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Electrophysiological changes in laterodorsal tegmental neurons associated with prenatal nicotine exposure: implications for heightened susceptibility to addict to drugs of abuse

Published online by Cambridge University Press:  23 October 2014

M. H. Christensen ,
M. L. Nielsen  and
K. A. Kohlmeier
M. H. Christensen
Affiliation:
Department of Drug design and Pharmacology, Faculty of Health Sciences, University of Copenhagen, Denmark
M. L. Nielsen
Affiliation:
Department of Drug design and Pharmacology, Faculty of Health Sciences, University of Copenhagen, Denmark
K. A. Kohlmeier*
Affiliation:
Department of Drug design and Pharmacology, Faculty of Health Sciences, University of Copenhagen, Denmark
*
*Address for correspondence: K. A. Kohlmeier, Department of Drug Design and Pharmacology, Faculty of Health Sciences, Universitetsparken 2, University of Copenhagen, Copenhagen 2100, Denmark. (Email [email protected])
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Abstract

Prenatal nicotine exposure (PNE) is a risk factor for developing an addiction to nicotine at a later stage in life. Understanding the neurobiological changes in reward related circuitry induced by exposure to nicotine prenatally is vital if we are to combat the heightened addiction liability in these vulnerable individuals. The laterodorsal tegmental nucleus (LDT), which is comprised of cholinergic, GABAergic and glutamatergic neurons, is importantly involved in reward mediation via demonstrated excitatory projections to dopamine-containing ventral tegmental neurons. PNE could lead to alterations in LDT neurons that would be expected to alter responses to later-life nicotine exposure. To examine this issue, we monitored nicotine-induced responses of LDT neurons in brain slices of PNE and drug naive mice using calcium imaging and whole-cell patch clamping. Nicotine was found to induce rises in calcium in a smaller proportion of LDT cells in PNE mice aged 7–15 days and smaller rises in calcium in PNE animals from postnatal ages 11–21 days when compared with age-matched control animals. While inward currents induced by nicotine were not found to be different, nicotine did induce larger amplitude excitatory postsynaptic currents in PNE animals in the oldest age group when compared with amplitudes induced in similar-aged control animals. Immunohistochemically identified cholinergic LDT cells from PNE animals exhibited slower spike rise and decay slopes, which likely contributed to the wider action potential observed. Further, PNE was associated with a more negative action potential afterhyperpolarization in cholinergic cells. Interestingly, the changes found in these parameters in animals exposed prenatally to nicotine were age related, in that they were not apparent in animals from the oldest age group examined. Taken together, our data suggest that PNE induces changes in cholinergic LDT cells that would be expected to alter cellular excitability. As the changes are age related, these PNE-associated alterations could contribute differentially across ontogeny to nicotine-mediated reward and may contribute to the particular susceptibility of in utero nicotine exposed individuals to addict to nicotine upon nicotine exposure in the juvenile period.

