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Presynaptic Nicotinic Acetylcholine Receptors and the Modulation of Circuit Excitability

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Part of the book series: The Receptors ((REC,volume 26))

Abstract

Cholinergic modulation of circuit excitability by activation of nicotinic acetylcholine receptors (nAChRs) is involved in essential aspects of motivated behaviors, attention, and affect. In this review we focus entirely on the contribution of presynaptic nAChRs to the regulation and dysregulation of synapses and circuits in the CNS. In particular we highlight recent insights into the regulation of presynaptic nAChR targeting and advances into discerning the mechanisms by which presynaptic nAChRs regulate neurotransmitter release and synaptic transmission in the brain.

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References

  1. Koelle GB. A proposed dual neurohumoral role of acetylcholine: its functions at the pre- and post-synaptic sites. Nature. 1961;190:208–11. Epub 1961/04/15.

    CAS  PubMed  Google Scholar 

  2. Koelle GB. Early evidence of presynaptic receptors. Ann N Y Acad Sci. 1990;604:488–91. Epub 1990/01/01.

    CAS  PubMed  Google Scholar 

  3. Langer SZ. 25 years since the discovery of presynaptic receptors: present knowledge and future perspectives. Trends Pharmacol Sci. 1997;18(3):95–9. Epub 1997/03/01.

    CAS  PubMed  Google Scholar 

  4. Collier B, Katz HS. The synthesis, turnover and release of surplus acetylcholine in a sympathetic ganglion. J Physiol. 1971;214(3):537–52. Epub 1971/05/01.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Kalsner S. Heteroreceptors, autoreceptors, and other terminal sites. Ann N Y Acad Sci. 1990;604:1–6. Epub 1990/01/01.

    CAS  PubMed  Google Scholar 

  6. Brown DA, Jones KB, Halliwell JV, Quilliam JP. Evidence against a presynaptic action of acetylcholine during ganglionic transmission. Nature. 1970;226(5249):958–9. Epub 1970/06/06.

    CAS  PubMed  Google Scholar 

  7. Brown DA, Docherty RJ, Halliwell JV. The action of cholinomimetic substances on impulse conduction in the habenulointerpeduncular pathway of the rat in vitro. J Physiol. 1984;353:101–9. Epub 1984/08/01.

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature. 1996;383(6602):713–6. Epub 1996/10/24.

    CAS  PubMed  Google Scholar 

  9. 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. Epub 1995/09/22.

    CAS  PubMed  Google Scholar 

  10. Vidal C, Changeux JP. Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience. 1993;56(1):23–32. Epub 1993/09/01.

    CAS  PubMed  Google Scholar 

  11. MacDermott AB, Role LW, Siegelbaum SA. Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci. 1999;22:443–85. Epub 1999/04/15.

    CAS  PubMed  Google Scholar 

  12. Clarke PB, Hamill GS, Nadi NS, Jacobowitz DM, Pert A. 3H-nicotine- and 125I-alpha-bungarotoxin-labeled nicotinic receptors in the interpeduncular nucleus of rats. II. Effects of habenular deafferentation. J Comp Neurol. 1986;251(3):407–13. Epub 1986/09/15.

    CAS  PubMed  Google Scholar 

  13. Wonnacott S, Irons J, Rapier C, Thorne B, Lunt GG. Presynaptic modulation of transmitter release by nicotinic receptors. Prog Brain Res. 1989;79:157–63. Epub 1989/01/01.

    CAS  PubMed  Google Scholar 

  14. Kaiser SA, Soliakov L, Harvey SC, Luetje CW, Wonnacott S. Differential inhibition by alpha-conotoxin-MII of the nicotinic stimulation of [3H]dopamine release from rat striatal synaptosomes and slices. J Neurochem. 1998;70(3):1069–76. Epub 1998/03/07.

    CAS  PubMed  Google Scholar 

  15. Rapier C, Lunt GG, Wonnacott S. Nicotinic modulation of [3H]dopamine release from striatal synaptosomes: pharmacological characterisation. J Neurochem. 1990;54(3):937–45. Epub 1990/03/01.

    CAS  PubMed  Google Scholar 

  16. Rowell PP. Nanomolar concentrations of nicotine increase the release of [3H]dopamine from rat striatal synaptosomes. Neurosci Lett. 1995;189(3):171–5. Epub 1995/04/21.

    CAS  PubMed  Google Scholar 

  17. Wonnacott S, Kaiser S, Mogg A, Soliakov L, Jones IW. Presynaptic nicotinic receptors modulating dopamine release in the rat striatum. Eur J Pharmacol. 2000;393(1–3):51–8. Epub 2000/04/20.

    CAS  PubMed  Google Scholar 

  18. Reuben M, Clarke PB. Nicotine-evoked [3H]5-hydroxytryptamine release from rat striatal synaptosomes. Neuropharmacology. 2000;39(2):290–9. Epub 2000/02/12.

    CAS  PubMed  Google Scholar 

  19. Grady S, Marks MJ, Wonnacott S, Collins AC. Characterization of nicotinic receptor-mediated [3H]dopamine release from synaptosomes prepared from mouse striatum. J Neurochem. 1992;59(3):848–56. Epub 1992/09/01.

    CAS  PubMed  Google Scholar 

  20. Takano Y, Sakurai Y, Kohjimoto Y, Honda K, Kamiya HO. Presynaptic modulation of the release of dopamine from striatal synaptosomes: differences in the effects of high K+ stimulation, methamphetamine and nicotinic drugs. Brain Res. 1983;279(1–2):330–4. Epub 1983/11/21.

    CAS  PubMed  Google Scholar 

  21. Marchi M, Raiteri M. Nicotinic autoreceptors mediating enhancement of acetylcholine release become operative in conditions of “impaired” cholinergic presynaptic function. J Neurochem. 1996;67(5):1974–81. Epub 1996/11/01.

    CAS  PubMed  Google Scholar 

  22. Meyer EM, Arendash GW, Judkins JH, Ying L, Wade C, Kem WR. Effects of nucleus basalis lesions on the muscarinic and nicotinic modulation of [3H]acetylcholine release in the rat cerebral cortex. J Neurochem. 1987;49(6):1758–62. Epub 1987/12/01.

    CAS  PubMed  Google Scholar 

  23. McGehee DS, Role LW. Presynaptic ionotropic receptors. Curr Opin Neurobiol. 1996;6(3):342–9. Epub 1996/06/01.

    CAS  PubMed  Google Scholar 

  24. Wonnacott S. Presynaptic nicotinic ACh receptors. Trends Neurosci. 1997;20(2):92–8. Epub 1997/02/01.

    CAS  PubMed  Google Scholar 

  25. Clarke PB, Reuben M. Release of [3H]-noradrenaline from rat hippocampal synaptosomes by nicotine: mediation by different nicotinic receptor subtypes from striatal [3H]-dopamine release. Br J Pharmacol. 1996;117(4):595–606. Epub 1996/02/01.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev. 2009;89(1):73–120. Epub 2009/01/08.

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Gaimarri A, Moretti M, Riganti L, Zanardi A, Clementi F, Gotti C. Regulation of neuronal nicotinic receptor traffic and expression. Brain Res Rev. 2007;55(1):134–43. Epub 2007/03/27.

    CAS  PubMed  Google Scholar 

  28. Gotti C, Clementi F, Fornari A, Gaimarri A, Guiducci S, Manfredi I, et al. Structural and functional diversity of native brain neuronal nicotinic receptors. Biochem Pharmacol. 2009;78(7):703–11. Epub 2009/06/02.

    CAS  PubMed  Google Scholar 

  29. Gotti C, Riganti L, Vailati S, Clementi F. Brain neuronal nicotinic receptors as new targets for drug discovery. Curr Pharm Des. 2006;12(4):407–28. Epub 2006/02/14.

    CAS  PubMed  Google Scholar 

  30. Hogg RC, Raggenbass M, Bertrand D. Nicotinic acetylcholine receptors: from structure to brain function. Rev Physiol Biochem Pharmacol. 2003;147:1–46. Epub 2003/06/05.

    CAS  PubMed  Google Scholar 

  31. Picciotto MR, Higley MJ, Mineur YS. Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron. 2012;76(1):116–29. Epub 2012/10/09.

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Tammimaki A, Horton WJ, Stitzel JA. Recent advances in gene manipulation and nicotinic acetylcholine receptor biology. Biochem Pharmacol. 2011;82(8):808–19. Epub 2011/06/28.

