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Psychopharmacology

, Volume 233, Issue 23–24, pp 3829–3848 | Cite as

Nicotine self-administration research: the legacy of Steven R. Goldberg and implications for regulation, health policy, and research

  • Jack E. HenningfieldEmail author
  • Tracy T. Smith
  • Bethea A. Kleykamp
  • Reginald V. Fant
  • Eric C. Donny
Review

Abstract

Background and rationale

Steven R. Goldberg was a pioneering behavioral pharmacologist whose intravenous drug self-administration studies advanced the understanding of conditioned stimuli and schedules of reinforcement as determinants of pattern and persistence of drug-seeking behavior, and in particular, the importance of nicotine in tobacco use. His passing in 2014 led to invitations to contribute articles to psychopharmacology dedicated to his work.

Objectives

The objectives of this review are to summarize and put into historical perspective Goldberg’s contributions to elucidate the reinforcing effects of nicotine and to summarize the implications of his research for medication development, tobacco regulation, and potential tobacco control policy options. This includes a review of intravenous nicotine self-administration research from the 1960s to 2016.

Results

Goldberg’s application of behavioral pharmacology methods to investigate nicotine reinforcement and the influence of schedule of reinforcement and conditioned stimuli on nicotine administration contributed to the conclusions of the US National Institute on Drug Abuse, and the Surgeon General, that nicotine met the criteria as a dependence-producing drug and cigarette smoking as a prototypic drug dependency or “addiction.” Equally important, this work has been systematically extended to other species and applied to address a range of factors relevant to tobacco use, medication development, regulation, and public health policy.

Conclusions

Steven R. Goldberg was a pioneering scientist whose systematic application of the science of behavioral pharmacology advanced the understanding of tobacco and nicotine use and contributed to the scientific foundation for tobacco product regulation and potential public health tobacco control policy development.

Keywords

Behavioral pharmacology Self-administration Intravenous Nicotine Tobacco Sensory Second-order schedule Reinforcement Punishment Antagonists 

Notes

Acknowledgments

The time and effort of Fant, Henningfield, and Kleykamp were supported by PinneyAssociates without input from any such commercial interests. The effort of Donny was supported by the National Institute on Drug Abuse and FDA Center for Tobacco Products (CTP) (U54 DA031659). The effort of Smith was supported by the National Cancer Institute (T32 CA186783). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or the Food and Drug Administration. The authors are grateful for the care and efforts of Evan Schnoll and Jonathan Gougelet with editing and referencing.

Conflicts of interest

Through Pinney Associates, Drs. Fant, Henningfield, and Kleykamp have consulted or are presently consulting to GlaxoSmithKline on smoking cessation, NJOY on electronic cigarettes, Reynolds American Vapor Products, and to pharmaceutical companies on substance abuse-related regulatory issues on drug products under development. Henningfield shares interest in a patent for a new nicotine gum for smoking cessation that is under license to Niconovum, which is a smoking cessation product subsidiary of Reynolds American, Inc.

Drs. Smith and Donny have no conflicts of interest to report.

