Abuse liability assessment of an e-cigarette refill liquid using intracranial self-stimulation and self-administration models in rats

Drug and Alcohol Dependence

Volumn 168, Issue , 2016, Pages 76-88

  LeSage, M G ^a,b,c   Staley, M ^a   Muelken, P ^a   Smethells, J R ^a,c   Stepanov, I ^d   Vogel, R I ^d   Pentel, P R ^a,b   Harris, A C ^a,b,c  

^a MINNEAPOLIS MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Behavioral economics; E cigarettes; Intracranial self stimulation; Nicotine; Rat; Self administration; Tobacco control policy

Indexed keywords

ALKALOID; MECAMYLAMINE; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC AGENT; NICOTINIC RECEPTOR BLOCKING AGENT;

ADULT; ANHEDONIA; ANIMAL EXPERIMENT; ARTICLE; AVERSION; CHEMICAL COMPOSITION; CONTROLLED STUDY; ELECTRONIC CIGARETTE; INTRACRANIAL SELF-STIMULATION TEST; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING ASSAY; REINFORCEMENT; SELF ADMINISTRATION TEST; SUBSTANCE ABUSE; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; DRUG SELF ADMINISTRATION; SELF STIMULATION; SPRAGUE DAWLEY RAT;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRONIC CIGARETTES; MALE; MECAMYLAMINE; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RATS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT (PSYCHOLOGY); SELF ADMINISTRATION; SELF STIMULATION;

EID: 84994292946     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2016.08.628     Document Type: Article

References (103)

1. Abobo, C.V., Ma, J., Liang, D., Effect of menthol on nicotine pharmacokinetics in rats after cigarette smoke inhalation. Nicotine Tob. Res. 14 (2012), 801–808.
2. Alsharari, S.D., King, J.R., Nordman, J.C., Muldoon, P.P., Jackson, A., Zhu, A.Z., Tyndale, R.F., Kabbani, N., Damaj, M.I., Effects of menthol on nicotine pharmacokinetic, pharmacology and dependence in mice. PLoS One, 10, 2015, e0137070.
3. Ambrose, V., Miller, J.H., Dickson, S.J., Hampton, S., Truman, P., Lea, R.A., Fowles, J., Tobacco particulate matter is more potent than nicotine at upregulating nicotinic receptors on SH-SY5Y cells. Nicotine Tob. Res. 9 (2007), 793–799.
4. Arrazola, R.A., Singh, T., Corey, C.G., Husten, C.G., Neff, L.J., Apelberg, B.J., Bunnell, R.E., Choiniere, C.J., King, B.A., Cox, S., McAfee, T., Caraballo, R.S., Centers for Disease, C., Prevention, Tobacco use among middle and high school students − United States, 2011–2014. MMWR 64 (2015), 381–385.
5. Bardo, M.T., Green, T.A., Crooks, P.A., Dwoskin, L.P., Nornicotine is self-administered intravenously by rats. Psychopharmacology (Berl.) 146 (1999), 290–296.
6. Bauco, P., Wise, R.A., Potentiation of lateral hypothalamic and midline mesencephalic brain stimulation reinforcement by nicotine: examination of repeated treatment. J. Pharmacol. Exp. Ther. 271 (1994), 294–301.
7. Belluzzi, J.D., Wang, R., Leslie, F.M., Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 30 (2005), 705–712.
8. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a powerful and practical approach to multiple testing. in behavior genetics research. J. R. Stat. Soc. Series B Methodol. 57 (1995), 289–300.
9. Benjamini, Y., Yekutieli, D., The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29 (2001), 1165–1188.
10. Benowitz, N.L., Kuyt, F., Jacob, P. 3rd, Circadian blood nicotine concentrations during cigarette smoking. Clin. Pharmacol. Ther. 32 (1982), 758–764.
11. Benowitz, N.L., Herrera, B., Jacob, P. 3rd, Mentholated cigarette smoking inhibits nicotine metabolism. J. Pharmacol. Exp. Ther. 310 (2004), 1208–1215.