Keywords

addictionLDTREM sleepmouse
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 6 , Issue 3 , June 2015 , pp. 182 - 200
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1. Egebjerg, JK, Jensen, A, Nohr, B, Kruger, KS. Do pregnant women still smoke? A study of smoking patterns among 261,029 primiparous women in Denmark 1997–2005. Acta Obstet Gynecol Scand. 2008; 87, 760–767.Google Scholar
2. SAMHSA. Results from the 2007 National Survey on Drug Use and Health: National Findings, 2008. U.S. Department of Health and Human Services, Office of Applied Studies: Rockville, MD.Google Scholar
3. Jaddoe, VW, Troe, EJ, Hofman, A, et al. Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study. Paediatr Perinat Epidemiol. 2008; 22, 162–171.Google Scholar
4. Mitchell, EA, Ford, RP, Stewart, AW, et al. Smoking and the sudden infant death syndrome. Pediatrics. 1993; 91, 893–896.Google Scholar
5. Bruin, JE, Gerstein, HC, Holloway, AC. Long-term consequences of fetal and neonatal nicotine exposure: a critical review. Toxicol Sci. 2010; 116, 364–374.CrossRefGoogle ScholarPubMed
6. Chen, J, Millar, WJ. Age of smoking initiation: implications for quitting. Health Rep. 1998; 9, 39–46.Google ScholarPubMed
7. Buka, SL, Shenassa, ED, Niaura, R. Elevated risk of tobacco dependence among offspring of mothers who smoked during pregnancy: a 30-year prospective study. Am J Psychiatry. 2003; 160, 1978–1984.Google Scholar
8. Al Mamun, A, O'Callaghan, FV, Alati, R, et al. Does maternal smoking during pregnancy predict the smoking patterns of young adult offspring? A birth cohort study. Tob Control. 2006; 15, 452–457.CrossRefGoogle ScholarPubMed
9. Kandel, DB, Wu, P, Davies, M. Maternal smoking during pregnancy and smoking by adolescent daughters. Am J Public Health. 1994; 84, 1407–1413.CrossRefGoogle ScholarPubMed
10. Lieb, R, Schreier, A, Pfister, H, Wittchen, HU. Maternal smoking and smoking in adolescents: a prospective community study of adolescents and their mothers. Eur Addict Res. 2003; 9, 120–130.Google Scholar
11. DiFranza, JR. Hooked from the first cigarette. Sci Am. 2008; 298, 82–87.CrossRefGoogle ScholarPubMed
12. Fidler, JA, Wardle, J, Brodersen, NH, Jarvis, MJ, West, R. Vulnerability to smoking after trying a single cigarette can lie dormant for three years or more. Tob Control. 2006; 15, 205–209.Google Scholar
13. Chistyakov, V, Patkina, N, Tammimaki, A, et al. Nicotine exposure throughout early development promotes nicotine self-administration in adolescent mice and induces long-lasting behavioural changes. Eur J Pharmacol. 2010; 640, 87–93.CrossRefGoogle ScholarPubMed
14. Klein, LC, Stine, MM, Pfaff, DW, Vandenbergh, DJ. Maternal nicotine exposure increases nicotine preference in periadolescent male but not female C57B1/6 J mice. Nicotine Tob Res. 2003; 5, 117–124.Google Scholar
15. Levin, ED, Lawrence, S, Petro, A, et al. Increased nicotine self-administration following prenatal exposure in female rats. Pharmacol Biochem Behav. 2006; 85, 669–674.CrossRefGoogle ScholarPubMed
16. Pastrakuljic, A, Schwartz, R, Simone, C, Derewlany, LO, Knie, B, Koren, G. Transplacental transfer and biotransformation studies of nicotine in the human placental cotyledon perfused in vitro. Life Sci. 1998; 63, 2333–2342.Google Scholar
17. Luck, W, Nau, H, Hansen, R, Steldinger, R. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev Pharmacol Ther. 1985; 8, 384–395.Google Scholar
18. Suzuki, K, Horiguchi, T, Comas-Urrutia, AC, Mueller-Heubach, E, Morishima, HO, Adamsons, K. Placental transfer and distribution of nicotine in the pregnant rhesus monkey. Am J Obstet Gynecol. 1974; 119, 253–262.CrossRefGoogle ScholarPubMed
