Age-related changes in nicotine response of cholinergic and non-cholinergic laterodorsal tegmental neurons: Implications for the heightened adolescent susceptibility to nicotine addiction

Neuropharmacology

Volumn 85, Issue , 2014, Pages 263-283

  Christensen, Mark H ^a   Ishibashi, Masaru ^b   Nielsen, Michael L ^a   Leonard, Christopher S ^b   Kohlmeier, Kristi A ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Electrophysiology; LDT; Mouse; REM sleep

Indexed keywords

CALCIUM; NICOTINE; CATION; NICOTINIC AGENT;

AFTERHYPERPOLARIZATION; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; BRAIN; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DRUG SENSITIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; LATERODORSAL TEGMENTAL NUCLEUS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NONHUMAN; ONTOGENY; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; TOBACCO DEPENDENCE; WHOLE CELL PATCH CLAMP; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; IMPEDANCE; METABOLISM; MINIATURE ENDPLATE POTENTIAL; NERVE CELL; PHYSIOLOGY; TEGMENTUM; TISSUE CULTURE TECHNIQUE;

ACTION POTENTIALS; AGING; ANIMALS; CALCIUM; CATIONS; CHOLINERGIC NEURONS; ELECTRIC IMPEDANCE; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, INBRED C57BL; MINIATURE POSTSYNAPTIC POTENTIALS; NEURONS; NICOTINE; NICOTINIC AGONISTS; TEGMENTUM MESENCEPHALI; TISSUE CULTURE TECHNIQUES;

EID: 84902594612     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.05.010     Document Type: Article

References (106)

1. E.X. Albuquerque, E.F. Pereira, M. Alkondon, and S.W. Rogers Mammalian nicotinic acetylcholine receptors: from structure to function Physiol. Rev. 89 2009 73 120
2. M. Alkondon, and E.X. Albuquerque Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes J. Pharmacol. Exp. Ther. 265 1993 1455 1473 (Pubitemid 23321055)
3. M. Alkondon, E.F. Pereira, S. Wonnacott, and E.X. Albuquerque Blockade of nicotinic currents in hippocampal neurons defines methyllycaconitine as a potent and specific receptor antagonist Mol. Pharmacol. 41 1992 802 808 (Pubitemid 23021472)
4. American Psychiatric Association D-V Diagnostic and Statistical Manual of Mental Disorders fifth ed. 2013 DSM-V
5. L. Azam, Y. Chen, and F.M. Leslie Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons Neuroscience 144 2007 1347 1360 (Pubitemid 46123818)
6. L. Azam, U. Winzer-Serhan, and F.M. Leslie Co-expression of alpha7 and beta2 nicotinic acetylcholine receptor subunit mRNAs within rat brain cholinergic neurons Neuroscience 119 2003 965 977 (Pubitemid 36776447)
7. J. Baumgold, I. Zimmerman, and L. Bambrick Appearance of [3H]saxitoxin binding sites in developing rat brain Brain Res. 285 1983 405 407 (Pubitemid 13050186)
8. S.A. Bayer, J. Altman, R.J. Russo, and X. Zhang Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat Neurotoxicology 14 1993 83 144 (Pubitemid 23195769)
9. Y. Ben-Ari Excitatory actions of gaba during development: the nature of the nurture Nat. Rev. Neurosci. 3 2002 728 739 (Pubitemid 135706678)
10. M.J. Berridge Neuronal calcium signaling Neuron 21 1998 13 26 (Pubitemid 28355688)
11. M. Biel, C. Wahl-Schott, S. Michalakis, and X. Zong Hyperpolarization- activated cation channels: from genes to function Physiol. Rev. 89 2009 847 885
12. C.D. Blaha, L.F. Allen, S. Das, W.L. Inglis, M.P. Latimer, S.R. Vincent, and P. Winn Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats J. Neurosci. 16 1996 714 722
13. S. Boucetta, and B.E. Jones Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats J. Neurosci. 29 2009 4664 4674
