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Modulation of Hippocampus-Dependent Learning and Synaptic Plasticity by Nicotine

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Abstract

A long-standing relationship between nicotinic acetylcholine receptors (nAChRs) and cognition exists. Drugs that act at nAChRs can have cognitive-enhancing effects and diseases that disrupt cognition such as Alzheimer’s disease and schizophrenia are associated with altered nAChR function. Specifically, hippocampus-dependent learning is particularly sensitive to the effects of nicotine. However, the effects of nicotine on hippocampus-dependent learning vary not only with the doses of nicotine used and whether nicotine is administered acutely, chronically, or withdrawn after chronic nicotine treatment but also vary across different hippocampus-dependent tasks such as the Morris water maze, the radial arm maze, and contextual fear conditioning. In addition, nicotine has variable effects across different types of hippocampal long-term potentiation (LTP). Because different types of hippocampus-dependent learning and LTP involve different neural and molecular substrates, comparing the effects of nicotine across these paradigms can yield insights into the mechanisms that may underlie the effects of nicotine on learning and memory and aid in understanding the variable effects of nicotine on cognitive processes. This review compares and contrasts the effects of nicotine on hippocampus-dependent learning and LTP and briefly discusses how the effects of nicotine on learning could contribute to nicotine addiction.

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Notes

  1. Studies that use nicotine tartrate salt vary in whether they report doses based on salt weight or nicotine base weight. When studies reported doses as salt weight, we converted them to free base. If a study did not specify, we used the dose they reported. For a detailed discussion of this, see [17].

References

  1. Penfield W, Milner B (1958) Memory deficit produced by bilateral lesions in the hippocampal zone. AMA Arch Neurol Psychiatry 79(5):475–497

    PubMed  CAS  Google Scholar 

  2. Rudy JW, O’Reilly RC (1999) Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus. Behav Neurosci 113(5):867–880

    PubMed  CAS  Google Scholar 

  3. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641

    PubMed  CAS  Google Scholar 

  4. Eichenbaum H (1999) The hippocampus and mechanisms of declarative memory. Behav Brain Res 103(2):123–133

    PubMed  CAS  Google Scholar 

  5. Antonova E et al (2004) The relationship between brain structure and neurocognition in schizophrenia: a selective review. Schizophr Res 70(2–3):117–145

    PubMed  Google Scholar 

  6. Boyer P et al (2007) Hippocampal abnormalities and memory deficits: new evidence of a strong pathophysiological link in schizophrenia. Brain Res Rev 54(1):92–112

    PubMed  CAS  Google Scholar 

  7. Hughes JR et al (1986) Prevalence of smoking among psychiatric outpatients. Am J Psychiatry 143(8):993–997

    PubMed  CAS  Google Scholar 

  8. Kumari V, Postma P (2005) Nicotine use in schizophrenia: the self medication hypotheses. Neurosci Biobehav Rev 29(6):1021–1034

    PubMed  CAS  Google Scholar 

  9. Muir JL (1997) Acetylcholine, aging, and Alzheimer’s disease. Pharmacol Biochem Behav 56(4):687–696

    PubMed  CAS  Google Scholar 

  10. Nordberg A (2001) Nicotinic receptor abnormalities of Alzheimer’s disease: therapeutic implications. Biol Psychiatry 49(3):200–210

    PubMed  CAS  Google Scholar 

  11. Oddo S, LaFerla FM (2006) The role of nicotinic acetylcholine receptors in Alzheimer’s disease. J Physiol Paris 99(2–3):172–179

    PubMed  CAS  Google Scholar 

  12. Birks J (2006) Cholinesterase inhibitors for Alzheimer’s disease. Cochrane Database Syst Rev (1):CD005593

  13. Rogers JL, See RE (2007) Selective inactivation of the ventral hippocampus attenuates cue-induced and cocaine-primed reinstatement of drug-seeking in rats. Neurobiol Learn Mem 87(4):688–692

    PubMed  CAS  Google Scholar 

  14. Mash DC et al (2007) Gene expression in human hippocampus from cocaine abusers identifies genes which regulate extracellular matrix remodeling. PLoS ONE 2(11):e1187

    PubMed  Google Scholar 

  15. Kelley AE (2004) Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44(1):161–179

    PubMed  CAS  Google Scholar 

  16. Gould TJ (2006) Nicotine and hippocampus-dependent learning: implications for addiction. Mol Neurobiol 34(2):93–107

    PubMed  CAS  Google Scholar 

  17. Matta SG et al (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190(3):269–319

    CAS  Google Scholar 

  18. Le Novere N, Grutter T, Changeux JP (2002) Models of the extracellular domain of the nicotinic receptors and of agonist- and Ca2+-binding sites. Proc Natl Acad Sci USA 99(5):3210–3215

    PubMed  Google Scholar 

  19. Rush R et al (2002) First and second transmembrane segments of alpha3, alpha4, beta2, and beta4 nicotinic acetylcholine receptor subunits influence the efficacy and potency of nicotine. Mol Pharmacol 61(6):1416–1422

    PubMed  CAS  Google Scholar 

  20. Lena C, Changeux JP (1998) Allosteric nicotinic receptors, human pathologies. J Physiol Paris 92(2):63–74

    PubMed  CAS  Google Scholar 

  21. Cordero-Erausquin M et al (2000) Nicotinic receptor function: new perspectives from knockout mice. Trends Pharmacol Sci 21(6):211–217