19. Huang, LZ, Abbott, LC, Winzer-Serhan, UH. Effects of chronic neonatal nicotine exposure on nicotinic acetylcholine receptor binding, cell death and morphology in hippocampus and cerebellum. Neuroscience. 2007; 146, 1854–1868.Google Scholar
20. Shacka, JJ, Robinson, SE. Exposure to prenatal nicotine transiently increases neuronal nicotinic receptor subunit alpha7, alpha4 and beta2 messenger RNAs in the postnatal rat brain. Neuroscience. 1998; 84, 1151–1161.CrossRefGoogle ScholarPubMed
21. Slotkin, TA, Orband-Miller, L, Queen, KL. Development of [3H]nicotine binding sites in brain regions of rats exposed to nicotine prenatally via maternal injections or infusions. J Pharmacol Exp Ther. 1987; 242, 232–237.Google Scholar
22. Abreu-Villaca, Y, Seidler, FJ, Tate, CA, Cousins, MM, Slotkin, TA. Prenatal nicotine exposure alters the response to nicotine administration in adolescence: effects on cholinergic systems during exposure and withdrawal. Neuropsychopharmacology. 2004; 29, 879–890.Google Scholar
23. Miao, H, Liu, C, Bishop, K, Gong, ZH, Nordberg, A, Zhang, X. Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain. J Neurochem. 1998; 70, 752–762.CrossRefGoogle ScholarPubMed
24. Chen, H, Parker, SL, Matta, SG, Sharp, BM. Gestational nicotine exposure reduces nicotinic cholinergic receptor (nAChR) expression in dopaminergic brain regions of adolescent rats. Eur J Neurosci. 2005; 22, 380–388.Google Scholar
25. Good, CH, Bay, KD, Buchanan, RA, McKeon, KA, Skinner, RD, Garcia-Rill, E. Prenatal exposure to cigarette smoke affects the physiology of pedunculopontine nucleus (PPN) neurons in development. Neurotoxicol Teratol. 2006; 28, 210–219.Google Scholar
26. Pilarski, JQ, Wakefield, HE, Fuglevand, AJ, Levine, RB, Fregosi, RF. Developmental nicotine exposure alters neurotransmission and excitability in hypoglossal motoneurons. J Neurophysiol. 2011; 105, 423–433.Google Scholar
27. Kohlmeier, KA, Christensen, MH, Kristensen, MP, Kristiansen, U. Pharmacological evidence of functional inhibitory metabotrophic glutamate receptors on mouse arousal-related cholinergic laterodorsal tegmental neurons. Neuropharmacology. 2013; 66, 99–113.Google Scholar
28. Kohlmeier, KA. Off the beaten path: drug addiction and the pontine laterodorsal tegmentum. ISRN Neurosci. 2013; 2013, 604847.Google Scholar
29. Lodge, DJ, Grace, AA. The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc Natl Acad Sci USA. 2006; 103, 5167–5172.Google Scholar
30. Floresco, SB, West, AR, Ash, B, Moore, H, Grace, AA. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci. 2003; 6, 968–973.Google Scholar
31. Forster, GL, Blaha, CD. 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. 2000; 12, 3596–3604.Google Scholar
32. Blaha, CD, Allen, LF, Das, S, et al. 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. 1996; 16, 714–722.Google Scholar
33. Drevets, WC, Gautier, C, Price, JC, et al. Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry. 2001; 49, 81–96.Google Scholar
34. Pontieri, FE, Tanda, G, Orzi, F, Di, CG. Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature. 1996; 382, 255–257.Google Scholar
35. Pontieri, FE, Tanda, G, Di, CG. 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. 1995; 92, 12304–12308.Google Scholar
36. Lammel, S, Lim, BK, Ran, C, et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature. 2012; 491, 212–217.CrossRefGoogle ScholarPubMed
37. Omelchenko, N, Sesack, SR. Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol. 2005; 483, 217–235.Google Scholar
38. Omelchenko, N, Sesack, SR. Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J Comp Neurol. 2006; 494, 863–875.Google Scholar