12. Biala, G., Staniak, N., Budzynska, B., Effects of varenicline and mecamylamine on the acquisition expression, and reinstatement of nicotine-conditioned place preference by drug priming in rats. Naunyn Schmiedebergs Arch. Pharmacol. 381 (2010), 361–370.
13. Brandon, T.H., Goniewicz, M.L., Hanna, N.H., Hatsukami, D.K., Herbst, R.S., Hobin, J.A., Ostroff, J.S., Shields, P.G., Toll, B.A., Tyne, C.A., Viswanath, K., Warren, G.W., Electronic nicotine delivery systems: a policy statement from the American Association for Cancer Research and the American Society of Clinical Oncology. J. Clin. Oncol. 33 (2015), 952–963.
14. Breland, A.B., Spindle, T., Weaver, M., Eissenberg, T., Science and electronic cigarettes: current data, future needs. J. Addict. Med. 8 (2014), 223–233.
15. Brennan, K.A., Crowther, A., Putt, F., Roper, V., Waterhouse, U., Truman, P., Tobacco particulate matter self-administration in rats: differential effects of tobacco type. Addict. Biol., 2013.
16. Brennan, K.A., Putt, F., Roper, V., Waterhouse, U., Truman, P., Nicotine and tobacco particulate self-administration: effects of mecamylamine: SCH23390 and ketanserin pretreatment. Curr. Psychopharmacol. 2 (2013), 229–240.
17. Brennan, K.A., Putt, F., Truman, P., Nicotine-, tobacco particulate matter- and methamphetamine-produced locomotor sensitisation in rats. Psychopharmacology (Berl.) 228 (2013), 659–672.
18. Brennan, K.A., Laugesen, M., Truman, P., Whole tobacco smoke extracts to model tobacco dependence in animals. Neurosci. Biobehav. Rev. 47C (2014), 53–69.
19. Brower, V.G., Fu, Y., Matta, S.G., Sharp, B.M., Rat strain differences in nicotine self-administration using an unlimited access paradigm. Brain Res. 930 (2002), 12–20.
20. Caggiula, A.R., Donny, E.C., Palmatier, M.I., Liu, X., Chaudhri, N., Sved, A.F., The role of nicotine in smoking: a dual-reinforcement model. Nebr. Symp. Motiv. 55 (2009), 91–109.
21. Cao, J., Belluzzi, J.D., Loughlin, S.E., Keyler, D.E., Pentel, P.R., Leslie, F.M., Acetaldehyde, a major constituent of tobacco smoke, enhances behavioral, endocrine, and neuronal responses to nicotine in adolescent and adult rats. Neuropsychopharmacology 32 (2007), 2025–2035.
22. Chaudhri, N., Caggiula, A.R., Donny, E.C., Palmatier, M.I., Liu, X., Sved, A.F., Complex interactions between nicotine and nonpharmacological stimuli reveal multiple roles for nicotine in reinforcement. Psychopharmacology (Berl.) 184 (2006), 353–366.
23. Clarke, P.B.S., Kumar, R., The effects of nicotine on locomotor activity in non-tolerant and tolerant rats. Br. J. Pharmacol. 78 (1983), 329–337.
24. Clemens, K.J., Caille, S., Stinus, L., Cador, M., The addition of five minor tobacco alkaloids increases nicotine-induced hyperactivity, sensitization and intravenous self-administration in rats. Int. J. Neuropsychopharmacol., 2009, 1355–1366.
25. Cobb, C.O., Hendricks, P.S., Eissenberg, T., Electronic cigarettes and nicotine dependence: evolving products, evolving problems. BMC Med., 13, 2015, 119.
26. Costello, M.R., Reynaga, D.D., Mojica, C.Y., Zaveri, N.T., Belluzzi, J.D., Leslie, F.M., Comparison of the reinforcing properties of nicotine and cigarette smoke extract in rats. Neuropsychopharmacology 39 (2014), 1843–1851.