    PubMed Central  PubMed  Google Scholar 

  33. Hellstrom-Lindahl E, Mousavi M, Zhang X, Ravid R, Nordberg A. Regional distribution of nicotinic receptor subunit mRNAs in human brain: comparison between Alzheimer and normal brain. Brain Res Mol Brain Res. 1999;66(1–2):94–103. Epub 1999/03/30.

    CAS  PubMed  Google Scholar 

  34. Yeh JJ, Yasuda RP, Davila-Garcia MI, Xiao Y, Ebert S, Gupta T, et al. Neuronal nicotinic acetylcholine receptor alpha3 subunit protein in rat brain and sympathetic ganglion measured using a subunit-specific antibody: regional and ontogenic expression. J Neurochem. 2001;77(1):336–46. Epub 2001/03/30.

    CAS  PubMed  Google Scholar 

  35. Duffy AM, Fitzgerald ML, Chan J, Robinson DC, Milner TA, Mackie K, et al. Acetylcholine alpha7 nicotinic and dopamine D2 receptors are targeted to many of the same postsynaptic dendrites and astrocytes in the rodent prefrontal cortex. Synapse. 2011;65(12):1350–67. Epub 2011/08/23.

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG, et al. Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci. 2001;21(20):7993–8003. Epub 2001/10/06.

    CAS  PubMed  Google Scholar 

  37. Jones IW, Barik J, O'Neill MJ, Wonnacott S. Alpha bungarotoxin-1.4 nm gold: a novel conjugate for visualising the precise subcellular distribution of alpha 7* nicotinic acetylcholine receptors. J Neurosci Methods. 2004;134(1):65–74.

    CAS  PubMed  Google Scholar 

  38. Jones IW, Wonnacott S. Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci. 2004;24(50):11244–52. Epub 2004/12/17.

    CAS  PubMed  Google Scholar 

  39. Commons KG. Alpha4 containing nicotinic receptors are positioned to mediate postsynaptic effects on 5-HT neurons in the rat dorsal raphe nucleus. Neuroscience. 2008;153(3):851–9. Epub 2008/04/12.

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Jones IW, Bolam JP, Wonnacott S. Presynaptic localisation of the nicotinic acetylcholine receptor beta2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones. J Comp Neurol. 2001;439(2):235–47. Epub 2001/10/12.

    CAS  PubMed  Google Scholar 

  41. Nakayama H, Shioda S, Nakajo S, Ueno S, Nakashima T, Nakai Y. Immunocytochemical localization of nicotinic acetylcholine receptor in the rat cerebellar cortex. Neurosci Res. 1997;29(3):233–9. Epub 1998/01/22.

    CAS  PubMed  Google Scholar 

  42. Nashmi R, Dickinson ME, McKinney S, Jareb M, Labarca C, Fraser SE, et al. Assembly of alpha4beta2 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits: effects of localization, trafficking, and nicotine-induced upregulation in clonal mammalian cells and in cultured midbrain neurons. J Neurosci. 2003;23(37):11554–67. Epub 2003/12/20.

    CAS  PubMed  Google Scholar 

  43. Bruses JL. Cell surface localization of alpha3beta4 nicotinic acetylcholine receptors is regulated by N-cadherin homotypic binding and actomyosin contractility. PLoS One. 2013;8(4):e62435. Epub 2013/04/30.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Chatterjee S, Santos N, Holgate J, Haass-Koffler CL, Hopf FW, Kharazia V, et al. The alpha5 subunit regulates the expression and function of alpha4*-containing neuronal nicotinic acetylcholine receptors in the ventral-tegmental area. PLoS One. 2013;8(7):e68300. Epub 2013/07/23.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Colombo SF, Mazzo F, Pistillo F, Gotti C. Biogenesis, trafficking and up-regulation of nicotinic ACh receptors. Biochem Pharmacol. 2013;86(8):1063–73. Epub 2013/07/09.

    CAS  PubMed  Google Scholar 

  46. Drenan RM, Nashmi R, Imoukhuede P, Just H, McKinney S, Lester HA. Subcellular trafficking, pentameric assembly, and subunit stoichiometry of neuronal nicotinic acetylcholine receptors containing fluorescently labeled alpha6 and beta3 subunits. Mol Pharmacol. 2008;73(1):27–41. Epub 2007/10/13.

    CAS  PubMed  Google Scholar 

  47. Grailhe R, de Carvalho LP, Paas Y, Le Poupon C, Soudant M, Bregestovski P, et al. Distinct subcellular targeting of fluorescent nicotinic alpha 3 beta 4 and serotoninergic 5-HT3A receptors in hippocampal neurons. Eur J Neurosci. 2004;19(4):855–62. Epub 2004/03/11.

    PubMed  Google Scholar 

  48. Murray TA, Liu Q, Whiteaker P, Wu J, Lukas RJ. Nicotinic acetylcholine receptor alpha7 subunits with a C2 cytoplasmic loop yellow fluorescent protein insertion form functional receptors. Acta Pharmacol Sin. 2009;30(6):828–41. Epub 2009/06/06.

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Richards CI, Srinivasan R, Xiao C, Mackey ED, Miwa JM, Lester HA. Trafficking of alpha4* nicotinic receptors revealed by superecliptic phluorin: effects of a beta4 amyotrophic lateral sclerosis-associated mutation and chronic exposure to nicotine. J Biol Chem. 2011;286(36):31241–9. Epub 2011/07/20.

    CAS  PubMed Central  PubMed  Google Scholar 

  50. St John PA. Cellular trafficking of nicotinic acetylcholine receptors. Acta Pharmacol Sin. 2009;30(6):656–62. Epub 2009/06/06.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Xu J, Zhu Y, Heinemann SF. Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J Neurosci. 2006;26(38):9780–93. Epub 2006/09/22.

    CAS  PubMed  Google Scholar 

  52. Graham AJ, Martin-Ruiz CM, Teaktong T, Ray MA, Court JA. Human brain nicotinic receptors, their distribution and participation in neuropsychiatric disorders. Curr Drug Targets CNS Neurol Disord. 2002;1(4):387–97. Epub 2003/05/29.

    CAS  PubMed  Google Scholar 

  53. Paterson D, Nordberg A. Neuronal nicotinic receptors in the human brain. Prog Neurobiol. 2000;61(1):75–111. Epub 2000/04/12.

    CAS  PubMed  Google Scholar 

  54. Colloby SJ, Firbank MJ, Pakrasi S, Perry EK, Pimlott SL, Wyper DJ, et al. Alterations in nicotinic alpha4beta2 receptor binding in vascular dementia using (1)(2)(3)I-5IA-85380 SPECT: comparison with regional cerebral blood flow. Neurobiol Aging. 2011;32(2):293–301. Epub 2009/03/10.

    CAS  PubMed  Google Scholar 

  55. Ellis JR, Nathan PJ, Villemagne VL, Mulligan RS, Ellis KA, Tochon-Danguy HJ, et al. The relationship between nicotinic receptors and cognitive functioning in healthy aging: An in vivo positron emission tomography (PET) study with 2-[(18)F]fluoro-A-85380. Synapse. 2009;63(9):752–63. Epub 2009/06/02.

    CAS  PubMed  Google Scholar 

  56. Gallezot JD, Bottlaender M, Gregoire MC, Roumenov D, Deverre JR, Coulon C, et al. In vivo imaging of human cerebral nicotinic acetylcholine receptors with 2-18F-fluoro-A-85380 and PET. J Nucl Med. 2005;46(2):240–7. Epub 2005/02/08.

    CAS  PubMed  Google Scholar 

  57. Kimes AS, Horti AG, London ED, Chefer SI, Contoreggi C, Ernst M, et al. 2-[18F]F-A-85380: PET imaging of brain nicotinic acetylcholine receptors and whole body distribution in humans. FASEB J. 2003;17(10):1331–3. Epub 2003/05/22.

    CAS  PubMed  Google Scholar 

  58. Hashimoto K, Nishiyama S, Ohba H, Matsuo M, Kobashi T, Takahagi M, et al. CHIBA-1001 as a novel PET ligand for alpha7 nicotinic receptors in the brain: a PET study in conscious monkeys. PLoS One. 2008;3(9):e3231. Epub 2008/09/19.

    PubMed Central  PubMed  Google Scholar 

  59. Toyohara J, Sakata M, Wu J, Ishikawa M, Oda K, Ishii K, et al. Preclinical and the first clinical studies on [11C]CHIBA-1001 for mapping alpha7 nicotinic receptors by positron emission tomography. Ann Nucl Med. 2009;23(3):301–9. Epub 2009/04/02.