39. Lester, DB, Miller, AD, Blaha, CD. Muscarinic receptor blockade in the ventral tegmental area attenuates cocaine enhancement of laterodorsal tegmentum stimulation-evoked accumbens dopamine efflux in the mouse. Synapse. 2010; 64, 216–223.Google Scholar
40. Laviolette, SR, Priebe, RP, Yeomans, JS. Role of the laterodorsal tegmental nucleus in scopolamine- and amphetamine-induced locomotion and stereotypy. Pharmacol Biochem Behav. 2000; 65, 163–174.CrossRefGoogle ScholarPubMed
41. Forster, GL, Blaha, CD. Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat. Eur J Neurosci. 2003; 17, 751–762.Google Scholar
42. Oakman, SA, Faris, PL, Kerr, PE, Cozzari, C, Hartman, BK. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci. 1995; 15, 5859–5869.Google Scholar
43. Pauly, JR, Sparks, JA, Hauser, KF, Pauly, TH. In utero nicotine exposure causes persistent, gender-dependant changes in locomotor activity and sensitivity to nicotine in C57Bl/6 mice. Int J Dev Neurosci. 2004; 22, 329–337.CrossRefGoogle ScholarPubMed
44. Nesil, T, Kanit, L, Collins, AC, Pogun, S. Individual differences in oral nicotine intake in rats. Neuropharmacology. 2011; 61, 189–201.CrossRefGoogle ScholarPubMed
45. Matta, SG, Balfour, DJ, Benowitz, NL, et al. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl). 2007; 190, 269–319.Google Scholar
46. Bachmanov, AA, Reed, DR, Beauchamp, GK, Tordoff, MG. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002; 32, 435–443.Google Scholar
47. Kane, VB, Fu, Y, Matta, SG, Sharp, BM. Gestational nicotine exposure attenuates nicotine-stimulated dopamine release in the nucleus accumbens shell of adolescent Lewis rats. J Pharmacol Exp Ther. 2004; 308, 521–528.Google Scholar
48. Christensen, MH, Ishibashi, M, Nielsen, ML, Leonard, CS, Kohlmeier, KA. Age-related changes in nicotine response of cholinergic and non-cholinergic laterodorsal tegmental neurons: implications for the heightened adolescent susceptibility to nicotine addiction. Neuropharmacology. 2014; 85, 263–283.Google Scholar
49. Tsien, RY. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature. 1981; 290, 527–528.Google Scholar
50. Kohlmeier, KA, Inoue, T, Leonard, CS. Hypocretin/orexin peptide signaling in the ascending arousal system: elevation of intracellular calcium in the mouse dorsal raphe and laterodorsal tegmentum. J Neurophysiol. 2004; 92, 221–235.Google Scholar
51. Grynkiewicz, G, Poenie, M, Tsien, RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985; 260, 3440–3450.Google Scholar
52. Boucetta, S, Jones, BE. Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats. J Neurosci. 2009; 29, 4664–4674.Google Scholar
53. Mieda, M, Hasegawa, E, Kisanuki, YY, Sinton, CM, Yanagisawa, M, Sakurai, T. Differential roles of orexin receptor-1 and -2 in the regulation of non-REM and REM sleep. J Neurosci. 2011; 31, 6518–6526.Google Scholar
54. Jia, HG, Yamuy, J, Sampogna, S, Morales, FR, Chase, MH. 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. 2003; 992, 205–219.Google Scholar
55. Vincent, SR, Satoh, K, Armstrong, DM, Fibiger, HC. NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci Lett. 1983; 43, 31–36.Google Scholar
56. Vincent, SR, Kimura, H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience. 1992; 46, 755–784.Google Scholar
57. Shen, JX, Yakel, JL. Nicotinic acetylcholine receptor-mediated calcium signaling in the nervous system. Acta Pharmacol Sin. 2009; 30, 673–680.Google Scholar
58. Berridge, MJ. Neuronal calcium signaling. Neuron. 1998; 21, 13–26.Google Scholar
59. Kurosawa, R, Taoka, N, Shinohara, F, Minami, M, Kaneda, K. Cocaine exposure enhances excitatory synaptic drive to cholinergic neurons in the laterodorsal tegmental nucleus. Eur J Neurosci. 2013; doi:10.1111/ejn.12296 [Epub ahead of print].Google Scholar
