Sex differences in nicotine self-administration in rats during progressive unit dose reduction: Implications for nicotine regulation policy

Benowitz, 1994, Establishing a nicotine threshold for addiction. The implications for tobacco regulation, N Engl J Med, 331, 123, 10.1056/NEJM199407143310212 Benowitz, 2013, Reducing the nicotine content to make cigarettes less addictive, Tob Control, 22, i14, 10.1136/tobaccocontrol-2012-050860 Benowitz, 2007, Nicotine and carcinogen exposure with smoking of progressively reduced nicotine content cigarette, Cancer Epidemiol Biomarkers Prev, 16, 2479, 10.1158/1055-9965.EPI-07-0393 Benowitz, 2009, Progressive commercial cigarette yield reduction: biochemical exposure and behavioral assessment, Cancer Epidemiol Biomarkers Prev, 18, 876, 10.1158/1055-9965.EPI-08-0731 Benowitz, 2012, Smoking behavior and exposure to tobacco toxicants during 6months of smoking progressively reduced nicotine content cigarettes, Cancer Epidemiol Biomarkers Prev, 21, 761, 10.1158/1055-9965.EPI-11-0644 Bidwell, 2012, Latent factor structure of a behavioral economic cigarette demand curve in adolescent smokers, Addict Behav, 37, 1257, 10.1016/j.addbeh.2012.06.009 Brower, 2002, Rat strain differences in nicotine self-administration using an unlimited access paradigm, Brain Res, 930, 12, 10.1016/S0006-8993(01)03375-3 CDC, 2008, Smoking-attributable mortality, years of potential life lost, and productivity losses — United States, 2000–2004, Morb Mortal Wkly Rep, 57, 1226 Chaudhri, 2005, Sex differences in the contribution of nicotine and nonpharmacological stimuli to nicotine self-administration in rats, Psychopharmacology (Berl), 180, 258, 10.1007/s00213-005-2152-3 Chen, 2007, Acquisition of nicotine self-administration in adolescent rats given prolonged access to the drug, Neuropsychopharmacology, 32, 700, 10.1038/sj.npp.1301135 Christensen, 2008, Essential value of cocaine and food in rats: tests of the exponential model of demand, Psychopharmacology (Berl), 198, 221, 10.1007/s00213-008-1120-0 Clemens, 2009, The addition of five minor tobacco alkaloids increases nicotine-induced hyperactivity, sensitization and intravenous self-administration in rats, Int J Neuropsychopharmacol, 15, 1 Comer, 1995, Effects of food deprivation on cocaine base smoking in rhesus monkeys, Psychopharmacology (Berl), 119, 127, 10.1007/BF02246152 Corrigall, 1989, Nicotine maintains robust self-administration in rats on a limited-access schedule, Psychopharmacology (Berl), 99, 473, 10.1007/BF00589894 Cosgrove, 2012, Sex differences in availability of β2*-nicotinic acetylcholine receptors in recently abstinent tobacco smokers, Arch Gen Psychiatry, 69, 418, 10.1001/archgenpsychiatry.2011.1465 DeGrandpre, 1992, Behavioral economics of drug self-administration. III. A reanalysis of the nicotine regulation hypothesis, Psychopharmacology, 108, 1, 10.1007/BF02245277 Denoble, 2006, Intravenous nicotine self-administration in rats: effects of mecamylamine, hexamethonium and naloxone, Psychopharmacology (Berl), 184, 266, 10.1007/s00213-005-0054-z Diergaarde, 2011, Poor impulse control predicts inelastic demand for nicotine but not alcohol in rats, Addict Biol, 17, 576, 10.1111/j.1369-1600.2011.00376.x Donny, 1998, Acquisition of nicotine self-administration in rats: the effects of dose, feeding schedule, and drug contingency, Psychopharmacology (Berl), 136, 83, 10.1007/s002130050542 Donny, 2000, Nicotine self-administration in rats: estrous cycle effects, sex differences and