    CAS  PubMed  Google Scholar 

  60. Yin L, Zhao Q, Li L, Zhang SL, Chen XQ, Ma C, et al. An experimental study on (131)I-CHIBA-1001: a radioligand for alpha7 nicotinic acetylcholine receptors. PLoS One. 2013;8(7):e70188. Epub 2013/08/13.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Brasic JR, Zhou Y, Musachio JL, Hilton J, Fan H, Crabb A, et al. Single photon emission computed tomography experience with (S)-5-[(123)I]iodo-3-(2-azetidinylmethoxy)pyridine in the living human brain of smokers and nonsmokers. Synapse. 2009;63(4):339–58. Epub 2009/01/14.

    CAS  PubMed Central  PubMed  Google Scholar 

  62. Kimes AS, Chefer SI, Matochik JA, Contoreggi CS, Vaupel DB, Stein EA, et al. Quantification of nicotinic acetylcholine receptors in the human brain with PET: bolus plus infusion administration of 2-[18F]F-A85380. Neuroimage. 2008;39(2):717–27. Epub 2007/10/27.

    PubMed Central  PubMed  Google Scholar 

  63. Picard F, Bruel D, Servent D, Saba W, Fruchart-Gaillard C, Schollhorn-Peyronneau MA, et al. Alteration of the in vivo nicotinic receptor density in ADNFLE patients: a PET study. Brain. 2006;129(Pt 8):2047–60. Epub 2006/07/04.

    CAS  PubMed  Google Scholar 

  64. Picard F, Sadaghiani S, Leroy C, Courvoisier DS, Maroy R, Bottlaender M. High density of nicotinic receptors in the cingulo-insular network. Neuroimage. 2013;79:42–51. Epub 2013/05/02.

    CAS  PubMed  Google Scholar 

  65. Mukhin AG, Kimes AS, Chefer SI, Matochik JA, Contoreggi CS, Horti AG, et al. Greater nicotinic acetylcholine receptor density in smokers than in nonsmokers: a PET study with 2-18F-FA-85380. J Nucl Med. 2008;49(10):1628–35. Epub 2008/09/17.

    PubMed Central  PubMed  Google Scholar 

  66. Oishi N, Hashikawa K, Yoshida H, Ishizu K, Ueda M, Kawashima H, et al. Quantification of nicotinic acetylcholine receptors in Parkinson’s disease with (123)I-5IA SPECT. J Neurol Sci. 2007;256(1–2):52–60. Epub 2007/03/21.

    CAS  PubMed  Google Scholar 

  67. Descarries L, Gisiger V, Steriade M. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol. 1997;53(5):603–25. Epub 1998/01/09.

    CAS  PubMed  Google Scholar 

  68. Vinson PN, Justice Jr JB. Effect of neostigmine on concentration and extraction fraction of acetylcholine using quantitative microdialysis. J Neurosci Methods. 1997;73(1):61–7. Epub 1997/04/25.

    CAS  PubMed  Google Scholar 

  69. Quirion R, Richard J, Wilson A. Muscarinic and nicotinic modulation of cortical acetylcholine release monitored by in vivo microdialysis in freely moving adult rats. Synapse. 1994;17(2):92–100. Epub 1994/06/01.

    CAS  PubMed  Google Scholar 

  70. Testylier G, Dykes RW. Acetylcholine release from frontal cortex in the waking rat measured by microdialysis without acetylcholinesterase inhibitors: effects of diisopropylfluorophosphate. Brain Res. 1996;740(1–2):307–15. Epub 1996/11/18.

    CAS  PubMed  Google Scholar 

  71. Vizi ES, Fekete A, Karoly R, Mike A. Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. Br J Pharmacol. 2010;160(4):785–809. Epub 2010/02/09.

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Bruno JP, Gash C, Martin B, Zmarowski A, Pomerleau F, Burmeister J, et al. Second-by-second measurement of acetylcholine release in prefrontal cortex. Eur J Neurosci. 2006;24(10):2749–57. Epub 2006/12/13.

    PubMed  Google Scholar 

  73. Giuliano C, Parikh V, Ward JR, Chiamulera C, Sarter M. Increases in cholinergic neurotransmission measured by using choline-sensitive microelectrodes: enhanced detection by hydrolysis of acetylcholine on recording sites? Neurochem Int. 2008;52(7):1343–50. Epub 2008/03/19.

    CAS  PubMed Central  PubMed  Google Scholar 

  74. Mattinson CE, Burmeister JJ, Quintero JE, Pomerleau F, Huettl P, Gerhardt GA. Tonic and phasic release of glutamate and acetylcholine neurotransmission in sub-regions of the rat prefrontal cortex using enzyme-based microelectrode arrays. J Neurosci Methods. 2011;202(2):199–208. Epub 2011/09/08.

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Parikh V, Kozak R, Martinez V, Sarter M. Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron. 2007;56(1):141–54. Epub 2007/10/09.

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Parikh V, Pomerleau F, Huettl P, Gerhardt GA, Sarter M, Bruno JP. Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels. Eur J Neurosci. 2004;20(6):1545–54. Epub 2004/09/10.

    PubMed  Google Scholar 

  77. Fadel JR. Regulation of cortical acetylcholine release: insights from in vivo microdialysis studies. Behav Brain Res. 2011;221(2):527–36. Epub 2010/02/23.

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Sarter M, Parikh V, Howe WM. nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol. 2009;78(7):658–67. Epub 2009/05/02.

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Sarter M, Parikh V, Howe WM. Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat Rev Neurosci. 2009;10(5):383–90. Epub 2009/04/21.

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Howe WM, Ji J, Parikh V, Williams S, Mocaer E, Trocme-Thibierge C, et al. Enhancement of attentional performance by selective stimulation of alpha4beta2nAChRs: underlying cholinergic mechanisms. Neuropsychopharmacology. 2010;35(6):1391–401. Epub 2010/02/12.

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Zhou FM, Liang Y, Dani JA. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci. 2001;4(12):1224–9. Epub 2001/11/20.

    CAS  PubMed  Google Scholar 

  82. Garduno J, Galindo-Charles L, Jimenez-Rodriguez J, Galarraga E, Tapia D, Mihailescu S, et al. Presynaptic alpha4beta2 nicotinic acetylcholine receptors increase glutamate release and serotonin neuron excitability in the dorsal raphe nucleus. J Neurosci. 2012;32(43):15148–57. Epub 2012/10/27.

    CAS  PubMed  Google Scholar 

  83. Guo JZ, Liu Y, Sorenson EM, Chiappinelli VA. Synaptically released and exogenous ACh activates different nicotinic receptors to enhance evoked glutamatergic transmission in the lateral geniculate nucleus. J Neurophysiol. 2005;94(4):2549–60. Epub 2005/06/24.

    CAS  PubMed  Google Scholar 

  84. Cachope R, Mateo Y, Mathur BN, Irving J, Wang HL, Morales M, et al. Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2012;2(1):33–41. Epub 2012/07/31.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Tang AH, Karson MA, Nagode DA, McIntosh JM, Uebele VN, Renger JJ, et al. Nerve terminal nicotinic acetylcholine receptors initiate quantal GABA release from perisomatic interneurons by activating axonal T-type (Cav3) Ca(2)(+) channels and Ca(2)(+) release from stores. J Neurosci. 2011;31(38):13546–61. Epub 2011/09/24.

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Gu Z, Yakel JL. Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron. 2011;71(1):155–65. Epub 2011/07/13.

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Nakauchi S, Sumikawa K. Endogenously released ACh and exogenous nicotine differentially facilitate long-term potentiation induction in the hippocampal CA1 region of mice. Eur J Neurosci. 2012;35(9):1381–95. Epub 2012/04/03.

    PubMed  Google Scholar 

  88. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron. 2012;75(1):58–64. Epub 2012/07/17.

    CAS  PubMed  Google Scholar 

  89. Alkondon M, Pereira EF, Cortes WS, Maelicke A, Albuquerque EX. Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci. 1997;9(12):2734–42. Epub 1998/03/28.

    CAS  PubMed  Google Scholar 

  90. Higley MJ, Strittmatter SM. Neuroscience. Lynx for braking plasticity. Science. 2010;330(6008):1189–90. Epub 2010/11/27.

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Ibanez-Tallon I, Miwa JM, Wang HL, Adams NC, Crabtree GW, Sine SM, et al. Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron. 2002;33(6):893–903. Epub 2002/03/22.

    CAS  PubMed  Google Scholar 

  92. Miwa JM, Freedman R, Lester HA. Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron. 2011;70(1):20–33. Epub 2011/04/13.