References

  1. Abrams DB (2014) Promise and 9010peril of e-cigarettes: can disruptive technology make cigarettes obsolete? JAMA 311(2):135–136PubMedCrossRefGoogle Scholar
  2. Abrams, D. B. (2015) What science says: operationalizing methods to estimate net public health impact. Data trumps dogma. Presented at the E-Cigarette Summit, Royal Society, London, November 12, 2015Google Scholar
  3. Abrams DB, Niaura R (2015) The importance of science-informed policy and what the data really tell us about e-cigarettes. Isr J Health Policy Res 4(22)Google Scholar
  4. Agaku IT, King BA, Dube SR, C. Centers for Disease and Prevention (2014) Current cigarette smoking among adults—United States, 2005-2012. MMWR Morb Mortal Wkly Rep 63(2):29–34PubMedGoogle Scholar
  5. American Psychiatric Association (APA) (1980) Diagnostic and statistical manual of mental disorders, 3rd edn (DMS-III). American Psychiatric Publishing, Arlington, VAGoogle Scholar
  6. American Psychiatric Association (APA) (1994) Diagnostic and statistical manual of mental disorders, 4th edn (DSM-IV). American Psychiatric Publishing, Arlington, VAGoogle Scholar
  7. American Psychiatric Association (APA) (2013) Diagnostic and statistical manual of mental disorders, 5th edn (DSM-V). American Psychiatric Publishing, Arlington, VAGoogle Scholar
  8. Arnold MM, Loughlin SE, Belluzzi JD, Leslie FM (2014) Reinforcing and neural activating effects of norharmane, a non-nicotine tobacco constituent, alone and in combination with nicotine. Neuropharmacology 85:293–304PubMedCrossRefGoogle Scholar
  9. Arrazola RA, Singh T, Corey CG, Husten CG, Neff LJ, Apelberg BJ, Bunnell RE, Choiniere CJ, King BA, Cox S, McAfee T, Caraballo RS, C. Centers for Disease and Prevention (2015) Tobacco use among middle and high school students—United States, 2011–2014. MMWR Morb Mortal Wkly Rep 64(14):381–385PubMedGoogle Scholar
  10. Ator NA, Griffiths RR (1980) Intravenous self-administration of nicotine in the baboon. Fed Proc 40:298Google Scholar
  11. Ator NA, Griffiths RR (1983) Nicotine self-administration in baboons. Pharmacol Biochem Behav 19:993–1003PubMedCrossRefGoogle Scholar
  12. Ator NA, Griffiths RR (2003) Principles of drug abuse liability assessment in laboratory animals. Drug Alcohol Depend 70:S55–S72PubMedCrossRefGoogle Scholar
  13. Ballin S (1991) Chairman of the Coalition on Smoking and Health, letter to the Food and Drug Administration recommending that insofar as tobacco use was sustained by the addictive drug effects of nicotine, the FDA should regulate tobacco products as drugs. https://goo.gl/photos/zb2ri72GZiZGVdug7. Accessed 13 Sept 2016
  14. Bardo MT, Green TA, Crooks PA, Dwoskin LP (1999) Nornicotine is self-administered intravenously by rats. Psychopharmacology 146(3):290–296PubMedCrossRefGoogle Scholar
  15. Barrett JE, Stanley JA (1980) Maintenance of responding by squirrel monkeys under a concurrent shock-postponement, fixed-interval shock-presentation schedule. J Exp Anal Behav 34(1):117–129PubMedPubMedCentralCrossRefGoogle Scholar
  16. Barrett ST, Bevins RA (2013) Nicotine enhances operant responding for qualitatively distinct reinforcers under maintenance and extinction conditions. Pharmacol Biochem Behav. doi: 10.1016/j.pbb.2013.10.012
  17. Barry H (2006) Censorship by a tobacco company. Psychopharmacology 184(3):273–273PubMedCrossRefGoogle Scholar
  18. Belluzzi JD, Wang R, Leslie FM (2005) Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 30(4):705–712PubMedCrossRefGoogle Scholar
  19. Benowitz NL, Henningfield JE (1994) Establishing a nicotine threshold for addiction. The implications for tobacco regulation. N Engl J Med 331(2):123–125PubMedCrossRefGoogle Scholar
  20. Benowitz NL, Henningfield JE (2013) Reducing the nicotine content to make cigarettes less addictive. Tob Control 22(1):2012–050860Google Scholar
  21. Benowitz NL, Dains KM, Hall SM, Stewart S, Wilson M, Dempsey D, Jacob P 3rd (2012) Smoking behavior and exposure to tobacco toxicants during 6 months of smoking progressively reduced nicotine content cigarettes. Cancer Epidemiol Biomark Prev 21(5):761–769CrossRefGoogle Scholar