    PubMed  CAS  Google Scholar 

  22. McGehee DS (1999) Molecular diversity of neuronal nicotinic acetylcholine receptors. Ann N Y Acad Sci 868:565–577

    PubMed  CAS  Google Scholar 

  23. Decker MW et al (1995) Diversity of neuronal nicotinic acetylcholine receptors: lessons from behavior and implications for CNS therapeutics. Life Sci 56(8):545–570

    PubMed  CAS  Google Scholar 

  24. Hogg RC, Raggenbass M, Bertrand D (2003) Nicotinic acetylcholine receptors: from structure to brain function. Rev Physiol Biochem Pharmacol 147:1–46

    PubMed  CAS  Google Scholar 

  25. Jones S, Sudweeks S, Yakel JL (1999) Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22(12):555–561

    PubMed  CAS  Google Scholar 

  26. Salminen O et al (2004) Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol 65(6):1526–1535

    PubMed  CAS  Google Scholar 

  27. Salminen O et al (2007) Pharmacology of alpha-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol Pharmacol 71(6):1563–1571

    PubMed  CAS  Google Scholar 

  28. Marks MJ, Collins AC (1982) Characterization of nicotine binding in mouse brain and comparison with the binding of alpha-bungarotoxin and quinuclidinyl benzilate. Mol Pharmacol 22(3):554–564

    PubMed  CAS  Google Scholar 

  29. Whiteaker P et al (1999) An autoradiographic study of the distribution of binding sites for the novel alpha7-selective nicotinic radioligand [3H]-methyllycaconitine in the mouse brain. Eur J Neurosci 11(8):2689–2696

    PubMed  CAS  Google Scholar 

  30. Broide RS, Leslie FM (1999) The alpha7 nicotinic acetylcholine receptor in neuronal plasticity. Mol Neurobiol 20(1):1–16

    PubMed  CAS  Google Scholar 

  31. Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci 20(2):92–98

    PubMed  CAS  Google Scholar 

  32. Perry DC et al (2002) Measuring nicotinic receptors with characteristics of alpha4beta2, alpha3beta2 and alpha3beta4 subtypes in rat tissues by autoradiography. J Neurochem 82(3):468–481

    PubMed  CAS  Google Scholar 

  33. Fenster CP et al (1997) Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J Neurosci 17(15):5747–5759

    PubMed  CAS  Google Scholar 

  34. Papke RL, Sanberg PR, Shytle RD (2001) Analysis of mecamylamine stereoisomers on human nicotinic receptor subtypes. J Pharmacol Exp Ther 297(2):646–656

    PubMed  CAS  Google Scholar 

  35. Berg DK, Conroy WG (2002) Nicotinic alpha 7 receptors: synaptic options and downstream signaling in neurons. J Neurobiol 53(4):512–523

    PubMed  CAS  Google Scholar 

  36. Wooltorton JR et al (2003) Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23(8):3176–3185

    PubMed  CAS  Google Scholar 

  37. Orr-Urtreger A et al (1997) Mice deficient in the alpha7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents. J Neurosci 17(23):9165–9171

    PubMed  CAS  Google Scholar 

  38. Zhang ZW, Coggan JS, Berg DK (1996) Synaptic currents generated by neuronal acetylcholine receptors sensitive to alpha-bungarotoxin. Neuron 17(6):1231–1240

    PubMed  CAS  Google Scholar 

  39. Barrantes GE, Westwick J, Wonnacott S (1994) Nicotinic acetylcholine receptors in primary cultures of hippocampal neurons: pharmacology and Ca++ permeability. Biochem Soc Trans 22(3):294S

    PubMed  CAS  Google Scholar 

  40. Sorenson EM, Shiroyama T, Kitai ST (1998) Postsynaptic nicotinic receptors on dopaminergic neurons in the substantia nigra pars compacta of the rat. Neuroscience 87(3):659–673

    PubMed  CAS  Google Scholar 

  41. Porter JT et al (1999) Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19(13):5228–5235

    PubMed  CAS  Google Scholar 

  42. Nomikos GG et al (2000) Role of alpha7 nicotinic receptors in nicotine dependence and implications for psychiatric illness. Behav Brain Res 113(1–2):97–103

    PubMed  CAS  Google Scholar 

  43. Eilers H et al (1997) Functional deactivation of the major neuronal nicotinic receptor caused by nicotine and a protein kinase C-dependent mechanism. Mol Pharmacol 52(6):1105–1112

    PubMed  CAS  Google Scholar 

  44. Dajas-Bailador FA, Soliakov L, Wonnacott S (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J Neurochem 80(3):520–530

    PubMed  CAS  Google Scholar 

  45. Barrantes GE et al (1995) Nicotine increases intracellular calcium in rat hippocampal neurons via voltage-gated calcium channels. Neurosci Lett 196(1–2):101–104

    PubMed  CAS  Google Scholar 

  46. Sabban EL, Gueorguiev VD (2002) Effects of short- and long-term nicotine treatment on intracellular calcium and tyrosine hydroxylase gene expression. Ann N Y Acad Sci 971:39–44

    PubMed  CAS  Google Scholar 

  47. Nakayama H et al (2001) Nicotine-induced phosphorylation of extracellular signal-regulated protein kinase and CREB in PC12h cells. J Neurochem 79(3):489–498

    PubMed  CAS  Google Scholar 

  48. Amaral D, Lavenex P (2007) Hippocampal neuroanatomy. In: Anderson P et al (ed) The hippocampus book. Oxford University Press, New York, pp 37–114