    CAS  PubMed  Google Scholar 

  93. Miwa JM, Ibanez-Tallon I, Crabtree GW, Sanchez R, Sali A, Role LW, et al. lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron. 1999;23(1):105–14. Epub 1999/07/13.

    CAS  PubMed  Google Scholar 

  94. Miwa JM, Lester HA, Walz A. Optimizing cholinergic tone through lynx modulators of nicotinic receptors: implications for plasticity and nicotine addiction. Physiology (Bethesda). 2012;27(4):187–99. Epub 2012/08/10.

    CAS  Google Scholar 

  95. Miwa JM, Stevens TR, King SL, Caldarone BJ, Ibanez-Tallon I, Xiao C, et al. The prototoxin lynx1 acts on nicotinic acetylcholine receptors to balance neuronal activity and survival in vivo. Neuron. 2006;51(5):587–600. Epub 2006/09/05.

    CAS  PubMed  Google Scholar 

  96. Morishita H, Miwa JM, Heintz N, Hensch TK. Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science. 2010;330(6008):1238–40. Epub 2010/11/13.

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Benowitz NL, Porchet H, Jacob 3rd P. Nicotine dependence and tolerance in man: pharmacokinetic and pharmacodynamic investigations. Prog Brain Res. 1989;79:279–87. Epub 1989/01/01.

    CAS  PubMed  Google Scholar 

  98. Henningfield JE, Stapleton JM, Benowitz NL, Grayson RF, London ED. Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug Alcohol Depend. 1993;33(1):23–9. Epub 1993/06/01.

    CAS  PubMed  Google Scholar 

  99. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA. Nicotine activates and desensitizes midbrain dopamine neurons. Nature. 1997;390(6658):401–4. Epub 1997/12/06.

    CAS  PubMed  Google Scholar 

  100. Picciotto MR, Kenny PJ. Molecular mechanisms underlying behaviors related to nicotine addiction. Cold Spring Harb Perspect Med. 2013;3(1):a012112. Epub 2012/11/13.

    PubMed Central  PubMed  Google Scholar 

  101. Mansvelder HD, Keath JR, McGehee DS. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron. 2002;33(6):905–19. Epub 2002/03/22.

    CAS  PubMed  Google Scholar 

  102. Mansvelder HD, McGehee DS. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron. 2000;27(2):349–57. Epub 2000/09/14.

    CAS  PubMed  Google Scholar 

  103. Xiao C, Nashmi R, McKinney S, Cai H, McIntosh JM, Lester HA. Chronic nicotine selectively enhances alpha4beta2* nicotinic acetylcholine receptors in the nigrostriatal dopamine pathway. J Neurosci. 2009;29(40):12428–39. Epub 2009/10/09.

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Dani JA, Bertrand D. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol. 2007;47:699–729. Epub 2006/10/03.

    CAS  PubMed  Google Scholar 

  105. Pidoplichko VI, Noguchi J, Areola OO, Liang Y, Peterson J, Zhang T, et al. Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction. Learn Mem. 2004;11(1):60–9. Epub 2004/01/30.

    PubMed Central  PubMed  Google Scholar 

  106. Poorthuis RB, Mansvelder HD. Nicotinic acetylcholine receptors controlling attention: behavior, circuits and sensitivity to disruption by nicotine. Biochem Pharmacol. 2013;86(8):1089–98. Epub 2013/07/17.

    CAS  PubMed  Google Scholar 

  107. Picciotto MR, Addy NA, Mineur YS, Brunzell DH. It is not “either/or”: activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood. Prog Neurobiol. 2008;84(4):329–42. Epub 2008/02/05.

    CAS  PubMed Central  PubMed  Google Scholar 

  108. Fenster CP, Whitworth TL, Sheffield EB, Quick MW, Lester RA. Upregulation of surface alpha4beta2 nicotinic receptors is initiated by receptor desensitization after chronic exposure to nicotine. J Neurosci. 1999;19(12):4804–14. Epub 1999/06/15.

    CAS  PubMed  Google Scholar 

  109. Marks MJ, Burch JB, Collins AC. Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J Pharmacol Exp Ther. 1983;226(3):817–25. Epub 1983/09/01.

    CAS  PubMed  Google Scholar 

  110. Quick MW, Lester RA. Desensitization of neuronal nicotinic receptors. J Neurobiol. 2002;53(4):457–78. Epub 2002/11/19.

    CAS  PubMed  Google Scholar 

  111. Schwartz RD, Kellar KJ. In vivo regulation of [3H]acetylcholine recognition sites in brain by nicotinic cholinergic drugs. J Neurochem. 1985;45(2):427–33. Epub 1985/08/01.

    CAS  PubMed  Google Scholar 

  112. Lopez-Hernandez GY, Sanchez-Padilla J, Ortiz-Acevedo A, Lizardi-Ortiz J, Salas-Vincenty J, Rojas LV, et al. Nicotine-induced up-regulation and desensitization of alpha4beta2 neuronal nicotinic receptors depend on subunit ratio. J Biol Chem. 2004;279(36):38007–15. Epub 2004/07/13.

    CAS  PubMed  Google Scholar 

  113. Moroni M, Zwart R, Sher E, Cassels BK, Bermudez I. alpha4beta2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol Pharmacol. 2006;70(2):755–68. Epub 2006/05/25.

    CAS  PubMed  Google Scholar 

  114. Nelson ME, Kuryatov A, Choi CH, Zhou Y, Lindstrom J. Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors. Mol Pharmacol. 2003;63(2):332–41. Epub 2003/01/16.

    CAS  PubMed  Google Scholar 

  115. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P, et al. 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. 2007;27(31):8202–18. Epub 2007/08/03.

    CAS  PubMed  Google Scholar 

  116. Papke RL, Trocme-Thibierge C, Guendisch D, Al Rubaiy SA, Bloom SA. Electrophysiological perspectives on the therapeutic use of nicotinic acetylcholine receptor partial agonists. J Pharmacol Exp Ther. 2011;337(2):367–79. Epub 2011/02/03.

    CAS  PubMed Central  PubMed  Google Scholar 

  117. Peng C, Stokes C, Mineur YS, Picciotto MR, Tian C, Eibl C, et al. Differential modulation of brain nicotinic acetylcholine receptor function by cytisine, varenicline, and two novel bispidine compounds: emergent properties of a hybrid molecule. J Pharmacol Exp Ther. 2013;347(2):424–37. Epub 2013/08/21.

    CAS  PubMed Central  PubMed  Google Scholar 

  118. Coe JW, Brooks PR, Vetelino MG, Wirtz MC, Arnold EP, Huang J, et al. Varenicline: an alpha4beta2 nicotinic receptor partial agonist for smoking cessation. J Med Chem. 2005;48(10):3474–7. Epub 2005/05/13.

    CAS  PubMed  Google Scholar 

  119. Mihalak KB, Carroll FI, Luetje CW. Varenicline is a partial agonist at alpha4beta2 and a full agonist at alpha7 neuronal nicotinic receptors. Mol Pharmacol. 2006;70(3):801–5. Epub 2006/06/13.

    CAS  PubMed  Google Scholar 

  120. Papke RL, Heinemann SF. Partial agonist properties of cytisine on neuronal nicotinic receptors containing the beta 2 subunit. Mol Pharmacol. 1994;45(1):142–9. Epub 1994/01/01.

    CAS  PubMed  Google Scholar 

  121. Rollema H, Coe JW, Chambers LK, Hurst RS, Stahl SM, Williams KE. Rationale, pharmacology and clinical efficacy of partial agonists of alpha4beta2 nACh receptors for smoking cessation. Trends Pharmacol Sci. 2007;28(7):316–25. Epub 2007/06/19.

    CAS  PubMed  Google Scholar 

  122. Dajas-Bailador F, Wonnacott S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci. 2004;25(6):317–24. Epub 2004/05/29.

    CAS  PubMed  Google Scholar 

  123. De Filippi G, Baldwinson T, Sher E. Nicotinic receptor modulation of neurotransmitter release in the cerebellum. Prog Brain Res. 2005;148:307–20. Epub 2005/01/22.

    PubMed  Google Scholar 

  124. Hurst R, Rollema H, Bertrand D. Nicotinic acetylcholine receptors: from basic science to therapeutics. Pharmacol Ther. 2013;137(1):22–54. Epub 2012/08/29.