  22. Benowitz NL, Donny EC et al (2016) Reduced nicotine content cigarettes, e-cigarettes and the cigarette end game. Addiction. doi: 10.1111/add.13534 Google Scholar
  23. Brady JV, Lukas SE (1984) Testing drugs for physical dependence potential and abuse liability. NIDA research Monograph 52. U.S. Department of Health and Human Services, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute on Drug Abuse. U.S. Government Printing Office, Washington, D. CGoogle Scholar
  24. Branch MN (2006) How research in behavioral pharmacology informs behavioral science. J Exp Anal Behav 85(3):407–423PubMedPubMedCentralCrossRefGoogle Scholar
  25. Brandon TH, Goniewicz ML, Hanna NH, Hatsukami DK, Herbst RS, Hobin JA, Ostroff JS, Shields PG, Toll BA, Tyne CA, Viswanath K, Warren GW (2015) 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(8):952–963PubMedCrossRefGoogle Scholar
  26. Brandt EN Jr (1982) Statements of Edward N. Brandt, Jr., M. D., Assistant Secretary of Health, and Dr. C. Everett Coop, Surgeon General, Public Health Service, Department of Health and Human Services, accompanied by Dr. Vincent T. DeVita, Director, National Cancer Institute, and Dr. William Pollin, Director, National Institute on Drug Abuse. In: Comprehensive Smoking Prevention Education Act, Hearing before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representatives, Ninety-Seventh Congress, second session on H. R. 5653 and H. R. 4957. March 5, 11, and 12, 1982. Serial no. 97–106. U. S. Government Printing Office, Washington, pp 278–350Google Scholar
  27. Brandt AM (2007) The cigarette century: the rise, fall, and deadly persistence of the product that defined America. Basic Books, New YorkGoogle Scholar
  28. Brennan KA, Putt F, Truman P (2013) Nicotine-, tobacco particulate matter- and methamphetamine-produced locomotor sensitisation in rats. Psychopharmacology 228(4):659–672PubMedCrossRefGoogle Scholar
  29. Brennan KA, Crowther A, Putt F, Roper V, Waterhouse U, Truman P (2015) Tobacco particulate matter self-administration in rats: differential effects of tobacco type. Addict Biol 20(2):227–235PubMedCrossRefGoogle Scholar
  30. Buffalari DM, Marfo NY, Smith TT, Levin ME, Weaver MT, Thiels E, Sved AF, Donny EC (2014) Nicotine enhances the expression of a sucrose or cocaine conditioned place preference in adult male rats. Pharmacol Biochem Behav 124:320–325PubMedPubMedCentralCrossRefGoogle Scholar
  31. Caggiula AR, Donny EC, Palmatier MI, Liu X, Chaudhri N, Sved AF (2009) The role of nicotine in smoking: a dual-reinforcement model. Neb Symp Motiv 55:91–109CrossRefGoogle Scholar
  32. Cahir E, Pillidge K, Drago J, Lawrence AJ (2011) The necessity of alpha4* nicotinic receptors in nicotine-driven behaviors: dissociation between reinforcing and motor effects of nicotine. Neuropsychopharmacology 36(7):1505–1517PubMedPubMedCentralCrossRefGoogle Scholar
  33. Caine SB, Collins GT, Thomsen M, Wright C, Lanier RK, Mello NK (2014) Nicotine-like behavioral effects of the minor tobacco alkaloids nornicotine, anabasine, and anatabine in male rodents. Exp Clin Psychopharmacol 22(1):9–22PubMedCrossRefGoogle Scholar
  34. Calderon SN, Klein M (2014) A regulatory perspective on the abuse potential evaluation of novel stimulant drugs in the United States. Neuropharmacology 87:97–103PubMedCrossRefGoogle Scholar
  35. Campbell WI (1994) Testimony of William I. Campbell, President, Philip Morris U. S. A., accompanied by Kathy Ellis, Director of Research; James W. Johnston, Chairman, RJ Reynolds Tobacco Co., accompanied by Andy Schindler, Head of Manufacturing, and Richard Cooper, counsel; Thomas E. Sandefur, Jr., Chairman, Brown & Williamson Tobacco Corp., accompanied by Tilford F. Riehl, Vice President; Andrew H. Tisch, Chairman, Lorillard Tobacco Co., accompanied by Alexander Spears III, Vice Chairman; Donald S. Johnston, President, American Tobacco Co.; Edward A. Horrigan, Jr., Chairman, Liggett Group, Inc.; and Joseph Taddeo, President, U.S. Tobacco Co. In: Regulation of Tobacco Products (part 1) Hearings before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representatives, One Hundred Third Congress, Second Session. March 25 and April 14, 1994. Serial no. 103–149. U. S. Government Printing Office, Washington, D. C. pp 542–546Google Scholar