    Google Scholar 

  49. Rolls ET, Kesner RP (2006) A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79(1):1–48

    PubMed  CAS  Google Scholar 

  50. Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3(2):165–182

    PubMed  CAS  Google Scholar 

  51. Lee I, Kesner RP (2004) Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14(1):66–76

    PubMed  Google Scholar 

  52. Gilbert PE, Kesner RP, Lee I (2001) Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 11(6):626–636

    PubMed  CAS  Google Scholar 

  53. Bakker A et al (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319(5870):1640–1642

    PubMed  CAS  Google Scholar 

  54. Gilbert PE, Kesner RP (2003) Localization of function within the dorsal hippocampus: the role of the CA3 subregion in paired-associate learning. Behav Neurosci 117(6):1385–1394

    PubMed  Google Scholar 

  55. Daumas S et al (2005) Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learn Mem 12(4):375–382

    PubMed  Google Scholar 

  56. Nakazawa K et al (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297(5579):211–218

    PubMed  CAS  Google Scholar 

  57. Gold AE, Kesner RP (2005) The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15(6):808–814

    PubMed  Google Scholar 

  58. Huerta PT et al (2000) Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25(2):473–480

    PubMed  CAS  Google Scholar 

  59. Hoge J, Kesner RP (2007) Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects. Neurobiol Learn Mem 88(2):225–231

    PubMed  CAS  Google Scholar 

  60. Vago DR, Bevan A, Kesner RP (2007) The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval. Hippocampus 17(10):977–987

    PubMed  Google Scholar 

  61. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86

    PubMed  Google Scholar 

  62. Moscovitch M et al (2005) Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 207(1):35–66

    PubMed  Google Scholar 

  63. Remondes M, Schuman EM (2004) Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431(7009):699–703

    PubMed  CAS  Google Scholar 

  64. Fabian-Fine R et al (2001) Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21(20):7993–8003

    PubMed  CAS  Google Scholar 

  65. Wada E et al (1989) Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol 284(2):314–335

    PubMed  CAS  Google Scholar 

  66. Zarei MM et al (1999) Distributions of nicotinic acetylcholine receptor alpha7 and beta2 subunits on cultured hippocampal neurons. Neuroscience 88(3):755–764

    PubMed  CAS  Google Scholar 

  67. Alkondon M, Pereira EF, Albuquerque EX (1996) Mapping the location of functional nicotinic and gamma-aminobutyric acid A receptors on hippocampal neurons. J Pharmacol Exp Ther 279(3):1491–1506

    PubMed  CAS  Google Scholar 

  68. Radcliffe KA et al (1999) Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 868:591–610

    PubMed  CAS  Google Scholar 

  69. Alkondon M, Albuquerque EX (2001) Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86(6):3043–3055

    PubMed  CAS  Google Scholar 

  70. Alkondon M, Albuquerque EX (2004) The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex. Prog Brain Res 145:109–120

    PubMed  CAS  Google Scholar 

  71. McQuiston AR, Madison DV (1999) Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19(8):2887–2896

    PubMed  CAS  Google Scholar 

  72. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39

    PubMed  CAS  Google Scholar 

  73. Martin SJ, Morris RG (2002) New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus 12(5):609–636

    PubMed  CAS  Google Scholar 

  74. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232(2):331–356

    PubMed  CAS  Google Scholar 

  75. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84(1):87–136

    PubMed  CAS  Google Scholar 

  76. Sigurdsson T et al (2007) Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 52(1):215–227

    PubMed  CAS  Google Scholar 

  77. Whitlock JR et al (2006) Learning induces long-term potentiation in the hippocampus. Science 313(5790):1093–1097

    PubMed  CAS  Google Scholar 

  78. Pastalkova E et al (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313(5790):1141–1144

    PubMed  CAS  Google Scholar 

  79. Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16(6):710–715

    PubMed  CAS  Google Scholar 

  80. Benowitz NL, Porchet H, Jacob P 3rd (1989) Nicotine dependence and tolerance in man: pharmacokinetic and pharmacodynamic investigations. Prog Brain Res 79:279–287

    PubMed  CAS  Google Scholar 

  81. Yu JP et al (2007) Noradrenaline release by activation of kappa-bungarotoxin-sensitive nicotinic acetylcholine receptors participates in long-term potentiation-like response induced by nicotine. Sheng Li Xue Bao 59(6):814–820

    PubMed  Google Scholar 

  82. He J et al (2000) Long-term potentiation induced by nicotine in CA1 region of hippocampal slice is Ca(2+)-dependent. Acta Pharmacol Sin 21(5):429–432

    PubMed  CAS  Google Scholar 

  83. Wang J et al (2001) Activation of p42/44 mitogen-activated protein kinase pathway in long-term potentiation induced by nicotine in hippocampal CA1 region in rats. Acta Pharmacol Sin 22(8):685–690

    PubMed  CAS  Google Scholar 

  84. He J et al (2003) Different synaptic mechanisms of long-term potentiation induced by nicotine and tetanic stimulation in hippocampal CA1 region of rats. Acta Pharmacol Sin 24(5):398–402

    PubMed  CAS  Google Scholar 

  85. Fujii S et al (1999) Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Res 846(1):137–143

    PubMed  CAS  Google Scholar 

  86. Fujii S, Ji Z, Sumikawa K (2000) Inactivation of alpha7 ACh receptors and activation of non-alpha7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region. Neurosci Lett 286(2):134–138

    PubMed  CAS  Google Scholar 

  87. Fujii S et al (2000) Nicotine reverses GABAergic inhibition of long-term potentiation induction in the hippocampal CA1 region. Brain Res 863(1–2):259–265