nicotinic receptor binding, Psychopharmacology (Berl), 151, 392, 10.1007/s002130000497 Donny, 2012, Impact of tobacco regulation on animal research: new perspectives and opportunities, Nicotine Tob Res, 14, 1319, 10.1093/ntr/nts162 Emery, 2001, Simulated effect of tobacco tax variation on Latino health in California, Am J Prev Med, 21, 278, 10.1016/S0749-3797(01)00368-3 Feltenstein, 2012, Nicotine self-administration and reinstatement of nicotine-seeking in male and female rats, Drug Alcohol Depend, 121, 240, 10.1016/j.drugalcdep.2011.09.001 Fu, 2003, Norepinephrine release in amygdala of rats during chronic nicotine self-administration: an in vivo microdialysis study, Neuropharmacology, 45, 514, 10.1016/S0028-3908(03)00201-6 Harris, 2008, Compensatory nicotine self-administration in rats during reduced access to nicotine: an animal model of smoking reduction, Exp Clin Psychopharmacol, 16, 86, 10.1037/1064-1297.16.1.86 Harris, 2009, Correlates of individual differences in compensatory nicotine self-administration in rats following a decrease in nicotine unit dose, Psychopharmacology (Berl), 205, 599, 10.1007/s00213-009-1567-7 Harris, 2011, A lack of association between severity of nicotine withdrawal and individual differences in compensatory nicotine self-administration in rats, Psychopharmacology (Berl), 217, 153, 10.1007/s00213-011-2273-9 Hatsukami, 2010, Reduced nicotine content cigarettes: effects on toxicant exposure, dependence and cessation, Addiction, 105, 343, 10.1111/j.1360-0443.2009.02780.x Hatsukami, 2010, Nicotine reduction revisited: science and future directions, Tob Control, 19, e1, 10.1136/tc.2009.035584 Henningfield, 2004, Reducing tobacco addiction through tobacco product regulation, Tob Control, 13, 132, 10.1136/tc.2003.006890 Hubert, 2000, The effects of diet, ad libitum feeding, and moderate and severe dietary restriction on body weight, survival, clinical pathology parameters, and cause of death in control Sprague–Dawley rats, Toxicol Sci, 58, 195, 10.1093/toxsci/58.1.195 Hukkanen, 2005, Metabolism and disposition kinetics of nicotine, Pharmacol Rev, 57, 79, 10.1124/pr.57.1.3 Hursh, 1991, Behavioral economics of drug self-administration and drug abuse policy, J Exp Anal Behav, 56, 377, 10.1901/jeab.1991.56-377 Hursh, 2013, Behavioral economics and empirical public policy, J Exp Anal Behav, 99, 98, 10.1002/jeab.7 Hursh, 2008, Economic demand and essential value, Psychol Rev, 115, 186, 10.1037/0033-295X.115.1.186 Johnson, 2012, Assessing the effects of chronic sazetidine-A delivery on nicotine self-administration in both male and female rats, Psychopharmacology (Berl), 222, 269, 10.1007/s00213-012-2642-z Keenan, 1995, Diet, overfeeding, and moderate dietary restriction in control Sprague–Dawley rats: II. Effects on age-related proliferative and degenerative lesions, Toxicol Pathol, 23, 287, 10.1177/019262339502300306 Keenan, 1996, The effects of diet, ad libitum overfeeding, and moderate dietary restriction on the rodent bioassay: the uncontrolled variable in safety assessment, Toxicol Pathol, 24, 757, 10.1177/019262339602400620 Keenan, 1997, The effects of diet, overfeeding and moderate dietary restriction on Sprague–Dawley rat survival, disease and toxicology, J Nutr, 127, 851S, 10.1093/jn/127.5.851S Kenny, 2006, Nicotine self-administration acutely activates brain reward systems and induces a long-lasting increase in reward sensitivity, Neuropsychopharmacology, 31, 1203, 10.1038/sj.npp.1300905 Kessler, 1994, Statement on