  36. Campbell ND (2007) Discovering addiction. The University of Michigan Press, Ann ArborCrossRefGoogle Scholar
  37. Campbell ND (2009) The history of a public science: how the addiction research center became the NIDA intramural research program. 107(1):108–112Google Scholar
  38. Carter LP, Griffiths RR (2009) Principles of laboratory assessment of drug abuse liability and implications for clinical development. Drug Alcohol Depend 105(suppl 1):S15–S25Google Scholar
  39. Carter LP, Stitzer ML, Henningfield JE, O’Conner RJ, Cummings KM, Hatsukami DK (2009) Abuse liability assessment of tobacco products including potential reduced exposure products. Cancer Epidemiol Biomark Prev 18:3241–3262CrossRefGoogle Scholar
  40. Centers for Disease, C. and Prevention (2011) Quitting smoking among adults—United States, 2001–2010. MMWR Morb Mortal Wkly Rep 60(44):1513–1519Google Scholar
  41. Centers for Disease, C. and Prevention (2012) Current tobacco use among middle and high school students--United States, 2011. MMWR Morb Mortal Wkly Rep 61(31):581–585Google Scholar
  42. Chang Q, Hanania T, Mash DC, Maillet EL (2015) Noribogaine reduces nicotine self-administration in rats. J Psychopharmacol 29(6):704–711PubMedPubMedCentralCrossRefGoogle Scholar
  43. Chaudhri N, Caggiula AR, Donny EC, Booth S, Gharib MA, Craven LA, Allen SS, Sved AF, Perkins KA (2005) Sex differences in the contribution of nicotine and nonpharmacological stimuli to nicotine self-administration in rats. Psychopharmacology 180(2):258–266PubMedCrossRefGoogle Scholar
  44. Chen H, Matta SG, Sharp BM (2007) Acquisition of nicotine self-administration in adolescent rats given prolonged access to the drug. Neuropsychopharmacology 32(3):700–709PubMedCrossRefGoogle Scholar
  45. Cippitelli A, Wu J et al (2015) AT-1001: a high-affinity alpha3beta4 nAChR ligand with novel nicotine-suppressive pharmacology. Br J Pharmacol 172(7):1834–1845PubMedPubMedCentralCrossRefGoogle Scholar
  46. Clemens KJ, Caille S, Stinus L, Cador M (2009) The addition of five minor tobacco alkaloids increases nicotine-induced hyperactivity, sensitization and intravenous self-administration in rats. Int J Neuropsychopharmacol 12(10):1355–1366PubMedCrossRefGoogle Scholar
  47. Clemens KJ, Caille S, Cador M (2010) The effects of response operandum and prior food training on intravenous nicotine self-administration in rats. Psychopharmacology 211(1):43–54PubMedCrossRefGoogle Scholar
  48. Cobb CO, Hendricks PS, Eissenberg T (2015) Electronic cigarettes and nicotine dependence: evolving products, evolving problems. BMC Medicine 13(1):1–4CrossRefGoogle Scholar
  49. Cohen A, Koob GF, George O (2012) Robust escalation of nicotine intake with extended access to nicotine self-administration and intermittent periods of abstinence. Neuropsychopharmacology 37(9):2153–2160PubMedPubMedCentralCrossRefGoogle Scholar
  50. Committee on Problems of Drug Dependence (1973) Testing for dependence liabilities in animals and man (revised 1972). Bull Narc 25:25–39Google Scholar
  51. Corrigall WA (1992) A rodent model for nicotine self-administration. In: Boulton A, Baker G, Wu P (eds) Neuromethods. Humana Press, Clifton, New Jersey, pp. 315–344Google Scholar
  52. Corrigall WA (1999) Nicotine self-administration in animals as a dependence model. Nicotine Tob Res 1:11–20PubMedCrossRefGoogle Scholar
  53. Corrigall WA, Coen KM (1989) Nicotine maintains robust self-administration in rats on a limited-access schedule. Psychopharmacology 99(4):473–478PubMedCrossRefGoogle Scholar
  54. Corrigall WA, Coen KM (1991a) Opiate antagonists reduce cocaine but not nicotine self-administration. Psychopharmacology 104:167–170PubMedCrossRefGoogle Scholar