    PubMed  CAS  Google Scholar 

  88. Nakauchi S et al (2007) Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2* nicotinic ACh receptors. Eur J Neurosci 25(9):2666–2681

    PubMed  Google Scholar 

  89. Ji D, Dani JA (2000) Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83(5):2682–2690

    PubMed  CAS  Google Scholar 

  90. Yamazaki Y et al (2005) Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. Eur J Neurosci 22(4):845–860

    PubMed  Google Scholar 

  91. Ji D, Lape R, Dani JA (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31(1):131–141

    PubMed  CAS  Google Scholar 

  92. Fujii S, Sumikawa K (2001) Nicotine accelerates reversal of long-term potentiation and enhances long-term depression in the rat hippocampal CA1 region. Brain Res 894(2):340–346

    PubMed  CAS  Google Scholar 

  93. Ge S, Dani JA (2005) Nicotinic acetylcholine receptors at glutamate synapses facilitate long-term depression or potentiation. J Neurosci 25(26):6084–6091

    PubMed  CAS  Google Scholar 

  94. Matsuyama S, Matsumoto A (2003) Epibatidine induces long-term potentiation (LTP) via activation of alpha4beta2 nicotinic acetylcholine receptors (nAChRs) in vivo in the intact mouse dentate gyrus: both alpha7 and alpha4beta2 nAChRs essential to nicotinic LTP. J Pharmacol Sci 93(2):180–187

    PubMed  CAS  Google Scholar 

  95. Matsuyama S et al (2000) Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. Eur J Neurosci 12(10):3741–3747

    PubMed  CAS  Google Scholar 

  96. Miner LL, Collins AC (1989) Strain comparison of nicotine-induced seizure sensitivity and nicotinic receptors. Pharmacol Biochem Behav 33(2):469–475

    PubMed  CAS  Google Scholar 

  97. Salas R et al (2004) The alpha3 and beta4 nicotinic acetylcholine receptor subunits are necessary for nicotine-induced seizures and hypolocomotion in mice. Neuropharmacology 47(3):401–407

    PubMed  CAS  Google Scholar 

  98. Hara K, Harris RA (2002) The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 94(2):313–318, table of contents

    PubMed  CAS  Google Scholar 

  99. Welsby P, Rowan M, Anwyl R (2006) Nicotinic receptor-mediated enhancement of long-term potentiation involves activation of metabotropic glutamate receptors and ryanodine-sensitive calcium stores in the dentate gyrus. Eur J Neurosci 24(11):3109–3118

    PubMed  Google Scholar 

  100. Welsby PJ, Rowan MJ, Anwyl R (2007) Beta-amyloid blocks high frequency stimulation induced LTP but not nicotine enhanced LTP. Neuropharmacology 53(1):188–195

    PubMed  CAS  Google Scholar 

  101. Marks MJ et al (1992) Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J Neurosci 12(7):2765–2784

    PubMed  CAS  Google Scholar 

  102. Gentry CL, Lukas RJ (2002) Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr Drug Targets CNS Neurol Disord 1(4):359–385

    PubMed  CAS  Google Scholar 

  103. Nashmi R et al (2007) Chronic nicotine cell specifically upregulates functional alpha 4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci 27(31):8202–8218

    PubMed  CAS  Google Scholar 

  104. Yamazaki Y et al (2006) Nicotine withdrawal suppresses nicotinic modulation of long-term potentiation induction in the hippocampal CA1 region. Eur J Neurosci 24(10):2903–2916

    PubMed  Google Scholar 

  105. Mansvelder HD, McGehee DS (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27(2):349–357

    PubMed  CAS  Google Scholar 

  106. Picciotto MR, Corrigall WA (2002) Neuronal systems underlying behaviors related to nicotine addiction: neural circuits and molecular genetics. J Neurosci 22(9):3338–33341

    PubMed  CAS  Google Scholar 

  107. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33–46

    PubMed  CAS  Google Scholar 

  108. Simosky JK, Stevens KE, Freedman R (2002) Nicotinic agonists and psychosis. Curr Drug Targets CNS Neurol Disord 1(2):149–162

    PubMed  CAS  Google Scholar 

  109. Mudo G, Belluardo N, Fuxe K (2007) Nicotinic receptor agonists as neuroprotective/neurotrophic drugs. Progress in molecular mechanisms. J Neural Transm 114(1):135–147

    PubMed  CAS  Google Scholar 

  110. Picciotto MR, Zoli M (2008) Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer’s and Parkinson’s disease. Front Biosci 13:492–504

    PubMed  CAS  Google Scholar 

  111. Albensi BC et al (2007) Electrical stimulation protocols for hippocampal synaptic plasticity and neuronal hyper-excitability: are they effective or relevant? Exp Neurol 204(1):1–13

    PubMed  Google Scholar 

  112. Morris RG et al (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681–683

    PubMed  CAS  Google Scholar 

  113. Giniatullin R, Nistri A, Yakel JL (2005) Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28(7):371–378

    PubMed  CAS  Google Scholar 

  114. Socci DJ, Sanberg PR, Arendash GW (1995) Nicotine enhances Morris water maze performance of young and aged rats. Neurobiol Aging 16(5):857–860

    PubMed  CAS  Google Scholar 

  115. Attaway CM, Compton DM, Turner MD (1999) The effects of nicotine on learning and memory: a neuropsychological assessment in young and senescent Fischer 344 rats. Physiol Behav 67(3):421–431