27. Craig, E.L., Zhao, B., Cui, J.Z., Novalen, M., Miksys, S., Tyndale, R.F., Nicotine pharmacokinetics in rats is altered as a function of age, impacting the interpretation of animal model data. Drug Metab. Dispos. 42 (2014), 1447–1455.
28. Da Silva, A.L., Elisabetsky, E., Interference of propylene glycol with the hole-board test. Braz. J. Med. Biol. Res. 34 (2001), 545–547.
29. Deehan, G.A. Jr., Hauser, S.R., Waeiss, R.A., Knight, C.P., Toalston, J.E., Truitt, W.A., McBride, W.J., Rodd, Z.A., Co-administration of ethanol and nicotine: the enduring alterations in the rewarding properties of nicotine and glutamate activity within the mesocorticolimbic system of female alcohol-preferring (P) rats. Psychopharmacology (Berl.) 232 (2015), 4293–4302.
30. Donny, E.C., Caggiula, A.R., Rowell, P.P., Gharib, M.A., Maldovan, V., Booth, S., Mielke, M.M., Hoffman, A., McCallum, S., Nicotine self-administration in rats: estrous cycle effects, sex differences and nicotinic receptor binding. Psychopharmacology (Berl.) 151 (2000), 392–405.
31. Donny, E.C., Taylor, T.G., LeSage, M.G., Levin, M., Buffalari, D.M., Joel, D., Sved, A.F., Impact of tobacco regulation on animal research: new perspectives and opportunities. Nicotine Tob. Res. 14 (2012), 1319–1338.
32. Dwoskin, L.P., Buxton, S.T., Jewell, A.L., Crooks, P.A., S(−)-nornicotine increases dopamine release in a calcium-dependent manner from superfused rat striatal slices. J. Neurochem. 60 (1993), 2167–2174.
33. Dwoskin, L.P., Teng, L., Buxton, S.T., Ravard, A., Deo, N., Crooks, P.A., Minor alkaloids of tobacco release [3H]dopamine from superfused rat striatal slices. Eur. J. Pharmacol. 276 (1995), 195–199.
34. Dwoskin, L.P., Crooks, P.A., Teng, L., Green, T.A., Bardo, M.T., Acute and chronic effects of nornicotine on locomotor activity in rats: altered response to nicotine. Psychopharmacology (Berl.) 145 (1999), 442–451.
35. Eissenberg, T., Balster, R.L., Initial tobacco use episodes in children and adolescents: current knowledge, future directions. Drug Alcohol Depend. 59:Suppl. 1 (2000), S41–60.
36. Etter, J.F., Zather, E., Svensson, S., Analysis of refill liquids for electronic cigarettes. Addiction 108 (2013), 1671–1679.
37. Evans, S.E., Hoffman, A.C., Electronic cigarettes: abuse liability, topography and subjective effects. Tob. Control 23:Suppl. 2 (2014), ii23–29.
38. Farsalinos, K.E., Spyrou, A., Stefopoulos, C., Tsimopoulou, K., Kourkoveli, P., Tsiapras, D., Kyrzopoulos, S., Poulas, K., Voudris, V., Nicotine absorption from electronic cigarette use: comparison between experienced consumers (vapers) and naive users (smokers). Sci. Rep., 5, 2015, 11269.
39. Foddai, M., Dosia, G., Spiga, S., Diana, M., Acetaldehyde increases dopaminergic neuronal activity in the VTA. Neuropsychopharmacology 29 (2004), 530–536.
40. Food and Drug Administration, Draft Guidance For Industry: Assessment Of Abuse Potential Of Drug. 2010 Retrieved from: http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM198650. pdf.
41. Forrest, P., Galletly, D.C., A double-blind comparative study of three formulations of diazepam in volunteers. Anaesth. Intensive Care 16 (1988), 158–163.