14. J. Chen, and W.J. Millar Age of smoking initiation: implications for quitting Health Rep. 9 1998 39 46
15. W.A. Corrigall, K.M. Coen, and K.L. Adamson Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area Brain Res. 653 1994 278 284 (Pubitemid 24252850)
16. W.A. Corrigall, K.B. Franklin, K.M. Coen, and P.B. Clarke The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine Psychopharmacol. Berl. 107 1992 285 289
17. F. Couraud, N. Martin-Moutot, A. Koulakoff, and Y. Berwald-Netter Neurotoxin-sensitive sodium channels in neurons developing in vivo and in vitro J. Neurosci. 6 1986 192 198 (Pubitemid 16149232)
18. D. Dautan, I. Huerta-Ocampo, I.B. Witten, K. Deisseroth, J.P. Bolam, T. Gerdjikov, and J. Mena-Segovia A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem J. Neurosci. 34 2014 4509 4518
19. J.R. DiFranza Hooked from the first cigarette Sci. Am. 298 2008 82 87 (Pubitemid 351917813)
20. J.R. DiFranza, N.A. Rigotti, A.D. McNeill, J.K. Ockene, J.A. Savageau, C.D. St, and M. Coleman Initial symptoms of nicotine dependence in adolescents Tob. Control 9 2000 313 319
21. J.R. DiFranza, M. Sweet, J. Savageau, and W.W. Ursprung An evaluation of a clinical approach to staging tobacco addiction J. Pediatr. 159 2011 999 1003
22. J. Dobbing, and J. Sands Comparative aspects of the brain growth spurt Early Hum. Dev. 3 1979 79 83 (Pubitemid 9141710)
23. T.L. Doremus-Fitzwater, E.I. Varlinskaya, and L.P. Spear Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors Brain Cogn. 72 2010 114 123
24. W.C. Drevets, C. Gautier, J.C. Price, D.J. Kupfer, P.E. Kinahan, A.A. Grace, J.L. Price, and C.A. Mathis Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria Biol. Psychiatry 49 2001 81 96 (Pubitemid 32119502)
25. J.B. Dwyer, S.C. McQuown, and F.M. Leslie The dynamic effects of nicotine on the developing brain Pharmacol. Ther. 122 2009 125 139
26. A. Erisir, D. Lau, B. Rudy, and C.S. Leonard Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons J. Neurophysiol. 82 1999 2476 2489
27. C.P. Fenster, M.F. Rains, B. Noerager, M.W. Quick, and R.A. Lester Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine J. Neurosci. 17 1997 5747 5759 (Pubitemid 27310490)
28. J.C. Fiala, M. Feinberg, V. Popov, and K.M. Harris Synaptogenesis via dendritic filopodia in developing hippocampal area CA1 J. Neurosci. 18 1998 8900 8911 (Pubitemid 28491754)
29. S.B. Floresco, A.R. West, B. Ash, H. Moore, and A.A. Grace Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission Nat. Neurosci. 6 2003 968 973 (Pubitemid 37064759)
30. G.L. Forster, and C.D. Blaha Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area Eur. J. Neurosci. 12 2000 3596 3604
31. G.L. Forster, J.S. Yeomans, J. Takeuchi, and C.D. Blaha M5 muscarinic receptors are required for prolonged accumbal dopamine release after electrical stimulation of the pons in mice J. Neurosci. 22 2002 RC190
32. M. Gao, Y. Jin, K. Yang, D. Zhang, R.J. Lukas, and J. Wu Mechanisms involved in systemic nicotine-induced glutamatergic synaptic plasticity on dopamine neurons in the ventral tegmental area J. Neurosci. 30 2010 13814 13825
33. C.H. Good, K.D. Bay, R.A. Buchanan, K.A. McKeon, R.D. Skinner, and E. Garcia-Rill Prenatal exposure to cigarette smoke affects the physiology of pedunculopontine nucleus (PPN) neurons in development Neurotoxicol Teratol. 28 2006 210 219
34. A.A. Grace, and S.P. Onn Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro J. Neurosci. 9 1989 3463 3481 (Pubitemid 19260019)
35. M. Griguoli, A. Maul, C. Nguyen, A. Giorgetti, P. Carloni, and E. Cherubini Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculare interneurons J. Neurosci. 30 2010 10773 10783
36. B. Gronier, and K. Rasmussen Activation of midbrain presumed dopaminergic neurones by muscarinic cholinergic receptors: an in vivo electrophysiological study in the rat Br. J. Pharmacol. 124 1998 455 464 (Pubitemid 28254500)
37. K.M. Harris, F.E. Jensen, and B. Tsao Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation J. Neurosci. 12 1992 2685 2705
38. J.R. Huguenard, O.P. Hamill, and D.A. Prince Developmental changes in Na+ conductances in rat neocortical neurons: appearance of a slowly inactivating component J. Neurophysiol. 59 1988 778 795
39. S. Ikemoto, and R.A. Wise Rewarding effects of the cholinergic agents carbachol and neostigmine in the posterior ventral tegmental area J. Neurosci. 22 2002 9895 9904 (Pubitemid 35332874)
40. M. Ishibashi, C.S. Leonard, and K.A. Kohlmeier Nicotinic activation of laterodorsal tegmental neurons: implications for addiction to nicotine Neuropsychopharmacology 34 2009 2529 2547
41. H.G. Jia, J. Yamuy, S. Sampogna, F.R. Morales, and M.H. Chase Colocalization of gamma-aminobutyric acid and acetylcholine in neurons in the laterodorsal and pedunculopontine tegmental nuclei in the cat: a light and electron microscopic study Brain Res. 992 2003 205 219 (Pubitemid 37415103)
42. T. Kanyshkova, M. Pawlowski, P. Meuth, C. Dube, R.A. Bender, A.L. Brewster, A. Baumann, T.Z. Baram, H.C. Pape, and T. Budde Postnatal expression pattern of HCN channel isoforms in thalamic neurons: relationship to maturation of thalamocortical oscillations J. Neurosci. 29 2009 8847 8857
43. H. Kawai, R. Lazar, and R. Metherate Nicotinic control of axon excitability regulates thalamocortical transmission Nat. Neurosci. 10 2007 1168 1175 (Pubitemid 47339954)
44. K.S. Kendler, J. Myers, M.I. Damaj, and X. Chen Early smoking onset and risk for subsequent nicotine dependence: a monozygotic co-twin control study Am. J. Psychiatry 170 2013 408 413
45. G.A. Kerchner, and R.A. Nicoll Silent synapses and the emergence of a postsynaptic mechanism for LTP Nat. Rev. Neurosci. 9 2008 813 825
46. T. Kobayashi, C. Good, J. Biedermann, C. Barnes, R.D. Skinner, and E. Garcia-Rill Developmental changes in pedunculopontine nucleus (PPN) neurons J. Neurophysiol. 91 2004 1470 1481 (Pubitemid 38339319)
47. K.A. Kohlmeier, M.H. Christensen, M.P. Kristensen, and U. Kristiansen Pharmacological evidence of functional inhibitory metabotrophic glutamate receptors on mouse arousal-related cholinergic laterodorsal tegmental neurons Neuropharmacology 66 2013 99 113
48. K.A. Kohlmeier, T. Inoue, and C.S. Leonard Hypocretin/orexin peptide signaling in the ascending arousal system: elevation of intracellular calcium in the mouse dorsal raphe and laterodorsal tegmentum J. Neurophysiol. 92 2004 221 235 (Pubitemid 38802246)
49. M.P. Kristensen, and C.S. Leonard Electrophysiological Properties of Laterodorsal Tegmental Nucleus (LDT) Neurons from the Developing Mouse: Excitability, Typology, Nitric Oxide Synthase (bNOS) Immunoreactivity and the Relation to Published Data from Other Species November 2007 Society for Neuroscience Annual Meeting San Diego, USA
50. C.R. Kuhlmann, J.R. Trumper, H. Tillmanns, S.C. Alexander, and A. Erdogan Nicotine inhibits large conductance Ca(2+)-activated K(+) channels and the NO/-cGMP signaling pathway in cultured human endothelial cells Scand. Cardiovasc J. 39 2005 348 352 (Pubitemid 43135196)