    PubMed  CAS  Google Scholar 

  116. Bernal MC et al (1999) Effects of nicotine on spatial learning in C57BL mice. Behav Pharmacol 10(3):333–336

    PubMed  CAS  Google Scholar 

  117. Abdulla FA et al (1996) Relationship between up-regulation of nicotine binding sites in rat brain and delayed cognitive enhancement observed after chronic or acute nicotinic receptor stimulation. Psychopharmacology (Berl) 124(4):323–331

    CAS  Google Scholar 

  118. Sharifzadeh M et al (2005) Post-training intrahippocampal infusion of nicotine prevents spatial memory retention deficits induced by the cyclo-oxygenase-2-specific inhibitor celecoxib in rats. J Neurochem 95(4):1078–1090

    PubMed  CAS  Google Scholar 

  119. Ren K et al (2007) alpha7 Nicotinic receptor gene delivery into mouse hippocampal neurons leads to functional receptor expression, improved spatial memory-related performance, and tau hyperphosphorylation. Neuroscience 145(1):314–322

    PubMed  CAS  Google Scholar 

  120. Scerri C et al (2006) The effects of chronic nicotine on spatial learning and bromodeoxyuridine incorporation into the dentate gyrus of the rat. Psychopharmacology (Berl) 184(3–4):540–546

    CAS  Google Scholar 

  121. Abrous DN et al (2002) Nicotine self-administration impairs hippocampal plasticity. J Neurosci 22(9):3656–3662

    PubMed  CAS  Google Scholar 

  122. Meck WH, Church RM, Olton DS (1984) Hippocampus, time, and memory. Behav Neurosci 98(1):3–22

    PubMed  CAS  Google Scholar 

  123. Levin E, Icenogle L, Farzad A (2005) Ketanserin attenuates nicotine-induced working memory improvement in rats. Pharmacol Biochem Behav 82(2):289–292

    PubMed  CAS  Google Scholar 

  124. Levin ED, Kaplan S, Boardman A (1997) Acute nicotine interactions with nicotinic and muscarinic antagonists: working and reference memory effects in the 16-arm radial maze. Behav Pharmacol 8(2–3):236–242

    PubMed  CAS  Google Scholar 

  125. Levin ED et al (1998) Nicotine–dizocilpine interactions and working and reference memory performance of rats in the radial-arm maze. Pharmacol Biochem Behav 61(3):335–340

    PubMed  CAS  Google Scholar 

  126. Levin ED, Torry D (1996) Acute and chronic nicotine effects on working memory in aged rats. Psychopharmacology (Berl) 123(1):88–97

    CAS  Google Scholar 

  127. Levin ED (1997) Chronic haloperidol administration does not block acute nicotine-induced improvements in radial-arm maze performance in the rat. Pharmacol Biochem Behav 58(4):899–902

    PubMed  CAS  Google Scholar 

  128. Addy N, Levin ED (2002) Nicotine interactions with haloperidol, clozapine and risperidone and working memory function in rats. Neuropsychopharmacology 27(4):534–541

    PubMed  CAS  Google Scholar 

  129. Levin ED et al (2003) Ventral hippocampal NMDA blockade and nicotinic effects on memory function. Brain Res Bull 61(5):489–495

    PubMed  CAS  Google Scholar 

  130. Kholdebarin E et al (2007) Interaction of nicotinic and histamine H(3) systems in the radial-arm maze repeated acquisition task. Eur J Pharmacol 569(1–2):64–69

    PubMed  CAS  Google Scholar 

  131. Arthur D, Levin ED (2002) Chronic inhibition of alpha4beta2 nicotinic receptors in the ventral hippocampus of rats: impacts on memory and nicotine response. Psychopharmacology (Berl) 160(2):140–145

    CAS  Google Scholar 

  132. Levin ED et al (1990) Chronic nicotine and withdrawal effects on radial-arm maze performance in rats. Behav Neural Biol 53(2):269–276

    PubMed  CAS  Google Scholar 

  133. Levin ED et al (1993) Chronic nicotinic stimulation and blockade effects on working memory. Behav Pharmacol 4(2):179–182

    PubMed  CAS  Google Scholar 

  134. Levin ED et al (1999) Ventral hippocampal ibotenic acid lesions block chronic nicotine-induced spatial working memory improvement in rats. Brain Res Cogn Brain Res 7(3):405–410

    PubMed  CAS  Google Scholar 

  135. Levin ED et al (1993) Chronic nicotine reverses working memory deficits caused by lesions of the fimbria or medial basalocortical projection. Brain Res Cogn Brain Res 1(3):137–143

    PubMed  CAS  Google Scholar 

  136. Bancroft A, Levin ED (2000) Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology 39(13):2770–2778

    PubMed  CAS  Google Scholar 

  137. Bettany JH, Levin ED (2001) Ventral hippocampal alpha 7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze. Pharmacol Biochem Behav 70(4):467–474

    PubMed  CAS  Google Scholar 

  138. Levin ED et al (1992) Persistence of chronic nicotine-induced cognitive facilitation. Behav Neural Biol 58(2):152–158

    PubMed  CAS  Google Scholar 

  139. Levin ED et al (2002) Hippocampal alpha 7 and alpha 4 beta 2 nicotinic receptors and working memory. Neuroscience 109(4):757–765

    PubMed  CAS  Google Scholar 

  140. George TP et al (2002) Effects of smoking abstinence on visuospatial working memory function in schizophrenia. Neuropsychopharmacology 26(1):75–85

    PubMed  Google Scholar 

  141. Jacobsen LK et al (2005) Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 57(1):56–66

    PubMed  Google Scholar 

  142. Mendrek A et al (2006) Working memory in cigarette smokers: comparison to non-smokers and effects of abstinence. Addict Behav 31(5):833–844

    PubMed  Google Scholar 

  143. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci 3(Suppl):1184–1191

    PubMed  CAS  Google Scholar 

  144. Davis HP, Squire LR (1984) Protein synthesis and memory: a review. Psychol Bull 96(3):518–559

    PubMed  CAS  Google Scholar 

  145. Hernandez PJ, Abel T (2008) The role of protein synthesis in memory consolidation: progress amid decades of debate. Neurobiol Learn Mem 89(3):293–311

    PubMed  CAS  Google Scholar 

  146. Greenberg ME, Ziff EB, Greene LA (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234(4772):80–83

    PubMed  CAS  Google Scholar 

  147. Li MD et al (2004) Time-dependent changes in transcriptional profiles within five rat brain regions in response to nicotine treatment. Brain Res Mol Brain Res 132(2):168–180

    PubMed  CAS  Google Scholar 

  148. Gould TJ, Wehner JM (1999) Nicotine enhancement of contextual fear conditioning. Behav Brain Res 102(1–2):31–39

    PubMed  CAS  Google Scholar 

  149. Gould TJ, Lommock JA (2003) Nicotine enhances contextual fear conditioning and ameliorates ethanol-induced deficits in contextual fear conditioning. Behav Neurosci 117(6):1276–1282

    PubMed  CAS  Google Scholar 

  150. Gould TJ, Higgins SJ (2003) Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training. Neurobiol Learn Mem 80(2):147–157

    PubMed  CAS  Google Scholar 

  151. Gould TJ (2003) Nicotine produces a within-subject enhancement of contextual fear conditioning in C57BL/6 mice independent of sex. Integr Physiol Behav Sci 38(2):124–132

    PubMed  Google Scholar 

  152. Caldarone BJ, Duman CH, Picciotto MR (2000) Fear conditioning and latent inhibition in mice lacking the high affinity subclass of nicotinic acetylcholine receptors in the brain. Neuropharmacology 39(13):2779–2784

    PubMed  CAS  Google Scholar 

  153. Paylor R et al (1998) Alpha7 nicotinic receptor subunits are not necessary for hippocampal-dependent learning or sensorimotor gating: a behavioral characterization of Acra7-deficient mice. Learn Mem 5(4–5):302–316

    PubMed  CAS  Google Scholar 

  154. Burwell RD et al (2004) Corticohippocampal contributions to spatial and contextual learning. J Neurosci 24(15):3826–3836

    PubMed  CAS  Google Scholar 

  155. Good M, Honey RC (1997) Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111(3):487–493

    PubMed  CAS  Google Scholar 

  156. El-Ghundi M et al (1999) Spatial learning deficit in dopamine D(1) receptor knockout mice. Eur J Pharmacol 383(2):95–106

    PubMed  CAS  Google Scholar 

  157. Roberts AJ et al (2004) Mice lacking 5-HT receptors show specific impairments in contextual learning. Eur J Neurosci 19(7):1913–1922

    PubMed  Google Scholar 

  158. Voikar V et al (2004) Impaired behavioural flexibility and memory in mice lacking GDNF family receptor alpha2. Eur J Neurosci 20(1):308–312

    PubMed  Google Scholar 

  159. Graves L et al (2002) Behavioral analysis of CREB alpha delta mutation on a B6/129 F1 hybrid background. Hippocampus 12(1):18–26

    PubMed  CAS  Google Scholar 

  160. Van Dam D et al (2000) Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice. Behav Brain Res 117(1–2):127–136

    PubMed  Google Scholar 

  161. Peters M et al (2003) Loss of Ca2+/calmodulin kinase kinase beta affects the formation of some, but not all, types of hippocampus-dependent long-term memory. J Neurosci 23(30):9752–9760

    PubMed  CAS  Google Scholar 

  162. Yasuda M, Mayford MR (2006) CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory. Neuron 50(2):309–318

    PubMed  CAS  Google Scholar 

  163. Owen EH et al (1997) Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80(4):1087–1099

    PubMed  CAS  Google Scholar 

  164. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106(2):274–285

    PubMed  CAS  Google Scholar 

  165. Logue SF, Paylor R, Wehner JM (1997) Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behav Neurosci 111(1):104–113

    PubMed  CAS  Google Scholar 

  166. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931

    PubMed  CAS  Google Scholar 

  167. Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88(2):261–274

    PubMed  CAS  Google Scholar 

  168. Fanselow MS (2000) Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110(1–2):73–81

    PubMed  CAS  Google Scholar 

  169. Lopez-Fernandez MA et al (2007) Upregulation of polysialylated neural cell adhesion molecule in the dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. J Neurosci 27(17):4552–4561

    PubMed  CAS  Google Scholar 

  170. Abel T, Lattal KM (2001) Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11(2):180–187

    PubMed  CAS  Google Scholar 

  171. Gould TJ, McCarthy MM, Keith RA (2002) MK-801 disrupts acquisition of contextual fear conditioning but enhances memory consolidation of cued fear conditioning. Behav Pharmacol 13(4):287–294

    PubMed  CAS  Google Scholar 

  172. Young SL, Bohenek DL, Fanselow MS (1994) NMDA processes mediate anterograde amnesia of contextual fear conditioning induced by hippocampal damage: immunization against amnesia by context preexposure. Behav Neurosci 108(1):19–29

    PubMed  CAS  Google Scholar 

  173. Quinn JJ et al (2005) Dorsal hippocampus NMDA receptors differentially mediate trace and contextual fear conditioning. Hippocampus 15(5):665–674