42. Fowler, C.D., Kenny, P.J., Habenular signaling in nicotine reinforcement. Neuropsychopharmacology 37 (2012), 306–307.
43. Fowler, C.D., Kenny, P.J., Nicotine aversion: neurobiological mechanisms and relevance to tobacco dependence vulnerability. Neuropharmacology, 2013.
44. Fowler, C.D., Lu, Q., Johnson, P.M., Marks, M.J., Kenny, P.J., Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471 (2011), 597–601.
45. Glautier, S., Clements, K., White, J.A., Taylor, C., Stolerman, I.P., Alcohol and the reward value of cigarette smoking. Behav. Pharmacol. 7 (1996), 144–154.
46. Goniewicz, M.L., Knysak, J., Gawron, M., Kosmider, L., Sobczak, A., Kurek, J., Prokopowicz, A., Jablonska-Czapla, M., Rosik-Dulewska, C., Havel, C., Jacob, P. 3rd, Benowitz, N., Levels of selected carcinogens and toxicants in vapour from electronic cigarettes. Tob. Control 23 (2014), 133–139.
47. Grebenstein, P., Burroughs, D., Zhang, Y., LeSage, M.G., Sex differences in nicotine self-administration in rats during progressive unit dose reduction: implications for nicotine regulation policy. Pharmacol. Biochem. Behav 114–115 (2013), 70–81.
48. Grebenstein, P.E., Burroughs, D., Roiko, S.A., Pentel, P.R., LeSage, M.G., Predictors of the nicotine reinforcement threshold, compensation, and elasticity of demand in a rodent model of nicotine reduction policy. Drug Alcohol Depend. 151 (2015), 181–193.
49. Griffiths, R.R., Bigelow, G.E., Liebson, I., Facilitation of human tobacco self-administration by ethanol: a behavioral analysis. J. Exp. Anal. Behav. 25 (1976), 279–292.
50. Guillem, K., Vouillac, C., Azar, M.R., Parsons, L.H., Koob, G.F., Cador, M., Stinus, L., Monoamine oxidase inhibition dramatically increases the motivation to self-administer nicotine in rats. J. Neurosci. 25 (2005), 8593–8600.
51. Harrell, P.T., Simmons, V.N., Correa, J.B., Padhya, T.A., Brandon, T.H., Electronic nicotine delivery systems (e-cigarettes): review of safety and smoking cessation efficacy. Otolaryngol. Head Neck Surg. 151 (2014), 381–393.
52. Harris, A.C., Burroughs, D., Pentel, P.R., LeSage, M.G., Compensatory nicotine self-administration in rats during reduced access to nicotine: an animal model of smoking reduction. Exp. Clin. Psychopharmacol. 16 (2008), 86–97.
53. Harris, A.C., Pentel, P.R., LeSage, M.G., Correlates of individual differences in compensatory nicotine self-administration in rats following a decrease in nicotine unit dose. Psychopharmacology (Berl.) 205 (2009), 599–611.
54. Harris, A.C., Mattson, C., Lesage, M.G., Keyler, D.E., Pentel, P.R., Comparison of the behavioral effects of cigarette smoke and pure nicotine in rats. Pharmacol. Biochem. Behav. 96 (2010), 217–227.
55. Harris, A.C., Pentel, P.R., Burroughs, D., Staley, M.D., Lesage, M.G., A lack of association between severity of nicotine withdrawal and individual differences in compensatory nicotine self-administration in rats. Psychopharmacology (Berl.) 217 (2011), 153–166.
56. Harris, A.C., Stepanov, I., Pentel, P.R., Lesage, M.G., Delivery of nicotine in an extract of a smokeless tobacco product reduces its reinforcement-attenuating and discriminative stimulus effects in rats. Psychopharmacology (Berl.) 220 (2012), 565–576.
57. Harris, A.C., Tally, L., Muelken, P., Banal, A., Schmidt, C.E., Cao, Q., LeSage, M.G., Effects of nicotine and minor tobacco alkaloids on intracranial-self-stimulation in rats. Drug Alcohol Depend. 153 (2015), 330–334.