51. R. Kurosawa, N. Taoka, F. Shinohara, M. Minami, and K. Kaneda Cocaine exposure enhances excitatory synaptic drive to cholinergic neurons in the laterodorsal tegmental nucleus Eur. J. Neurosci. 2013 doi: 10.1111 epub ahead of print
52. M.G. Lacey, P. Calabresi, and R.A. North Muscarine depolarizes rat substantia nigra zona compacta and ventral tegmental neurons in vitro through M1-like receptors J. Pharmacol. Exp. Ther. 253 1990 395 400 (Pubitemid 20141527)
53. S. Lammel, B.K. Lim, C. Ran, K.W. Huang, M.J. Betley, K.M. Tye, K. Deisseroth, and R.C. Malenka Input-specific control of reward and aversion in the ventral tegmental area Nature 491 2012 212 217
54. L. Liu, W. Zhu, Z.S. Zhang, T. Yang, A. Grant, G. Oxford, and S.A. Simon Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors J. Neurophysiol. 91 2004 1482 1491 (Pubitemid 38339320)
55. X.B. Liu, L.K. Low, E.G. Jones, and H.J. Cheng Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus J. Neurosci. 25 2005 9124 9134 (Pubitemid 41500820)
56. D.J. Lodge, and A.A. Grace The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons Proc. Natl. Acad. Sci. U. S. a. 103 2006 5167 5172
57. R. Lujan, R. Shigemoto, and G. Lopez-Bendito Glutamate and GABA receptor signalling in the developing brain Neuroscience 130 2005 567 580 (Pubitemid 39601430)
58. L. Ma, Y.M. Wu, Y.Y. Guo, Q. Yang, B. Feng, Q. Song, S.B. Liu, D.Q. Zhao, and M.G. Zhao Nicotine addiction reduces the large-conductance Ca(2+)-activated potassium channels expression in the nucleus accumbens Neuromolecular Med. 15 2013 227 237
59. S.H. Macdonald, P. Ruth, H.G. Knaus, and M.J. Shipston Increased large conductance calcium-activated potassium (BK) channel expression accompanied by STREX variant downregulation in the developing mouse CNS BMC Dev. Biol. 6 2006 37
60. J. Mackay, and J. Crofton Tobacco and the developing world Br. Med. Bull. 52 1996 206 221 (Pubitemid 26039060)
61. M. Mameli-Engvall, A. Evrard, S. Pons, U. Maskos, T.H. Svensson, J.P. Changeux, and P. Faure Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors Neuron 50 2006 911 921 (Pubitemid 43850688)
62. H.D. Mansvelder, J.R. Keath, and D.S. McGehee Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas Neuron 33 2002 905 919 (Pubitemid 34246356)
63. D.A. McCormick, and D.A. Prince Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones J. Physiol. 393 1987 743 762 (Pubitemid 18092373)
64. M. Melis, S. Scheggi, G. Carta, C. Madeddu, S. Lecca, A. Luchicchi, F. Cadeddu, R. Frau, L. Fattore, P. Fadda, M.G. Ennas, M.P. Castelli, W. Fratta, B. Schilstrom, S. Banni, M.G. De Montis, and M. Pistis PPARalpha regulates cholinergic-driven activity of midbrain dopamine neurons via a novel mechanism involving alpha7 nicotinic acetylcholine receptors J. Neurosci. 33 2013 6203 6211
65. H. Miao, C. Liu, K. Bishop, Z.H. Gong, A. Nordberg, and X. Zhang Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain J. Neurochem. 70 1998 752 762 (Pubitemid 28079366)
66. M. Mieda, E. Hasegawa, Y.Y. Kisanuki, C.M. Sinton, M. Yanagisawa, and T. Sakurai Differential roles of orexin receptor-1 and -2 in the regulation of non-REM and REM sleep J. Neurosci. 31 2011 6518 6526
67. A.D. Miller, and C.D. Blaha Midbrain muscarinic receptor mechanisms underlying regulation of mesoaccumbens and nigrostriatal dopaminergic transmission in the rat Eur. J. Neurosci. 21 2005 1837 1846 (Pubitemid 40685864)