    CAS  PubMed  Google Scholar 

  125. Lawrence JJ. Cholinergic control of GABA release: emerging parallels between neocortex and hippocampus. Trends Neurosci. 2008;31(7):317–27. Epub 2008/06/17.

    CAS  PubMed  Google Scholar 

  126. Marchi M, Grilli M. Presynaptic nicotinic receptors modulating neurotransmitter release in the central nervous system: functional interactions with other coexisting receptors. Prog Neurobiol. 2010;92(2):105–11. Epub 2010/06/19.

    CAS  PubMed  Google Scholar 

  127. Sher E, Chen Y, Sharples TJ, Broad LM, Benedetti G, Zwart R, et al. Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr Top Med Chem. 2004;4(3):283–97. Epub 2004/02/03.

    CAS  PubMed  Google Scholar 

  128. Wonnacott S, Barik J, Dickinson J, Jones IW. Nicotinic receptors modulate transmitter cross talk in the CNS: nicotinic modulation of transmitters. J Mol Neurosci. 2006;30(1–2):137–40. Epub 2006/12/29.

    CAS  PubMed  Google Scholar 

  129. Exley R, Cragg SJ. Presynaptic nicotinic receptors: a dynamic and diverse cholinergic filter of striatal dopamine neurotransmission. Br J Pharmacol. 2008;153 Suppl 1:S283–97. Epub 2007/11/27.

    CAS  PubMed Central  PubMed  Google Scholar 

  130. Livingstone PD, Wonnacott S. Nicotinic acetylcholine receptors and the ascending dopamine pathways. Biochem Pharmacol. 2009;78(7):744–55. Epub 2009/06/16.

    CAS  PubMed  Google Scholar 

  131. Wonnacott S. Gates and filters: unveiling the physiological roles of nicotinic acetylcholine receptors in dopaminergic transmission. Br J Pharmacol. 2008;153 Suppl 1:S2–4. Epub 2008/02/05.

    CAS  PubMed Central  PubMed  Google Scholar 

  132. Azam L, McIntosh JM. Effect of novel alpha-conotoxins on nicotine-stimulated [3H]dopamine release from rat striatal synaptosomes. J Pharmacol Exp Ther. 2005;312(1):231–7. Epub 2004/08/19.

    CAS  PubMed  Google Scholar 

  133. Cui C, Booker TK, Allen RS, Grady SR, Whiteaker P, Marks MJ, et al. The beta3 nicotinic receptor subunit: a component of alpha-conotoxin MII-binding nicotinic acetylcholine receptors that modulate dopamine release and related behaviors. J Neurosci. 2003;23(35):11045–53. Epub 2003/12/06.

    CAS  PubMed  Google Scholar 

  134. Drenan RM, Grady SR, Steele AD, McKinney S, Patzlaff NE, McIntosh JM, et al. Cholinergic modulation of locomotion and striatal dopamine release is mediated by alpha6alpha4* nicotinic acetylcholine receptors. J Neurosci. 2010;30(29):9877–89. Epub 2010/07/28.

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Kulak JM, Nguyen TA, Olivera BM, McIntosh JM. Alpha-conotoxin MII blocks nicotine-stimulated dopamine release in rat striatal synaptosomes. J Neurosci. 1997;17(14):5263–70. Epub 1997/07/15.

    CAS  PubMed  Google Scholar 

  136. Salminen O, Drapeau JA, McIntosh JM, Collins AC, Marks MJ, Grady SR. Pharmacology of alpha-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol Pharmacol. 2007;71(6):1563–71. Epub 2007/03/08.

    CAS  PubMed  Google Scholar 

  137. Salminen O, Murphy KL, McIntosh JM, Drago J, Marks MJ, Collins AC, et al. Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol. 2004;65(6):1526–35. Epub 2004/05/25.

    CAS  PubMed  Google Scholar 

  138. Yang K, Buhlman L, Khan GM, Nichols RA, Jin G, McIntosh JM, et al. Functional nicotinic acetylcholine receptors containing alpha6 subunits are on GABAergic neuronal boutons adherent to ventral tegmental area dopamine neurons. J Neurosci. 2011;31(7):2537–48. Epub 2011/02/18.

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Soll LG, Grady SR, Salminen O, Marks MJ, Tapper AR. A role for alpha4(non-alpha6)* nicotinic acetylcholine receptors in motor behavior. Neuropharmacology. 2013;73:19–30. Epub 2013/05/22.

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Mogg AJ, Whiteaker P, McIntosh JM, Marks M, Collins AC, Wonnacott S. Methyllycaconitine is a potent antagonist of alpha-conotoxin-MII-sensitive presynaptic nicotinic acetylcholine receptors in rat striatum. J Pharmacol Exp Ther. 2002;302(1):197–204. Epub 2002/06/18.

    CAS  PubMed  Google Scholar 

  141. Cohen BN, Mackey ED, Grady SR, McKinney S, Patzlaff NE, Wageman CR, et al. Nicotinic cholinergic mechanisms causing elevated dopamine release and abnormal locomotor behavior. Neuroscience. 2012;200:31–41. Epub 2011/11/15.

    CAS  PubMed  Google Scholar 

  142. Grady SR, Meinerz NM, Cao J, Reynolds AM, Picciotto MR, Changeux JP, et al. Nicotinic agonists stimulate acetylcholine release from mouse interpeduncular nucleus: a function mediated by a different nAChR than dopamine release from striatum. J Neurochem. 2001;76(1):258–68. Epub 2001/01/09.

    CAS  PubMed  Google Scholar 

  143. Grady SR, Murphy KL, Cao J, Marks MJ, McIntosh JM, Collins AC. Characterization of nicotinic agonist-induced [(3)H]dopamine release from synaptosomes prepared from four mouse brain regions. J Pharmacol Exp Ther. 2002;301(2):651–60. Epub 2002/04/19.

    CAS  PubMed  Google Scholar 

  144. Parish CL, Nunan J, Finkelstein DI, McNamara FN, Wong JY, Waddington JL, et al. Mice lacking the alpha4 nicotinic receptor subunit fail to modulate dopaminergic neuronal arbors and possess impaired dopamine transporter function. Mol Pharmacol. 2005;68(5):1376–86. Epub 2005/08/04.

    CAS  PubMed  Google Scholar 

  145. Azam L, McIntosh JM. Characterization of nicotinic acetylcholine receptors that modulate nicotine-evoked [3H]norepinephrine release from mouse hippocampal synaptosomes. Mol Pharmacol. 2006;70(3):967–76. Epub 2006/06/01.

    CAS  PubMed  Google Scholar 

  146. Grilli M, Parodi M, Raiteri M, Marchi M. Chronic nicotine differentially affects the function of nicotinic receptor subtypes regulating neurotransmitter release. J Neurochem. 2005;93(5):1353–60. Epub 2005/06/07.

    CAS  PubMed  Google Scholar 

  147. Scholze P, Orr-Urtreger A, Changeux JP, McIntosh JM, Huck S. Catecholamine outflow from mouse and rat brain slice preparations evoked by nicotinic acetylcholine receptor activation and electrical field stimulation. Br J Pharmacol. 2007;151(3):414–22. Epub 2007/04/03.

    CAS  PubMed Central  PubMed  Google Scholar 

  148. Kaiser S, Wonnacott S. Alpha-bungarotoxin-sensitive nicotinic receptors indirectly modulate [(3)H]dopamine release in rat striatal slices via glutamate release. Mol Pharmacol. 2000;58(2):312–8. Epub 2000/07/25.

    CAS  PubMed  Google Scholar 

  149. Dickinson JA, Kew JN, Wonnacott S. Presynaptic alpha 7- and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol Pharmacol. 2008;74(2):348–59. Epub 2008/05/01.

    CAS  PubMed  Google Scholar 

  150. Livingstone PD, Dickinson JA, Srinivasan J, Kew JN, Wonnacott S. Glutamate-dopamine crosstalk in the rat prefrontal cortex is modulated by Alpha7 nicotinic receptors and potentiated by PNU-120596. J Mol Neurosci. 2010;40(1–2):172–6. Epub 2009/08/19.

    CAS  PubMed  Google Scholar 

  151. Marchi M, Risso F, Viola C, Cavazzani P, Raiteri M. Direct evidence that release-stimulating alpha7* nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J Neurochem. 2002;80(6):1071–8. Epub 2002/04/16.

    CAS  PubMed  Google Scholar 

  152. Marchi M, Zappettini S, Olivero G, Pittaluga A, Grilli M. Chronic nicotine exposure selectively activates a carrier-mediated release of endogenous glutamate and aspartate from rat hippocampal synaptosomes. Neurochem Int. 2012;60(6):622–30. Epub 2012/03/16.