  55. Corrigall WA, Coen KM (1991b) Selective dopamine antagonists reduce nicotine self-administration. Psychopharmacology 104:171–176PubMedCrossRefGoogle Scholar
  56. Corrigall WA, Franklin KBJ, Coen KM, Clarke PBS (1992) The mesolimbic dopamine system is implicated in the reinforcing effects of nicotine. Psychopharmacology 107:285–289PubMedCrossRefGoogle Scholar
  57. Corrigall WA, Coen KM, Adamson KL (1994) Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653:278–284PubMedCrossRefGoogle Scholar
  58. Deneau GA, Inoki R (1967) Nicotine self-administration in monkeys. Ann N Y Acad Sci 142:227–279CrossRefGoogle Scholar
  59. Deneau GA, Yanagita T, Seevers MH (1969) Self-administration of psychoactive substances by the monkey. Psychopharmacologia (Berl) 16:30–48CrossRefGoogle Scholar
  60. DeNoble VJ (1994) Testimony of Victor John DeNoble, senior behavior analyst, Delaware Community Mental Retardation Program, accompanied by Paul C. Mele, Armed Forces Radiobiology Research Institute. In: Regulation of Tobacco Products (Part 2) Hearings before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representations, One Hundred Third Congress, Second Session (Serial No. 103–153). U. S. Government Printing Office, Washington, D. C., pp 4–156Google Scholar
  61. DeNoble VJ, Mele PC (2006) Intravenous nicotine self-administration in rats: effects of mecamylamine, hexamethonium and naloxone. Psychopharmacology 184:266–272PubMedCrossRefGoogle Scholar
  62. Diergaarde L, van Mourik Y, Pattij T, Schoffelmeer AN, De Vries TJ (2012) Poor impulse control predicts inelastic demand for nicotine but not alcohol in rats. Addict Biol 17(3):576–587PubMedCrossRefGoogle Scholar
  63. Donny EC, Caggiula AR, Knopf S, Brown C (1995) Nicotine self-administration in rats. Psychopharmacology 122(4):390–394PubMedCrossRefGoogle Scholar
  64. Donny EC, Caggiula AR, Mielke MM, Booth S, Gharib MA, Hoffman A, Maldovan V, Shupenko C, McCallum SE (1999) Nicotine self-administration in rats on a progressive ratio schedule of reinforcement. Psychopharmacology 147(2):135–142PubMedCrossRefGoogle Scholar
  65. Donny EC, Caggiula AR, Rowell PP, Gharib MA, Maldovan V, Booth S, Mielke MM, Hoffman A, McCallum S (2000) Nicotine self-administration in rats: estrous cycle effects, sex differences and nicotinic receptor binding. Psychopharmacology 151(4):392–405PubMedCrossRefGoogle Scholar
  66. Donny EC, Chaudhri N, Caggiula AR, Evans-Martin FF, Booth S, Gharib MA, Clements LA, Sved AF (2003) Operant responding for a visual reinforcer in rats is enhanced by noncontingent nicotine: implications for nicotine self-administration and reinforcement. Psychopharmacology 169(1):68–76PubMedCrossRefGoogle Scholar
  67. Donny EC, Taylor TG, LeSage MG, Levin M, Buffalari DM, Joel D, Sved AF (2012) Impact of tobacco regulation on animal research: new perspectives and opportunities. Nicotine Tob Res 14(11):1319–1338PubMedPubMedCentralCrossRefGoogle Scholar
  68. Donny, E. C., D. K. Hatsukami, et al. (2014) Reduced nicotine product standards for combustible tobacco: Building an empirical basis for effective regulation. Prev Med 17–22Google Scholar
  69. Donny EC, Denlinger RL, Tidey JW, Koopmeiners JS, Benowitz NL, Vandrey RG, al’Absi M, Carmella SG, Cinciripini PM, Dermody SS, Drobes DJ, Hecht SS, Jensen J, Lane T, Le CT, McClernon FJ, Montoya ID, Murphy SE, Robinson JD, Stitzer ML, Strasser AA, Tindle H, Hatsukami DK (2015) Randomized trial of reduced-nicotine standards for cigarettes. N Engl J Med 373(14):1340–1349PubMedPubMedCentralCrossRefGoogle Scholar
  70. Dougherty J, Miller D, Togg G, Kostenbauder HB (1981) Reinforcing and other behavioral effects of nicotine. Neurosci Biobehav 5:487–495CrossRefGoogle Scholar
  71. Drug Enforcement Administration (DEA) (2016) Title 21 United States Code (USC) Controlled Substances Act. Department of Justice, Drug Enforcement Administration, Springfield, VAGoogle Scholar
  72. Epping-Jordan MP, Picciotto MR, Changeux JP, Pich EM (1999) