.R., Kangarlu-Haghighi K., Khalilzadeh A., Fazli-Tabaei S. Influence of intracerebroventricular administration of cannabinergic drugs on morphine state-dependent memory in the step-down passive avoidance test. Behav Pharmacol 2006, 17(3):231-237.
92. Zarrindast M.R., Nouraei N., Khallilzadeh A., Askari E. Influence of acute and sub-chronic nicotine pretreatment on morphine state-dependent learning. Behav Brain Res 2006, 173(2):268-273.
93. Zarrindast M.R., Meshkani J., Rezayof A., Beigzadeh R., Rostami P. Nicotinic acetylcholine receptors of the dorsal hippocampus and the basolateral amygdala are involved in ethanol-induced conditioned place preference. Neuroscience 2010, 168(2):505-513.
94. Zarrindast M.R., Mashayekhi M., Rezayof A., Ahmadi S. β-Adrenoceptors in the dorsal hippocampus are involved in ethanol-induced state-dependent retrieval in mice. Neurobiol Learn Mem 2013, 100:12-17.
95. Zuo Y., Kuryatov A., Lindstrom J.M., Yeh J.Z., Narahashi T. Alcohol modulation of neuronal nicotinic acetylcholine receptors is alpha subunit dependent. Alcohol Clin Exp Res 2002, 26(6):779-784.