    CAS  PubMed  Google Scholar 

  153. Patti L, Raiteri L, Grilli M, Zappettini S, Bonanno G, Marchi M. Evidence that alpha7 nicotinic receptor modulates glutamate release from mouse neocortical gliosomes. Neurochem Int. 2007;51(1):1–7. Epub 2007/04/28.

    CAS  PubMed  Google Scholar 

  154. Rousseau SJ, Jones IW, Pullar IA, Wonnacott S. Presynaptic alpha7 and non-alpha7 nicotinic acetylcholine receptors modulate [3H]d-aspartate release from rat frontal cortex in vitro. Neuropharmacology. 2005;49(1):59–72. Epub 2005/07/05.

    CAS  PubMed  Google Scholar 

  155. Zappettini S, Grilli M, Lagomarsino F, Cavallero A, Fedele E, Marchi M. Presynaptic nicotinic alpha7 and non-alpha7 receptors stimulate endogenous GABA release from rat hippocampal synaptosomes through two mechanisms of action. PLoS One. 2011;6(2):e16911. Epub 2011/02/25.

    CAS  PubMed Central  PubMed  Google Scholar 

  156. Zappettini S, Grilli M, Olivero G, Mura E, Preda S, Govoni S, et al. Beta amyloid differently modulate nicotinic and muscarinic receptor subtypes which stimulate in vitro and in vivo the release of glycine in the rat hippocampus. Front Pharmacol. 2012;3:146. Epub 2012/08/07.

    PubMed Central  PubMed  Google Scholar 

  157. Zappettini S, Grilli M, Salamone A, Fedele E, Marchi M. Pre-synaptic nicotinic receptors evoke endogenous glutamate and aspartate release from hippocampal synaptosomes by way of distinct coupling mechanisms. Br J Pharmacol. 2010;161(5):1161–71. Epub 2010/07/17.

    CAS  PubMed Central  PubMed  Google Scholar 

  158. Zappettini S, Mura E, Grilli M, Preda S, Salamone A, Olivero G, et al. Different presynaptic nicotinic receptor subtypes modulate in vivo and in vitro the release of glycine in the rat hippocampus. Neurochem Int. 2011;59(5):729–38. Epub 2011/07/19.

    CAS  PubMed  Google Scholar 

  159. Mansvelder HD, Mertz M, Role LW. Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits. Semin Cell Dev Biol. 2009;20(4):432–40. Epub 2009/06/30.

    CAS  PubMed Central  PubMed  Google Scholar 

  160. McKay BE, Placzek AN, Dani JA. Regulation of synaptic transmission and plasticity by neuronal nicotinic acetylcholine receptors. Biochem Pharmacol. 2007;74(8):1120–33. Epub 2007/08/11.

    CAS  PubMed Central  PubMed  Google Scholar 

  161. Yakel JL. Nicotinic ACh receptors in the hippocampus: role in excitability and plasticity. Nicotine Tob Res. 2012;14(11):1249–57. Epub 2012/04/05.

    CAS  PubMed Central  PubMed  Google Scholar 

  162. Jiang L, Role LW. Facilitation of cortico-amygdala synapses by nicotine: activity-dependent modulation of glutamatergic transmission. J Neurophysiol. 2008;99(4):1988–99. Epub 2008/02/15.

    CAS  PubMed Central  PubMed  Google Scholar 

  163. Kalappa BI, Feng L, Kem WR, Gusev AG, Uteshev VV. Mechanisms of facilitation of synaptic glutamate release by nicotinic agonists in the nucleus of the solitary tract. Am J Physiol Cell Physiol. 2011;301(2):C347–61. Epub 2011/05/27.

    CAS  PubMed Central  PubMed  Google Scholar 

  164. Parikh V, Ji J, Decker MW, Sarter M. Prefrontal beta2 subunit-containing and alpha7 nicotinic acetylcholine receptors differentially control glutamatergic and cholinergic signaling. J Neurosci. 2010;30(9):3518–30. Epub 2010/03/06.

    CAS  PubMed Central  PubMed  Google Scholar 

  165. Zhong C, Du C, Hancock M, Mertz M, Talmage DA, Role LW. Presynaptic type III neuregulin 1 is required for sustained enhancement of hippocampal transmission by nicotine and for axonal targeting of alpha7 nicotinic acetylcholine receptors. J Neurosci. 2008;28(37):9111–6. Epub 2008/09/12.

    CAS  PubMed Central  PubMed  Google Scholar 

  166. Barazangi N, Role LW. Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. J Neurophysiol. 2001;86(1):463–74. Epub 2001/06/30.

    CAS  PubMed  Google Scholar 

  167. Radcliffe KA, Fisher JL, Gray R, Dani JA. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci. 1999;868:591–610. Epub 1999/07/22.

    CAS  PubMed  Google Scholar 

  168. Seddik R, Schlichter R, Trouslard J. Modulation of GABAergic synaptic transmission by terminal nicotinic acetylcholine receptors in the central autonomic nucleus of the neonatal rat spinal cord. Neuropharmacology. 2006;51(1):77–89. Epub 2006/05/09.

    CAS  PubMed  Google Scholar 

  169. Exley R, Clements MA, Hartung H, McIntosh JM, Franklin M, Bermudez I, et al. Striatal dopamine transmission is reduced after chronic nicotine with a decrease in alpha6-nicotinic receptor control in nucleus accumbens. Eur J Neurosci. 2013;38:3036–43. Epub 2013/07/12.

    Google Scholar 

  170. Exley R, Maubourguet N, David V, Eddine R, Evrard A, Pons S, et al. Distinct contributions of nicotinic acetylcholine receptor subunit alpha4 and subunit alpha6 to the reinforcing effects of nicotine. Proc Natl Acad Sci U S A. 2011;108(18):7577–82. Epub 2011/04/20.

    CAS  PubMed Central  PubMed  Google Scholar 

  171. Exley R, McIntosh JM, Marks MJ, Maskos U, Cragg SJ. Striatal alpha5 nicotinic receptor subunit regulates dopamine transmission in dorsal striatum. J Neurosci. 2012;32(7):2352–6. Epub 2012/03/08.

    CAS  PubMed Central  PubMed  Google Scholar 

  172. Gao M, Jin Y, Yang K, Zhang D, Lukas RJ, Wu J. Mechanisms involved in systemic nicotine-induced glutamatergic synaptic plasticity on dopamine neurons in the ventral tegmental area. J Neurosci. 2010;30(41):13814–25. Epub 2010/10/15.

    CAS  PubMed Central  PubMed  Google Scholar 

  173. Schilstrom B, Ivanov VB, Wiker C, Svensson TH. Galantamine enhances dopaminergic neurotransmission in vivo via allosteric potentiation of nicotinic acetylcholine receptors. Neuropsychopharmacology. 2007;32(1):43–53. Epub 2006/04/28.

    PubMed  Google Scholar 

  174. Griguoli M, Cellot G, Cherubini E. In hippocampal oriens interneurons anti-Hebbian long-term potentiation requires cholinergic signaling via alpha7 nicotinic acetylcholine receptors. J Neurosci. 2013;33(3):1044–9. Epub 2013/01/18.

    CAS  PubMed  Google Scholar 

  175. Jia Y, Yamazaki Y, Nakauchi S, Ito K, Sumikawa K. Nicotine facilitates long-term potentiation induction in oriens-lacunosum moleculare cells via Ca2+ entry through non-alpha7 nicotinic acetylcholine receptors. Eur J Neurosci. 2010;31(3):463–76. Epub 2010/02/02.

    PubMed Central  PubMed  Google Scholar 

  176. Nakauchi S, Brennan RJ, Boulter J, Sumikawa K. Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2* nicotinic ACh receptors. Eur J Neurosci. 2007;25(9):2666–81. Epub 2007/05/01.

    PubMed  Google Scholar 

  177. Prestori F, Bonardi C, Mapelli L, Lombardo P, Goselink R, De Stefano ME, et al. Gating of long-term potentiation by nicotinic acetylcholine receptors at the cerebellum input stage. PLoS One. 2013;8(5):e64828. Epub 2013/06/07.

    CAS  PubMed Central  PubMed  Google Scholar 

  178. Yamazaki Y, Fujii S, Jia Y, Sumikawa K. Nicotine withdrawal suppresses nicotinic modulation of long-term potentiation induction in the hippocampal CA1 region. Eur J Neurosci. 2006;24(10):2903–16. Epub 2006/12/13.

    PubMed  Google Scholar 

  179. Le Magueresse C, Safiulina V, Changeux JP, Cherubini E. Nicotinic modulation of network and synaptic transmission in the immature hippocampus investigated with genetically modified mice. J Physiol. 2006;576(Pt 2):533–46. Epub 2006/08/12.

    PubMed Central  PubMed  Google Scholar 

  180. Perez XA, Bordia T, McIntosh JM, Quik M. α6ß2* and α4ß2* nicotinic receptors both regulate dopamine signaling with increased nigrostriatal damage: relevance to Parkinson’s disease. Mol Pharmacol. 2010;78(5):971–80. doi:10.1124/mol.110.067561. Epub 2010/08/23.

    CAS  PubMed Central  PubMed  Google Scholar 

  181. Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Lena C, et al. Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci. 2003;23(21):7820–9. Epub 2003/08/29.

    CAS  PubMed  Google Scholar 

  182. Lecca D, Shim I, Costa E, Javaid JI. Striatal application of nicotine, but not of lobeline, attenuates dopamine release in freely moving rats. Neuropharmacology. 2000;39(1):88–98. Epub 2000/02/09.

    CAS  PubMed  Google Scholar 

  183. Marubio LM, Gardier AM, Durier S, David D, Klink R, Arroyo-Jimenez MM, et al. Effects of nicotine in the dopaminergic system of mice lacking the alpha4 subunit of neuronal nicotinic acetylcholine receptors. Eur J Neurosci. 2003;17(7):1329–37. Epub 2003/04/26.

    CAS  PubMed  Google Scholar 

  184. Visanji NP, Mitchell SN, O’Neill MJ, Duty S. Chronic pre-treatment with nicotine enhances nicotine-evoked striatal dopamine release and alpha6 and beta3 nicotinic acetylcholine receptor subunit mRNA in the substantia nigra pars compacta of the rat. Neuropharmacology. 2006;50(1):36–46. Epub 2005/09/13.

    CAS  PubMed  Google Scholar 

  185. Zanetti L, Picciotto MR, Zoli M. Differential effects of nicotinic antagonists perfused into the nucleus accumbens or the ventral tegmental area on cocaine-induced dopamine release in the nucleus accumbens of mice. Psychopharmacology (Berl). 2007;190(2):189–99. Epub 2006/10/25.

    CAS  Google Scholar 

  186. Livingstone PD, Srinivasan J, Kew JN, Dawson LA, Gotti C, Moretti M, et al. alpha7 and non-alpha7 nicotinic acetylcholine receptors modulate dopamine release in vitro and in vivo in the rat prefrontal cortex. Eur J Neurosci. 2009;29(3):539–50. Epub 2009/02/04.

    PubMed  Google Scholar 

  187. Kennett A, Heal DJ, Wonnacott S. Pharmacological differences between rat frontal cortex and hippocampus in the nicotinic modulation of noradrenaline release implicate distinct receptor subtypes. Nicotine Tob Res. 2012;14(11):1339–45. Epub 2012/05/23.

    CAS  PubMed  Google Scholar 

  188. Mura E, Zappettini S, Preda S, Biundo F, Lanni C, Grilli M, et al. Dual effect of beta-amyloid on alpha7 and alpha4beta2 nicotinic receptors controlling the release of glutamate, aspartate and GABA in rat hippocampus. PLoS One. 2012;7(1):e29661. Epub 2012/01/19.

    CAS  PubMed Central  PubMed  Google Scholar 

  189. Bueno-Junior LS, Lopes-Aguiar C, Ruggiero RN, Romcy-Pereira RN, Leite JP. Muscarinic and nicotinic modulation of thalamo-prefrontal cortex synaptic plasticity [corrected] in vivo. PLoS One. 2012;7(10):e47484. Epub 2012/11/03.

    CAS  PubMed Central  PubMed  Google Scholar 

  190. Mao D, Gallagher K, McGehee DS. Nicotine potentiation of excitatory inputs to ventral tegmental area dopamine neurons. J Neurosci. 2011;31(18):6710–20. Epub 2011/05/06.

    CAS  PubMed Central  PubMed  Google Scholar 

  191. Matsuyama S, Matsumoto A, Enomoto T, Nishizaki T. Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. Eur J Neurosci. 2000;12(10):3741–7. Epub 2000/10/13.

    CAS  PubMed  Google Scholar 

  192. Wang Y, Sherwood JL, Lodge D. The alpha4beta2 nicotinic acetylcholine receptor agonist TC-2559 impairs long-term potentiation in the dentate gyrus in vivo. Neurosci Lett. 2006;406(3):183–8. Epub 2006/08/29.

    CAS  PubMed  Google Scholar 

  193. Keighron JD, Ewing AG, Cans AS. Analytical tools to monitor exocytosis: a focus on new fluorescent probes and methods. Analyst. 2012;137(8):1755–63. Epub 2012/02/22.

    CAS  PubMed  Google Scholar 

  194. Klingauf J, Kavalali ET, Tsien RW. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature. 1998;394(6693):581–5. Epub 1998/08/26.

    CAS  PubMed  Google Scholar 

  195. Mani M, Ryan TA. Live imaging of synaptic vesicle release and retrieval in dopaminergic neurons. Front Neural Circuits. 2009;3:3. Epub 2009/06/13.

    PubMed Central  PubMed  Google Scholar 

  196. Moulder KL, Jiang X, Taylor AA, Shin W, Gillis KD, Mennerick S. Vesicle pool heterogeneity at hippocampal glutamate and GABA synapses. J Neurosci. 2007;27(37):9846–54. Epub 2007/09/15.

    CAS  PubMed  Google Scholar 

  197. Welzel O, Henkel AW, Stroebel AM, Jung J, Tischbirek CH, Ebert K, et al. Systematic heterogeneity of fractional vesicle pool sizes and release rates of hippocampal synapses. Biophys J. 2011;100(3):593–601. Epub 2011/02/02.

    CAS  PubMed Central  PubMed  Google Scholar 

  198. Nguyen QT, Schroeder LF, Mank M, Muller A, Taylor P, Griesbeck O, et al. An in vivo biosensor for neurotransmitter release and in situ receptor activity. Nat Neurosci. 2010;13(1):127–32. Epub 2009/12/17.

    CAS  PubMed Central  PubMed  Google Scholar 

  199. Borghuis BG, Marvin JS, Looger LL, Demb JB. Two-photon imaging of nonlinear glutamate release dynamics at bipolar cell synapses in the mouse retina. J Neurosci. 2013;33(27):10972–85. Epub 2013/07/05.

    CAS  PubMed Central  PubMed  Google Scholar 

  200. Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J, et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods. 2013;10(2):162–70. Epub 2013/01/15.

    CAS  PubMed  Google Scholar 

  201. Bouron A, Reuter H. Muscarinic stimulation of synaptic activity by protein kinase C is inhibited by adenosine in cultured hippocampal neurons. Proc Natl Acad Sci U S A. 1997;94(22):12224–9. Epub 1997/10/29.

    CAS  PubMed Central  PubMed  Google Scholar 

  202. Breeze LJ, Vijayaraghavan S. Optical measurements of presynaptic nicotinic effects. Neuropharmacology. 2000;39(13):2706–14. Epub 2000/10/25.

    CAS  PubMed  Google Scholar 

  203. Blumenthal EM, Conroy WG, Romano SJ, Kassner PD, Berg DK. Detection of functional nicotinic receptors blocked by alpha-bungarotoxin on PC12 cells and dependence of their expression on post-translational events. J Neurosci. 1997;17(16):6094–104. Epub 1997/08/15.

    CAS  PubMed  Google Scholar 

  204. Wanamaker CP, Green WN. Endoplasmic reticulum chaperones stabilize nicotinic receptor subunits and regulate receptor assembly. J Biol Chem. 2007;282(43):31113–23. Epub 2007/08/31.

    CAS  PubMed Central  PubMed  Google Scholar 

  205. Alexander JK, Sagher D, Krivoshein AV, Criado M, Jefford G, Green WN. Ric-3 promotes alpha7 nicotinic receptor assembly and trafficking through the ER subcompartment of dendrites. J Neurosci. 2010;30(30):10112–26. Epub 2010/07/30.

    CAS  PubMed Central  PubMed  Google Scholar 

  206. Castillo M, Mulet J, Gutierrez LM, Ortiz JA, Castelan F, Gerber S, et al. Dual role of the RIC-3 protein in trafficking of serotonin and nicotinic acetylcholine receptors. J Biol Chem. 2005;280(29):27062–8. Epub 2005/06/02.

    CAS  PubMed  Google Scholar 

  207. Williams BM, Temburni MK, Levey MS, Bertrand S, Bertrand D, Jacob MH. The long internal loop of the alpha 3 subunit targets nAChRs to subdomains within individual synapses on neurons in vivo. Nat Neurosci. 1998;1(7):557–62. Epub 1999/04/10.

    CAS  PubMed  Google Scholar 

  208. Fernandes CC, Berg DK, Gomez-Varela D. Lateral mobility of nicotinic acetylcholine receptors on neurons is determined by receptor composition, local domain, and cell type. J Neurosci. 2010;30(26):8841–51. Epub 2010/07/02.

    CAS  PubMed Central  PubMed  Google Scholar 

  209. Temburni MK, Rosenberg MM, Pathak N, McConnell R, Jacob MH. Neuronal nicotinic synapse assembly requires the adenomatous polyposis coli tumor suppressor protein. J Neurosci. 2004;24(30):6776–84. Epub 2004/07/30.

    CAS  PubMed  Google Scholar 

  210. Cheng SB, Amici SA, Ren XQ, McKay SB, Treuil MW, Lindstrom JM, et al. Presynaptic targeting of alpha4beta 2 nicotinic acetylcholine receptors is regulated by neurexin-1beta. J Biol Chem. 2009;284(35):23251–9. Epub 2009/07/02.

    CAS  PubMed Central  PubMed  Google Scholar 

  211. Fischer H, Orr-Urtreger A, Role LW, Huck S. Selective deletion of the alpha5 subunit differentially affects somatic-dendritic versus axonally targeted nicotinic ACh receptors in mouse. J Physiol. 2005;563(Pt 1):119–37. Epub 2004/12/22.

    CAS  PubMed Central  PubMed  Google Scholar 

  212. Zhong C, Talmage DA, Role LW. Nicotine elicits prolonged calcium signaling along ventral hippocampal axons. PLoS One. 2013;8(12):e82719.

    PubMed Central  PubMed  Google Scholar 

  213. Chen YJ, Johnson MA, Lieberman MD, Goodchild RE, Schobel S, Lewandowski N, et al. Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. J Neurosci. 2008;28(27):6872–83. Epub 2008/07/04.

    CAS  PubMed Central  PubMed  Google Scholar 

  214. Jiang L, Emmetsberger J, Talmage DA, Role LW. Type III neuregulin 1 is required for multiple forms of excitatory synaptic plasticity of mouse cortico-amygdala circuits. J Neurosci. 2013;33(23):9655–66. Epub 2013/06/07.

    CAS  PubMed Central  PubMed  Google Scholar 

  215. Hancock ML, Canetta SE, Role LW, Talmage DA. Presynaptic type III neuregulin1-ErbB signaling targets {alpha}7 nicotinic acetylcholine receptors to axons. J Cell Biol. 2008;181(3):511–21. Epub 2008/05/07.

    CAS  PubMed Central  PubMed  Google Scholar 

  216. Gomez-Varela D, Berg DK. Lateral mobility of presynaptic alpha7-containing nicotinic receptors and its relevance for glutamate release. J Neurosci. 2013;33(43):17062–71. Epub 2013/10/25.

    CAS  PubMed Central  PubMed  Google Scholar 

  217. Gu Z, Lamb PW, Yakel JL. Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. J Neurosci. 2012;32(36):12337–48. Epub 2012/09/08.

    CAS  PubMed Central  PubMed  Google Scholar 

  218. del Barrio L, Egea J, Leon R, Romero A, Ruiz A, Montero M, et al. Calcium signalling mediated through alpha7 and non-alpha7 nAChR stimulation is differentially regulated in bovine chromaffin cells to induce catecholamine release. Br J Pharmacol. 2011;162(1):94–110. Epub 2010/09/16.

    PubMed Central  PubMed  Google Scholar 

  219. Gilbert D, Lecchi M, Arnaudeau S, Bertrand D, Demaurex N. Local and global calcium signals associated with the opening of neuronal alpha7 nicotinic acetylcholine receptors. Cell Calcium. 2009;45(2):198–207. Epub 2008/11/29.

    CAS  PubMed  Google Scholar 

  220. Szabo SI, Zelles T, Vizi ES, Lendvai B. The effect of nicotine on spiking activity and Ca2+ dynamics of dendritic spines in rat CA1 pyramidal neurons. Hippocampus. 2008;18(4):376–85. Epub 2008/01/15.

    CAS  PubMed  Google Scholar 

  221. Fayuk D, Yakel JL. Ca2+ permeability of nicotinic acetylcholine receptors in rat hippocampal CA1 interneurones. J Physiol. 2005;566(Pt 3):759–68. Epub 2005/06/04.

    CAS  PubMed Central  PubMed  Google Scholar 

  222. Fucile S. Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium. 2004;35(1):1–8. Epub 2003/12/13.

    CAS  PubMed  Google Scholar 

  223. Dajas-Bailador FA, Mogg AJ, Wonnacott S. Intracellular Ca2+ signals evoked by stimulation of nicotinic acetylcholine receptors in SH-SY5Y cells: contribution of voltage-operated Ca2+ channels and Ca2+ stores. J Neurochem. 2002;81(3):606–14. Epub 2002/06/18.

    CAS  PubMed  Google Scholar 

  224. Dajas-Bailador FA, Soliakov L, Wonnacott S. 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. 2002;80(3):520–30. Epub 2002/03/22.

    CAS  PubMed  Google Scholar 

  225. Sharma G, Vijayaraghavan S. Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci U S A. 2001;98(7):4148–53. Epub 2001/03/22.

    CAS  PubMed Central  PubMed  Google Scholar 

  226. Sharma G, Vijayaraghavan S. Nicotinic receptors containing the alpha7 subunit: a model for rational drug design. Curr Med Chem. 2008;15(28):2921–32. Epub 2008/12/17.

    CAS  PubMed Central  PubMed  Google Scholar 

  227. Welsby P, Rowan M, Anwyl R. 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. 2006;24(11):3109–18. Epub 2006/12/13.

    PubMed  Google Scholar 

  228. Cox ME, Parsons SJ. Roles for protein kinase C and mitogen-activated protein kinase in nicotine-induced secretion from bovine adrenal chromaffin cells. J Neurochem. 1997;69(3):1119–30. Epub 1997/09/01.

    CAS  PubMed  Google Scholar 

  229. Kihara T, Shimohama S, Sawada H, Honda K, Nakamizo T, Shibasaki H, et al. alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity. J Biol Chem. 2001;276(17):13541–6. Epub 2001/03/30.

    CAS  PubMed  Google Scholar 

  230. Dineley KT, Westerman M, Bui D, Bell K, Ashe KH, Sweatt JD. Beta-amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors: In vitro and in vivo mechanisms related to Alzheimer’s disease. J Neurosci. 2001;21(12):4125–33. Epub 2001/06/19.

    CAS  PubMed  Google Scholar 

  231. Chang KT, Berg DK. Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons. Neuron. 2001;32(5):855–65. Epub 2001/12/12.

    CAS  PubMed  Google Scholar 

  232. Damaj MI. Nicotinic regulation of calcium/calmodulin-dependent protein kinase II activation in the spinal cord. J Pharmacol Exp Ther. 2007;320(1):244–9. Epub 2006/10/17.

    CAS  PubMed  Google Scholar 

  233. Salin PA, Scanziani M, Malenka RC, Nicoll RA. Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci U S A. 1996;93(23):13304–9. Epub 1996/11/12.

    CAS  PubMed Central  PubMed  Google Scholar 

  234. Wang BW, Liao WN, Chang CT, Wang SJ. Facilitation of glutamate release by nicotine involves the activation of a Ca2+/calmodulin signaling pathway in rat prefrontal cortex nerve terminals. Synapse. 2006;59(8):491–501. Epub 2006/03/28.

    CAS  PubMed  Google Scholar 

  235. Nordman JC, Kabbani N. An interaction between alpha7 nicotinic receptors and a G-protein pathway complex regulates neurite growth in neural cells. J Cell Sci. 2012;125(Pt 22):5502–13. Epub 2012/09/08.

    CAS  PubMed  Google Scholar 

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Zhong, C., López-Hernández, G.Y., Talmage, D.A., Role, L.W. (2014). Presynaptic Nicotinic Acetylcholine Receptors and the Modulation of Circuit Excitability. In: Lester, R. (eds) Nicotinic Receptors. The Receptors, vol 26. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-1167-7_7

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