68. C.L. Nelson, J.B. Wetter, M. Milovanovic, and M.E. Wolf The laterodorsal tegmentum contributes to behavioral sensitization to amphetamine Neuroscience 146 2007 41 49 (Pubitemid 46654610)
69. M.E. Nelson, A. Kuryatov, C.H. Choi, Y. Zhou, and J. Lindstrom Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors Mol. Pharmacol. 63 2003 332 341 (Pubitemid 36158368)
70. Y. Ninomiya, Y. Kayama, and Y. Koyama Postnatal development of cholinergic neurons in the mesopontine tegmentum revealed by histochemistry Int. J. Dev. Neurosci. 23 2005 711 721 (Pubitemid 41674510)
71. Z. Nusser, S. Cull-Candy, and M. Farrant Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude Neuron 19 1997 697 709 (Pubitemid 27430755)
72. T.J. Nutter, and D.J. Adams Monovalent and divalent cation permeability and block of neuronal nicotinic receptor channels in rat parasympathetic ganglia J. Gen. Physiol. 105 1995 701 723
73. S.A. Oakman, P.L. Faris, P.E. Kerr, C. Cozzari, and B.K. Hartman Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area J. Neurosci. 15 1995 5859 5869
74. N. Omelchenko, and S.R. Sesack Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area J. Comp. Neurol. 483 2005 217 235 (Pubitemid 40189799)
75. N. Omelchenko, and S.R. Sesack Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons J. Comp. Neurol. 494 2006 863 875 (Pubitemid 43063984)
76. V.I. Pidoplichko, M. DeBiasi, J.T. Williams, and J.A. Dani Nicotine activates and desensitizes midbrain dopamine neurons Nature 390 1997 401 404 (Pubitemid 28027320)
77. V.I. Pidoplichko, J. Noguchi, O.O. Areola, Y. Liang, J. Peterson, T. Zhang, and J.A. Dani Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction Learn Mem. 11 2004 60 69 (Pubitemid 38167059)
78. A.N. Placzek, T.A. Zhang, and J.A. Dani Age dependent nicotinic influences over dopamine neuron synaptic plasticity Biochem Pharmacol. 78 2009 686 692
79. F.E. Pontieri, G. Tanda, and C.G. Di Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens Proc. Natl. Acad. Sci. U. S. A 92 1995 12304 12308
80. F.E. Pontieri, G. Tanda, F. Orzi, and C.G. Di Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs Nature 382 1996 255 257 (Pubitemid 26251360)
81. M.W. Quick, and R.A. Lester Desensitization of neuronal nicotinic receptors J. Neurobiol. 53 2002 457 478 (Pubitemid 35375579)
82. A.S. Ramoa, and D.A. McCormick Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections J. Neurosci. 14 1994 2089 2097 (Pubitemid 24108118)
83. D. Saal, Y. Dong, A. Bonci, and R.C. Malenka Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons Neuron 37 2003 577 582 (Pubitemid 36262980)
84. B. Schilstrom, N. Rawal, M. Mameli-Engvall, G.G. Nomikos, and T.H. Svensson Dual effects of nicotine on dopamine neurons mediated by different nicotinic receptor subtypes Int. J. Neuropsychopharmacol. 6 2003 1 11 (Pubitemid 36373095)
85. R. Scragg, R.J. Wellman, M. Laugesen, and J.R. DiFranza Diminished autonomy over tobacco can appear with the first cigarettes Addict. Behav. 33 2008 689 698
86. J.X. Shen, and J.L. Yakel Nicotinic acetylcholine receptor-mediated calcium signaling in the nervous system Acta Pharmacol. Sin. 30 2009 673 680
87. S. Shiffman, J.A. Paty, M. Gnys, J.D. Kassel, and C. Elash Nicotine withdrawal in chippers and regular smokers: subjective and cognitive effects Health Psychol. 14 1995 301 309
88. C. Simon, A. Hayar, and E. Garcia-Rill Responses of developing pedunculopontine neurons to glutamate receptor agonists J. Neurophysiol. 105 2011 1918 1931