60. Nelson, CL, Wetter, JB, Milovanovic, M, Wolf, ME. The laterodorsal tegmentum contributes to behavioral sensitization to amphetamine. Neuroscience. 2007; 146, 41–49.CrossRefGoogle ScholarPubMed
61. Huang, LZ, Winzer-Serhan, UH. Chronic neonatal nicotine upregulates heteromeric nicotinic acetylcholine receptor binding without change in subunit mRNA expression. Brain Res. 2006; 1113, 94–109.CrossRefGoogle ScholarPubMed
62. Ishibashi, M, Leonard, CS, Kohlmeier, KA. Nicotinic activation of laterodorsal tegmental neurons: implications for addiction to nicotine. Neuropsychopharmacology. 2009; 34, 2529–2547.Google Scholar
63. Christensen, MH, Kohlmeier, KA. Age-related changes in functional postsynaptic nAChR subunits in neurons of the laterodorsal tegmental nucleus. Addiction Biology, 2014, accepted for publication.Google Scholar
64. Wooltorton, JR, Pidoplichko, VI, Broide, RS, Dani, JA. Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci. 2003; 23, 3176–3185.Google Scholar
65. Quick, MW, Lester, RA. Desensitization of neuronal nicotinic receptors. J Neurobiol. 2002; 53, 457–478.Google Scholar
66. Quitadamo, C, Fabbretti, E, Lamanauskas, N, Nistri, A. Activation and desensitization of neuronal nicotinic receptors modulate glutamatergic transmission on neonatal rat hypoglossal motoneurons. Eur J Neurosci. 2005; 22, 2723–2734.CrossRefGoogle ScholarPubMed
67. Ma, L, Wu, YM, Guo, YY, et al. Nicotine addiction reduces the large-conductance Ca(2+)-activated potassium channels expression in the nucleus accumbens. Neuromolecular Med. 2013; 15, 227–237.Google Scholar
68. Wang, H, Shi, H, Zhang, L, et al. Nicotine is a potent blocker of the cardiac A-type K(+) channels. Effects on cloned Kv4.3 channels and native transient outward current. Circulation. 2000; 102, 1165–1171.Google Scholar
69. Kristensen, MP, Tyler, BS, Kohlmeier, KA, Leonard, CS. Comparative electrophysiological and cholinoceptive characteristics of laterodorsal tegmental neurons from the developing mouse. Soc for NS Annual Meeting, San Diego, November 2007.Google Scholar
70. Griguoli, M, Maul, A, Nguyen, C, Giorgetti, A, Carloni, P, Cherubini, E. Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculare interneurons. J Neurosci. 2010; 30, 10773–10783.Google Scholar
71. Faraday, MM, O’Donoghue, VA, Grunberg, NE. Effects of nicotine and stress on startle amplitude and sensory gating depend on rat strain and sex. Pharmacol Biochem Behav. 1999; 62, 273–284.CrossRefGoogle ScholarPubMed
72. Zocchi, A, Orsini, C, Cabib, S, Puglisi-Allegra, S. Parallel strain-dependent effect of amphetamine on locomotor activity and dopamine release in the nucleus accumbens: an in vivo study in mice. Neuroscience. 1998; 82, 521–528.CrossRefGoogle Scholar
73. LeSage, MG, Gustaf, E, Dufek, MB, Pentel, PR. Effects of maternal intravenous nicotine administration on locomotor behavior in pre-weanling rats. Pharmacol Biochem Behav. 2006; 85, 575–583.Google Scholar
74. Zhu, J, Zhang, X, Xu, Y, Spencer, TJ, Biederman, J, Bhide, PG. Prenatal nicotine exposure mouse model showing hyperactivity, reduced cingulate cortex volume, reduced dopamine turnover, and responsiveness to oral methylphenidate treatment. J Neurosci. 2012; 32, 9410–9418.Google Scholar
75. Diaz, R, Ogren, SO, Blum, M, Fuxe, K. Prenatal corticosterone increases spontaneous and d-amphetamine induced locomotor activity and brain dopamine metabolism in prepubertal male and female rats. Neuroscience. 1995; 66, 467–473.Google Scholar