58. Harris, A.C., Tally, L., Schmidt, C.E., Muelken, P., Stepanov, I., Saha, S., Vogel, R.I., LeSage, M.G., Animal models to assess the abuse liability of tobacco products: effects of smokeless tobacco extracts on intracranial self-stimulation. Drug Alcohol Depend. 147 (2015), 60–67.
59. Harrison, A.A., Gasparini, F., Markou, A., Nicotine potentiation of brain stimulation reward reversed by DH beta E and SCH 23390 but not by eticlopride, LY 314582 or MPEP in rats. Psychopharmacology (Berl.) 160 (2002), 56–66.
60. Hieda, Y., Keyler, D.E., VanDeVoort, J.T., Niedbala, R.S., Raphael, D.E., Ross, C.A., Pentel, P.R., Immunization of rats reduces nicotine distribution to brain. Psychopharmacology (Berl.) 143 (1999), 150–157.
61. Hillman, M.G., Schneider, C.W., Voluntary selection of and tolerance to 1,2 propanediol (propylene glycol) by high and low ethanol-selecting mouse strains. J. Comp. Physiol. Psychol. 88 (1975), 773–777.
62. Hu, M.C., Davies, M., Kandel, D.B., Epidemiology and correlates of daily smoking and nicotine dependence among young adults in the United States. Am. J. Public Health 96 (2006), 299–308.
63. Hursh, S.R., Silberberg, A., Economic demand and essential value. Psych. Rev. 115 (2008), 186–198.
64. Huston-Lyons, D., Kornetsky, C., Effects of nicotine on the threshold for rewarding brain stimulation in rats. Pharmacol. Biochem. Behav. 41 (1992), 755–759.
65. Jacob, P. 3rd, Wilson, M., Benowitz, N.L., Improved gas chromatographic method for the determination of nicotine and cotinine in biologic fluids. J. Chromatogr. 222 (1981), 61–70.
66. Kenny, P.J., Polis, I., Koob, G.F., Markou, A., Low dose cocaine self-administration transiently increases but high dose cocaine persistently decreases brain reward function in rats. Eur. J. Neurosci. 17 (2003), 191–195.
67. Kornetsky, C., Esposito, R.U., Euphorigenic drugs: effects on the reward pathways of the brain. Fed. Proc. 38 (1979), 2473–2476.
68. Kornetsky, C., Esposito, R.U., McLean, S., Jacobson, J.O., Intracranial self-stimulation thresholds: a model for the hedonic effects of drugs of abuse. Arch. Gen. Psychiatry 36 (1979), 289–292.
69. Kosmider, L., Sobczak, A., Fik, M., Knysak, J., Zaciera, M., Kurek, J., Goniewicz, M.L., Carbonyl compounds in electronic cigarette vapors: effects of nicotine solvent and battery output voltage. Nicotine Tob. Res. 16 (2014), 1319–1326.
70. Kramlinger, V.M., von Weymarn, L.B., Murphy, S.E., Inhibition and inactivation of cytochrome P450 2A6 and cytochrome P450 2A13 by menthofuran, beta-nicotyrine and menthol. Chem. Biol. Interact. 197 (2012), 87–92.
71. Kunin, D., Smith, B.R., Amit, Z., Nicotine and ethanol interaction on conditioned taste aversions induced by both drugs. Pharmacol. Biochem. Behav. 62 (1999), 215–221.
72. Lauterstein, D., Hoshino, R., Gordon, T., Watkins, B.X., Weitzman, M., Zelikoff, J., The changing face of tobacco use among United States youth. Curr. Drug Abuse Rev 7 (2014), 29–43.
73. LeSage, M.G., Keyler, D.E., Shoeman, D., Raphael, D., Collins, G., Pentel, P.R., Continuous nicotine infusion reduces nicotine self-administration in rats with 23-h/day access to nicotine. Pharmacol. Biochem. Behav. 72 (2002), 279–289.