89. E.T. Stoneham, E.M. Sanders, M. Sanyal, and T.C. Dumas Rules of engagement: factors that regulate activity-dependent synaptic plasticity during neural network development Biol. Bull. 219 2010 81 99
90. S. Tolu, R. Eddine, F. Marti, V. David, M. Graupner, S. Pons, M. Baudonnat, M. Husson, M. Besson, C. Reperant, J. Zemdegs, C. Pages, Y.A. Hay, B. Lambolez, J. Caboche, B. Gutkin, A.M. Gardier, J.P. Changeux, P. Faure, and U. Maskos Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement Mol. Psychiatry 18 2013 382 393
91. R.Y. Tsien A non-disruptive technique for loading calcium buffers and indicators into cells Nature 290 1981 527 528 (Pubitemid 11159085)
92. E.T. Tzavara, F.P. Bymaster, R.J. Davis, M.R. Wade, K.W. Perry, J. Wess, D.L. McKinzie, C. Felder, and G.G. Nomikos M4 muscarinic receptors regulate the dynamics of cholinergic and dopaminergic neurotransmission: relevance to the pathophysiology and treatment of related CNS pathologies FASEB J. 18 2004 1410 1412 (Pubitemid 39561597)
93. D.V. Vasilyev, and M.E. Barish Postnatal development of the hyperpolarization-activated excitatory current Ih in mouse hippocampal pyramidal neurons J. Neurosci. 22 2002 8992 9004 (Pubitemid 35379069)
94. M.T. Vilaro, J.M. Palacios, and G. Mengod Localization of m5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry Neurosci. Lett. 114 1990 154 159 (Pubitemid 20188950)
95. S.R. Vincent, and H. Kimura Histochemical mapping of nitric oxide synthase in the rat brain Neuroscience 46 1992 755 784
96. S.R. Vincent, K. Satoh, D.M. Armstrong, and H.C. Fibiger NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation Neurosci. Lett. 43 1983 31 36 (Pubitemid 14224425)
97. H. Wang, H. Shi, and Z. Wang Nicotine depresses the functions of multiple cardiac potassium channels Life Sci. 65 1999 L143 L149
98. H. Wang, H. Shi, L. Zhang, M. Pourrier, B. Yang, S. Nattel, and Z. Wang Nicotine is a potent blocker of the cardiac A-type K(+) channels. Effects on cloned Kv4.3 channels and native transient outward current Circulation 102 2000 1165 1171
99. H. Wang, B. Yang, L. Zhang, D. Xu, and Z. Wang Direct block of inward rectifier potassium channels by nicotine Toxicol. Appl. Pharmacol. 164 2000 97 101 (Pubitemid 30198549)
100. H.L. Wang, and M. Morales Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat Eur. J. Neurosci. 29 2009 340 358
101. A.V. Wilkinson, M.B. Schabath, A.V. Prokhorov, and M.R. Spitz Age-related differences in factors associated with smoking initiation Cancer Causes Control 18 2007 635 644 (Pubitemid 46883681)
102. J.R. Wooltorton, V.I. Pidoplichko, R.S. Broide, and J.A. Dani Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas J. Neurosci. 23 2003 3176 3185
103. J.S. Yeomans, O. Kofman, and V. McFarlane Cholinergic involvement in lateral hypothalamic rewarding brain stimulation Brain Res. 329 1985 19 26 (Pubitemid 15142217)
104. J.S. Yeomans, J. Takeuchi, M. Baptista, D.D. Flynn, K. Lepik, J. Nobrega, J. Fulton, and M.R. Ralph Brain-stimulation reward thresholds raised by an antisense oligonucleotide for the M5 muscarinic receptor infused near dopamine cells J. Neurosci. 20 2000 8861 8867
105. C.L. Zhang, Y. Verbny, S.A. Malek, P.K. Stys, and S.Y. Chiu Nicotinic acetylcholine receptors in mouse and rat optic nerves J. Neurophysiol. 91 2004 1025 1035 (Pubitemid 38168869)
106. X. Zhang, C. Liu, H. Miao, Z.H. Gong, and A. Nordberg Postnatal changes of nicotinic acetylcholine receptor alpha 2, alpha 3, alpha 4, alpha 7 and beta 2 subunits genes expression in rat brain Int. J. Dev. Neurosci. 16 1998 507 518 (Pubitemid 28555718)