nicotine-containing cigarettes, Tob Control, 3, 148, 10.1136/tc.3.2.148 Klein, 2004, Sex differences in voluntary oral nicotine consumption by adolescent mice: a dose–response experiment, Pharmacol Biochem Behav, 78, 13, 10.1016/j.pbb.2004.01.005 Koylu, 1997, Sex difference in up-regulation of nicotinic acetylcholine receptors in rat brain, Life Sci, 61, L185, 10.1016/S0024-3205(97)00665-6 Laaksonen, 2013, Food and water intake, growth, and adiposity of Sprague–Dawley rats with diet board for 24months, Lab Anim, 47, 245, 10.1177/0023677213488103 Lê, 2006, Increased vulnerability to nicotine self-administration and relapse in alcohol-naive offspring of rats selectively bred for high alcohol intake, J Neurosci, 26, 1872, 10.1523/JNEUROSCI.4895-05.2006 Lê, 2010, Coadministration of intravenous nicotine and oral alcohol in rats, Psychopharmacology (Berl), 208, 475, 10.1007/s00213-009-1746-6 LeSage, 2002, Continuous nicotine infusion reduces nicotine self-administration in rats with 23-h/day access to nicotine, Pharmacol Biochem Behav, 72, 279, 10.1016/S0091-3057(01)00775-4 LeSage, 2003, 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, 278, 10.1007/s00213-003-1539-2 LeSage, 2007, Effects of pregnancy on nicotine self-administration and nicotine pharmacokinetics in rats, Psychopharmacology (Berl), 194, 413, 10.1007/s00213-007-0830-z Li, 2012, Sex differences in yohimbine-induced increases in the reinforcing efficacy of nicotine in adolescent rats, Addict Biol Lynch, 2009, Sex and ovarian hormones influence vulnerability and motivation for nicotine during adolescence in rats, Pharmacol Biochem Behav, 94, 43, 10.1016/j.pbb.2009.07.004 Lynch, 2010, Role of progesterone in nicotine addiction: evidence from initiation to relapse, Exp Clin Psychopharmacol, 18, 451, 10.1037/a0021265 Mackillop, 2010, Behavioral economic analysis of cue-elicited craving for alcohol, Addiction, 105, 1599, 10.1111/j.1360-0443.2010.03004.x Mackillop, 2012, The neuroeconomics of nicotine dependence: a preliminary functional magnetic resonance imaging study of delay discounting of monetary and cigarette rewards in smokers, Psychiatry Res, 202, 20, 10.1016/j.pscychresns.2011.10.003 Mackillop, 2012, High-resolution behavioral economic analysis of cigarette demand to inform tax policy, Addiction, 107, 2191, 10.1111/j.1360-0443.2012.03991.x Matta, 2007, Guidelines on nicotine dose selection for in vivo research, Psychopharmacology (Berl), 190, 269, 10.1007/s00213-006-0441-0 Mochizuki, 1998, Nicotine induced up‐regulation of nicotinic receptors in CD-1 mice demonstrated with an in vivo radiotracer: gender differences, Synapse, 30, 116, 10.1002/(SICI)1098-2396(199809)30:1<116::AID-SYN15>3.0.CO;2-2 Nesil, 2011, Individual differences in oral nicotine intake in rats, Neuropharmacology, 61, 189, 10.1016/j.neuropharm.2011.03.027 O'Dell, 2007, Extended access to nicotine self-administration leads to dependence: circadian measures, withdrawal measures, and extinction behavior in rats, J Pharmacol Exp Ther, 320, 180, 10.1124/jpet.106.105270 Palmatier, 2007, Conditioned reinforcement in rats established with self-administered nicotine and enhanced by noncontingent nicotine, Psychopharmacology (Berl), 195, 235, 10.1007/s00213-007-0897-6 Park, 2007, Age, sex and early environment contribute to individual differences in nicotine/acetaldehyde-induced behavioral and endocrine responses in rats, Pharmacol Biochem Behav, 86, 297, 10.1016/j.pbb.2006.10.002 Parker, 2004, Up-regulation of brain nicotinic acetylcholine receptors in the rat during long-term self-administration of nicotine: disproportionate increase of the alpha6 subunit, Mol Pharmacol, 65, 611, 10.1124/mol.65.3.611 Paterson, 2004, Prolonged nicotine dependence associated with extended access to nicotine self-administration in rats, Psychopharmacology (Berl), 173, 64, 10.1007/s00213-003-1692-7 Pehrson, 2008, The effects of acute and repeated nicotine doses on spontaneous activity in male and female Sprague Dawley rats: analysis of brain area epibatidine binding and cotinine levels, Pharmacol Biochem Behav, 89, 424, 10.1016/j.pbb.2008.01.018 Perkins, 1996, Sex differences in nicotine versus nonnicotine reinforcement as determinants of tobacco smoking, Exp Clin Psychopharmacol, 4, 166, 10.1037/1064-1297.4.2.166 Perkins, 2001, Smoking cessation in women. Special considerations, CNS Drugs, 15, 391, 10.2165/00023210-200115050-00005 Perkins, 2009, Sex differences in nicotine reinforcement and reward: influences on the persistence of tobacco smoking, Nebr Symp Motiv, 55, 143, 10.1007/978-0-387-78748-0_9 Perkins, 2008, Sex differences in long-term smoking cessation rates due to nicotine patch, Nicotine Tob Res, 10, 1245, 10.1080/14622200802097506 Perkins, 1994, Nicotine discrimination in male and female smokers, Psychopharmacology (Berl), 116, 407, 10.1007/BF02247470 Perkins, 1999, Sex differences in nicotine effects and self-administration: review of human and animal evidence, Nicotine Tob Res, 1, 301, 10.1080/14622299050011431 Rodefer, 1997, A comparison of progressive ratio schedules versus behavioral economic measures: effect of an alternative reinforcer on the reinforcing efficacy of phencyclidine, Psychopharmacology (Berl), 132, 95, 10.1007/s002130050325 Rosecrans, 1972, Brain area nicotine levels in male and female rats with different levels of spontaneous activity, Neuropharmacology, 11, 863, 10.1016/0028-3908(72)90045-7 Scherer, 1999, Smoking behaviour and compensation: a review of the literature, Psychopharmacology (Berl), 145, 1, 10.1007/s002130051027 Shoaib, 1997, Nicotine self-administration in rats: strain and nicotine pre-exposure effects on acquisition, Psychopharmacology (Berl), 129, 35, 10.1007/s002130050159 Smith, 2013, Gradual and immediate nicotine reduction result in similar low-dose nicotine self-administration, Nicotine Tob Res, 15, 1918, 10.1093/ntr/ntt082 Sofuoglu, 2012, The reinforcement threshold for nicotine as a target for tobacco control, Drug Alcohol Depend, 125, 1, 10.1016/j.drugalcdep.2012.04.023 Tauras, 2001 Tengs, 2005, The AMA proposal to mandate nicotine reduction in cigarettes: a simulation of the population health impacts, Prev Med, 40, 170, 10.1016/j.ypmed.2004.05.017 Valentine, 1997, Self-administration in rats allowed unlimited access to nicotine, Psychopharmacology (Berl), 133, 300, 10.1007/s002130050405 Valle, 2005, Sex-related differences in energy balance in response to caloric restriction, Am J Physiol Endocrinol Metab, 289, E15, 10.1152/ajpendo.00553.2004 Wang, 2008, Neuroadaptive changes in the mesocortical glutamatergic system during chronic nicotine self-administration and after extinction in rats, J Neurochem, 106, 943, 10.1111/j.1471-4159.2008.05456.x Yu, 2010, Nicotine self-administration diminishes stress-induced norepinephrine secretion but augments adrenergic-responsiveness in the hypothalamic paraventricular nucleus and enhances adrenocorticotropic hormone and corticosterone release, J Neurochem, 112, 1327, 10.1111/j.1471-4159.2009.06551.x