    PubMed  CAS  Google Scholar 

  174. Sindreu CB, Scheiner ZS, Storm DR (2007) Ca2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 53(1):79–89

    PubMed  CAS  Google Scholar 

  175. Ohno M, Frankland PW, Silva AJ (2002) A pharmacogenetic inducible approach to the study of NMDA/alpha CaMKII signaling in synaptic plasticity. Curr Biol 12(8):654–656

    PubMed  CAS  Google Scholar 

  176. Roberson ED, Sweatt JD (1996) Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation. J Biol Chem 271(48):30436–30441

    PubMed  CAS  Google Scholar 

  177. Roberson ED et al (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19(11):4337–4348

    PubMed  CAS  Google Scholar 

  178. Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71(6):401–437

    PubMed  CAS  Google Scholar 

  179. Steiner RC, Heath CJ, Picciotto MR (2007) Nicotine-induced phosphorylation of ERK in mouse primary cortical neurons: evidence for involvement of glutamatergic signaling and CaMKII. J Neurochem 103(2):666–678

    PubMed  CAS  Google Scholar 

  180. Davis JA, Gould TJ (2006) The effects of DHBE and MLA on nicotine-induced enhancement of contextual fear conditioning in C57BL/6 mice. Psychopharmacology (Berl) 184(3–4):345–352

    CAS  Google Scholar 

  181. Davis JA, Porter J, Gould TJ (2006) Nicotine enhances both foreground and background contextual fear conditioning. Neurosci Lett 394(3):202–205

    PubMed  CAS  Google Scholar 

  182. Gould TJ, Feiro O, Moore D (2004) Nicotine enhances trace cued fear conditioning but not delay cued fear conditioning in C57BL/6 mice. Behav Brain Res 155(1):167–173

    PubMed  CAS  Google Scholar 

  183. Gulick D, Gould TJ (2007) Interactive effects of ethanol and nicotine on learning in C57BL/6J mice depend on both dose and duration of treatment. Psychopharmacology (Berl) 196:483–495

    Google Scholar 

  184. Davis JA et al (2005) Withdrawal from chronic nicotine administration impairs contextual fear conditioning in C57BL/6 mice. J Neurosci 25(38):8708–8713

    PubMed  CAS  Google Scholar 

  185. Szyndler J et al (2001) The anxiolytic-like effect of nicotine undergoes rapid tolerance in a model of contextual fear conditioning in rats. Pharmacol Biochem Behav 69(3–4):511–518

    PubMed  CAS  Google Scholar 

  186. Davis JA, Kenney JW, Gould TJ (2007) Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning. J Neurosci 27(40):10870–10877

    PubMed  CAS  Google Scholar 

  187. Seguela P et al (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13(2):596–604

    PubMed  CAS  Google Scholar 

  188. Chavez-Noriega LE et al (1997) Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors h alpha 2 beta 2, h alpha 2 beta 4, h alpha 3 beta 2, h alpha 3 beta 4, h alpha 4 beta 2, h alpha 4 beta 4 and h alpha 7 expressed in Xenopus oocytes. J Pharmacol Exp Ther 280(1):346–356

    PubMed  CAS  Google Scholar 

  189. Davis JA, Gould TJ (2007) beta2 subunit-containing nicotinic receptors mediate the enhancing effect of nicotine on trace cued fear conditioning in C57BL/6 mice. Psychopharmacology (Berl) 190(3):343–352

    CAS  Google Scholar 

  190. Wehner JM et al (2004) Role of neuronal nicotinic receptors in the effects of nicotine and ethanol on contextual fear conditioning. Neuroscience 129(1):11–24

    PubMed  CAS  Google Scholar 

  191. Allen TG, Abogadie FC, Brown DA (2006) Simultaneous release of glutamate and acetylcholine from single magnocellular “cholinergic” basal forebrain neurons. J Neurosci 26(5):1588–1595

    PubMed  CAS  Google Scholar 

  192. Hefft S et al (1999) Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol 515(Pt 3):769–776

    PubMed  CAS  Google Scholar 

  193. Alkondon M, Pereira EF, Albuquerque EX (2003) NMDA and AMPA receptors contribute to the nicotinic cholinergic excitation of CA1 interneurons in the rat hippocampus. J Neurophysiol 90(3):1613–1625

    PubMed  CAS  Google Scholar 

  194. Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18(18):7075–7083

    PubMed  CAS  Google Scholar 

  195. Lu Y, Wehner JM (1997) Enhancement of contextual fear-conditioning by putative (+/−)-alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor modulators and N-methyl-d-aspartate (NMDA) receptor antagonists in DBA/2J mice. Brain Res 768(1–2):197–207

    PubMed  CAS  Google Scholar 

  196. Gould TJ, Lewis MC (2005) Coantagonism of glutamate receptors and nicotinic acetylcholinergic receptors disrupts fear conditioning and latent inhibition of fear conditioning. Learn Mem 12(4):389–398

    PubMed  Google Scholar 

  197. Fayuk D, Yakel JL (2007) Dendritic Ca2+ signalling due to activation of alpha 7-containing nicotinic acetylcholine receptors in rat hippocampal neurons. J Physiol 582(Pt 2):597–611

    PubMed  CAS  Google Scholar 

  198. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271(40):24329–24332

    PubMed  CAS  Google Scholar 

  199. Raybuck JD, Gould TJ (2007) Extracellular signal-regulated kinase 1/2 involvement in the enhancement of contextual fear conditioning by nicotine. Behav Neurosci 121(5):1119–1124