76. Lordi, B, Patin, V, Protais, P, Mellier, D, Caston, J. Chronic stress in pregnant rats: effects on growth rate, anxiety and memory capabilities of the offspring. Int J Psychophysiol. 2000; 37, 195–205.Google Scholar
77. Dempsey, D, Jacob, P III, Benowitz, NL. Nicotine metabolism and elimination kinetics in newborns. Clin Pharmacol Ther. 2000; 67, 458–465.Google Scholar
78. Talhout, R, Schulz, T, Florek, E, van, BJ, Wester, P, Opperhuizen, A. Hazardous compounds in tobacco smoke. Int J Environ Res Public Health. 2011; 8, 613–628.Google Scholar
79. Tsuneki, H, Klink, R, Lena, C, Korn, H, Changeux, JP. Calcium mobilization elicited by two types of nicotinic acetylcholine receptors in mouse substantia nigra pars compacta. Eur J Neurosci. 2000; 12, 2475–2485.Google Scholar
80. Slotkin, TA, Seidler, FJ, Qiao, D, et al. Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys. Neuropsychopharmacology. 2005; 30, 129–144.Google Scholar
81. Britton, AF, Vann, RE, Robinson, SE. Perinatal nicotine exposure eliminates peak in nicotinic acetylcholine receptor response in adolescent rats. J Pharmacol Exp Ther. 2007; 320, 871–876.Google Scholar
82. Gentry, CL, Lukas, RJ. Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr Drug Targets CNS Neurol Disord. 2002; 1, 359–385.Google Scholar
83. Ke, L, Eisenhour, CM, Bencherif, M, Lukas, RJ. Effects of chronic nicotine treatment on expression of diverse nicotinic acetylcholine receptor subtypes. I. Dose- and time-dependent effects of nicotine treatment. J Pharmacol Exp Ther. 1998; 286, 825–840.Google Scholar
84. Buisson, B, Bertrand, D. Chronic exposure to nicotine upregulates the human (alpha)4((beta)2 nicotinic acetylcholine receptor function. J Neurosci. 2001; 21, 1819–1829.Google Scholar
85. Perry, DC, Kellar, KJ. [3H]epibatidine labels nicotinic receptors in rat brain: an autoradiographic study. J Pharmacol Exp Ther. 1995; 275, 1030–1034.Google Scholar
86. Pilarski, JQ, Wakefield, HE, Fuglevand, AJ, Levine, RB, Fregosi, RF. Increased nicotinic receptor desensitization in hypoglossal motor neurons following chronic developmental nicotine exposure. J Neurophysiol. 2012; 107, 257–264.Google Scholar
87. Gold, AB, Keller, AB, Perry, DC. Prenatal exposure of rats to nicotine causes persistent alterations of nicotinic cholinergic receptors. Brain Res. 2009; 1250, 88–100.Google Scholar
88. Ibanez-Tallon, I, Miwa, JM, Wang, HL, et al. Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron. 2002; 33, 893–903.Google Scholar
89. Miwa, JM, Ibanez-Tallon, I, Crabtree, GW, et al. lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron. 1999; 23, 105–114.Google Scholar
90. Damaj, MI. Calcium-acting drugs modulate expression and development of chronic tolerance to nicotine-induced antinociception in mice. J Pharmacol Exp Ther. 2005; 315, 959–964.Google Scholar
91. Katsura, M, Mohri, Y, Shuto, K, et al. Up-regulation of L-type voltage-dependent calcium channels after long term exposure to nicotine in cerebral cortical neurons. J Biol Chem. 2002; 277, 7979–7988.Google Scholar
92. Stevens, TR, Krueger, SR, Fitzsimonds, RM, Picciotto, MR. Neuroprotection by nicotine in mouse primary cortical cultures involves activation of calcineurin and L-type calcium channel inactivation. J Neurosci. 2003; 23, 10093–10099.Google Scholar
93. Kezunovic, N, Hyde, J, Goitia, B, Bisagno, V, Urbano, FJ, Garcia-Rill, E. Muscarinic modulation of high frequency oscillations in pedunculopontine neurons. Front Neurol. 2013; 4, 176.CrossRefGoogle ScholarPubMed
94. Kohlmeier, KA, Leonard, CS. Transmitter modulation of spike-evoked calcium transients in arousal related neurons: muscarinic inhibition of SNX-482-sensitive calcium influx. Eur J Neurosci. 2006; 23, 1151–1162.Google Scholar