74. LeSage, M.G., Keyler, D.E., Collins, G., Pentel, P.R., Effects of continuous nicotine infusion on nicotine self-administration in rats: relationship between continuously infused and self-administered nicotine doses and serum concentrations. Psychopharmacology (Berl.) 170 (2003), 278–286.
75. LeSage, M.G., Burroughs, D., Dufek, M., Keyler, D.E., Pentel, P.R., Reinstatement of nicotine self-administration in rats by presentation of nicotine-paired stimuli, but not nicotine priming. Pharmacol. Biochem. Behav. 79 (2004), 507–513.
76. LeSage, M.G., Shelley, D., Pravetoni, M., Pentel, P.R., Enhanced attenuation of nicotine discrimination in rats by combining nicotine-specific antibodies with a nicotinic receptor antagonist. Pharmacol. Biochem. Behav. 102 (2012), 157–162.
77. LeSage, M.G., Toward a nonhuman model of contingency management: effects of reinforcing abstinence from nicotine self-administration in rats with an alternative nondrug reinforcer. Psychopharmacology (Berl.) 203 (2009), 13–22.
78. Lin, H.Q., Burden, P.M., Johnston, G.A., Propylene glycol elicits anxiolytic-like responses to the elevated plus-maze in male mice. J. Pharm. Pharmacol. 50 (1998), 1127–1131.
79. Markou, A., Koob, G.F., Construct validity of a self-stimulation threshold paradigm: effects of reward and performance manipulations. Physiol. Behav. 51 (1992), 111–119.
80. Myers, W.D., Ng, K.T., Singer, G., Intravenous self-administration of acetaldehyde in the rat as a function of schedule, food deprivation and photoperiod. Pharmacol. Biochem. Behav. 17 (1982), 807–811.
81. Myers, W.D., Ng, K.T., Singer, G., Effects of naloxone and buprenorphine on intravenous acetaldehyde self-injection in rats. Physiol. Behav. 33 (1984), 449–455.
82. Negus, S.S., Miller, L.L., Intracranial self-stimulation to evaluate abuse potential of drugs. Pharmacol. Rev. 66 (2014), 869–917.
83. Orellana-Barrios, M.A., Payne, D., Mulkey, Z., Nugent, K., Electronic cigarettes-a narrative review for clinicians. Am. J. Med. 128 (2015), 674–681.
84. Paterson, N.E., Balfour, D.J., Markou, A., Chronic bupropion differentially alters the reinforcing, reward-enhancing and conditioned motivational properties of nicotine in rats. Nicotine Tob. Res. 10 (2008), 995–1008.
85. Ponzoni, L., Moretti, M., Sala, M., Fasoli, F., Mucchietto, V., Lucini, V., Cannazza, G., Gallesi, G., Castellana, C.N., Clementi, F., Zoli, M., Gotti, C., Braida, D., Different physiological and behavioural effects of e-cigarette vapour and cigarette smoke in mice. Eur. Neuropsychopharmacol. 25 (2015), 1775–1786.
86. Porter, L., Duke, J., Hennon, M., Dekevich, D., Crankshaw, E., Homsi, G., Farrelly, M., Electronic cigarette and traditional cigarette use among middle and high school students in Florida, 2011–2014. PLoS One, 10, 2015, e0124385.
87. Rangiah, K., Hwang, W.T., Mesaros, C., Vachani, A., Blair, I.A., Nicotine exposure and metabolizer phenotypes from analysis of urinary nicotine and its 15 metabolites by LC-MS. Bioanalysis 3 (2011), 745–761.
88. Roiko, S.A., Harris, A.C., LeSage, M.G., Keyler, D.E., Pentel, P.R., Passive immunization with a nicotine-specific monoclonal antibody decreases brain nicotine levels but does not precipitate withdrawal in nicotine-dependent rats. Pharmacol. Biochem. Behav. 93 (2009), 105–111.