    PubMed  CAS  Google Scholar 

  200. Portugal GS, Kenney JW, Gould TJ (2008) Beta2 subunit containing acetylcholine receptors mediate nicotine withdrawal deficits in the acquisition of contextual fear conditioning. Neurobiol Learn Mem 89(2):106–113

    PubMed  CAS  Google Scholar 

  201. Davis JA, Gould TJ (2007) Atomoxetine reverses nicotine withdrawal-associated deficits in contextual fear conditioning. Neuropsychopharmacology 32(9):2011–2019

    PubMed  CAS  Google Scholar 

  202. Portugal GS, Gould TJ (2007) Bupropion dose-dependently reverses nicotine withdrawal deficits in contextual fear conditioning. Pharmacol Biochem Behav 88(2):179–187

    PubMed  CAS  Google Scholar 

  203. Andre JM et al (2008) Nicotine withdrawal disrupts both foreground and background contextual fear conditioning but not pre-pulse inhibition of the acoustic startle response in C57BL/6 mice. Behav Brain Res 190(2):174–181

    PubMed  CAS  Google Scholar 

  204. Tian S et al (2008) Prior chronic nicotine impairs cued fear extinction but enhances contextual fear conditioning in rats. Neuroscience 153(4):935–943

    PubMed  CAS  Google Scholar 

  205. Milekic MH et al (2006) Persistent disruption of an established morphine conditioned place preference. J Neurosci 26(11):3010–3020

    PubMed  CAS  Google Scholar 

  206. Dayas CV et al (2007) Distinct patterns of neural activation associated with ethanol seeking: effects of naltrexone. Biol Psychiatry 61(8):979–989

    PubMed  CAS  Google Scholar 

  207. Rademacher DJ et al (2006) The neural substrates of amphetamine conditioned place preference: implications for the formation of conditioned stimulus–reward associations. Eur J Neurosci 24(7):2089–2097

    PubMed  Google Scholar 

  208. Marie-Claire C et al (2007) Sensitization to the conditioned rewarding effects of morphine modulates gene expression in rat hippocampus. Neuropharmacology 52(2):430–435

    PubMed  CAS  Google Scholar 

  209. Due DL et al (2002) Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. Am J Psychiatry 159(6):954–960

    PubMed  Google Scholar 

  210. Franklin TR et al (2007) Limbic activation to cigarette smoking cues independent of nicotine withdrawal: a perfusion fMRI study. Neuropsychopharmacology 32(11):2301–2309

    PubMed  CAS  Google Scholar 

  211. Zubieta JK et al (2005) Regional cerebral blood flow responses to smoking in tobacco smokers after overnight abstinence. Am J Psychiatry 162(3):567–577

    PubMed  Google Scholar 

  212. Jones S, Bonci A (2005) Synaptic plasticity and drug addiction. Curr Opin Pharmacol 5(1):20–25

    PubMed  CAS  Google Scholar 

  213. Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46(5):703–713

    PubMed  CAS  Google Scholar 

  214. Fudala PJ, Teoh KW, Iwamoto ET (1985) Pharmacologic characterization of nicotine-induced conditioned place preference. Pharmacol Biochem Behav 22(2):237–241

    PubMed  CAS  Google Scholar 

  215. Walters CL et al (2006) The beta2 but not alpha7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology (Berl) 184(3–4):339–344

    CAS  Google Scholar 

  216. Wilkinson JL, Bevins RA (2008) Intravenous nicotine conditions a place preference in rats using an unbiased design. Pharmacol Biochem Behav 88(3):256–264

    PubMed  CAS  Google Scholar 

  217. Kleinman KM, Vaughn RL, Christ TS (1973) Effects of cigarette smoking and smoking deprivation on paired-associate learning of high and low meaningful nonsense syllables. Psychol Rep 32(3):963–966

    PubMed  CAS  Google Scholar 

  218. Snyder FR, Davis FC, Henningfield JE (1989) The tobacco withdrawal syndrome: performance decrements assessed on a computerized test battery. Drug Alcohol Depend 23(3):259–266

    PubMed  CAS  Google Scholar 

  219. Rukstalis M et al (2005) Increases in hyperactive-impulsive symptoms predict relapse among smokers in nicotine replacement therapy. J Subst Abuse Treat 28(4):297–304

    PubMed  Google Scholar 

  220. Felix R, Levin ED (1997) Nicotinic antagonist administration into the ventral hippocampus and spatial working memory in rats. Neuroscience 81(4):1009–1017

    PubMed  CAS  Google Scholar 

  221. Bannerman DM et al (2003) Ventral hippocampal lesions affect anxiety but not spatial learning. Behav Brain Res 139(1–2):197–213

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Karen Coletti for assistance with the figure and acknowledge excellent suggestions from anonymous reviewers. Cited work from the authors’ laboratory was funded in part by the National Institute on Drug Abuse (NIDA) grant DA017949 (TJG) and the National Institute on Alcohol Abuse and Alcoholism grant AA015515 (TJG). JWK was supported by NIDA training grant DA07237.

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  1. Department of Psychology, Center for Substance Abuse Research, Weiss Hall, Temple University, Philadelphia, PA, 19122, USA

    Justin W. Kenney & Thomas J. Gould

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Kenney, J.W., Gould, T.J. Modulation of Hippocampus-Dependent Learning and Synaptic Plasticity by Nicotine. Mol Neurobiol 38, 101–121 (2008). https://doi.org/10.1007/s12035-008-8037-9

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