95. Yang, T, Colecraft, HM. Regulation of voltage-dependent calcium channels by RGK proteins. Biochim Biophys Acta. 2013; 1828, 1644–1654.Google Scholar
96. Campusano, JM, Su, H, Jiang, SA, Sicaeros, B, O’Dowd, DK. nAChR-mediated calcium responses and plasticity in Drosophila Kenyon cells. Dev Neurobiol. 2007; 67, 1520–1532.Google Scholar
97. Dautan, D, Huerta-Ocampo, I, Witten, IB, et al. A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J Neurosci. 2014; 34, 4509–4518.Google Scholar
98. Kuhlmann, CR, Trumper, JR, Tillmanns, H, Alexander, SC, Erdogan, A. Nicotine inhibits large conductance Ca(2+)-activated K(+) channels and the NO/-cGMP signaling pathway in cultured human endothelial cells. Scand Cardiovasc J. 2005; 39, 348–352.Google Scholar
99. Buttigieg, J, Brown, S, Holloway, AC, Nurse, CA. Chronic nicotine blunts hypoxic sensitivity in perinatal rat adrenal chromaffin cells via upregulation of KATP channels: role of alpha7 nicotinic acetylcholine receptor and hypoxia-inducible factor-2alpha. J Neurosci. 2009; 29, 7137–7147.Google Scholar
100. Bournaud, R, Hidalgo, J, Yu, H, Girard, E, Shimahara, T. Catecholamine secretion from rat foetal adrenal chromaffin cells and hypoxia sensitivity. Pflugers Arch. 2007; 454, 83–92.Google Scholar
101. Liu, L, Zhu, W, Zhang, ZS, et al. Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol. 2004; 91, 1482–1491.Google Scholar
102. Wang, H, Shi, H, Wang, Z. Nicotine depresses the functions of multiple cardiac potassium channels. Life Sci. 1999; 65, L143–L149.Google Scholar
103. Sabatini, BL, Regehr, WG. Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J Neurosci. 1997; 17, 3425–3435.CrossRefGoogle ScholarPubMed
104. Augustine, GJ. Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. J Physiol. 1990; 431, 343–364.Google Scholar
105. Richardson, SA, Tizabi, Y. Hyperactivity in the offspring of nicotine-treated rats: role of the mesolimbic and nigrostriatal dopaminergic pathways. Pharmacol Biochem Behav. 1994; 47, 331–337.Google Scholar
106. Goksor, E, Amark, M, Alm, B, Gustafsson, PM, Wennergren, G. The impact of pre- and post-natal smoke exposure on future asthma and bronchial hyper-responsiveness. Acta Paediatr. 2007; 96, 1030–1035.Google Scholar
107. Weissman, MM, Warner, V, Wickramaratne, PJ, Kandel, DB. Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J Am Acad Child Adolesc Psychiatry. 1999; 38, 892–899.Google Scholar
108. Talati, A, Bao, Y, Kaufman, J, Shen, L, Schaefer, CA, Brown, AS. Maternal smoking during pregnancy and bipolar disorder in offspring. Am J Psychiatry. 2013; 170, 1178–1185.Google Scholar
109. Pauly, JR, Slotkin, TA. Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatr. 2008; 97, 1331–1337.Google Scholar
110. Vaglenova, J, Parameshwaran, K, Suppiramaniam, V, Breese, CR, Pandiella, N, Birru, S. Long-lasting teratogenic effects of nicotine on cognition: gender specificity and role of AMPA receptor function. Neurobiol Learn Mem. 2008; 90, 527–536.Google Scholar
111. Duke, JC, Lee, YO, Kim, AE, et al. Exposure to electronic cigarette television advertisements among youth and young adults. Pediatrics. 2014; 134, e29–e36.Google Scholar
112. Gilmore, AB, Fooks, G, McKee, M. A review of the impacts of tobacco industry privatisation: implications for policy. Glob Public Health. 2011; 6, 621–642.Google Scholar
113. Blood-Siegfried, J, Rende, EK. The long-term effects of prenatal nicotine exposure on neurologic development. J Midwifery Womens Health. 2010; 55, 143–152.Google Scholar
114. Slotkin, TA. If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents? Neurotoxicol Teratol. 2008; 30, 1–19.Google Scholar