89. Sartor, C.E., Lessov-Schlaggar, C.N., Scherrer, J.F., Bucholz, K.K., Madden, P.A., Pergadia, M.L., Grant, J.D., Jacob, T., Xian, H., Initial response to cigarettes predicts rate of progression to regular smoking: findings from an offspring-of-twins design. Addict. Behav. 35 (2010), 771–778.
90. Singh, P.P., Junnarkar, A.Y., Seshagirirao, C., Kaushal, R., Naidu, M.U., Varma, R.K., Tripathi, R.M., Shridhar, D.R., A pharmacological study of propane-1,2-diol. Arzneimittelforschung 32 (1982), 1443–1446.
91. Spiller, K., Xi, Z.X., Li, X., Ashby, C.R. Jr., Callahan, P.M., Tehim, A., Gardner, E.L., Varenicline attenuates nicotine-enhanced brain-stimulation reward by activation of alpha4beta2 nicotinic receptors in rats. Neuropharmacology 57 (2009), 60–66.
92. Stalhandske, T., Slanina, P., Nicotyrine inhibits in vivo metabolism of nicotine without increasing its toxicity. Toxicol. Appl. Pharmacol. 65 (1982), 366–372.
93. Takayama, S., Uyeno, E.T., Intravenous self-administration of ethanol and acetaldehyde by rats. Yakubutsu. Seishin. Kodo. 5 (1985), 329–334.
94. Touiki, K., Rat, P., Molimard, R., Chait, A., de Beaurepaire, R., Effects of tobacco and cigarette smoke extracts on serotonergic raphe neurons in the rat. Neuroreport 18 (2007), 925–929.
95. Villegier, A.S., Lotfipour, S., McQuown, S.C., Belluzzi, J.D., Leslie, F.M., Tranylcypromine enhancement of nicotine self-administration. Neuropharmacology 52 (2007), 1415–1425.
96. Walton, K.M., Abrams, D.B., Bailey, W.C., Clark, D., Connolly, G.N., Djordjevic, M.V., Eissenberg, T.E., Fiore, M.C., Goniewicz, M.L., Haverkos, L., Hecht, S.S., Henningfield, J.E., Hughes, J.R., Oncken, C.A., Postow, L., Rose, J.E., Wanke, K.L., Yang, L., Hatsukami, D.K., NIH electronic cigarette workshop: developing a research agenda. Nicotine Tob. Res. 17 (2015), 259–269.
97. Wang, T., Wang, B., Chen, H., Menthol facilitates the intravenous self-administration of nicotine in rats. Front. Behav. Neurosci., 8, 2014, 437.
98. Wise, R.A., Bauco, P., Carlezon, W.A. Jr., Trojniar, W., Self-stimulation and drug reward mechanisms. Ann. N. Y. Acad. Sci. 654 (1992), 192–198.
99. Wise, R.A., Addictive drugs and brain stimulation reward. Annu. Rev. Neurosci. 19 (1996), 319–340.
100. Wise, R.A., Brain reward circuitry: insights from unsensed incentives. Neuron 36 (2002), 229–240.
101. Xiao, Y., Meyer, E.L., Thompson, J.M., Surin, A., Wroblewski, J., Kellar, K.J., Rat alpha3/beta4 subtype of neuronal nicotinic acetylcholine receptor stably expressed in a transfected cell line: pharmacology of ligand binding and function. Mol. Pharmacol. 54 (1998), 322–333.
102. Xiao, Y., Fan, H., Musachio, J.L., Wei, Z.L., Chellappan, S.K., Kozikowski, A.P., Kellar, K.J., Sazetidine-A, a novel ligand that desensitizes alpha4beta2 nicotinic acetylcholine receptors without activating them. Mol. Pharmacol. 70 (2006), 1454–1460.
103. Zaroslinski, J.F., Browne, R.K., Possley, L.H., Propylene glycol as a drug solvent in pharmacologic studies. Toxicol. Appl. Pharmacol. 19 (1971), 573–578.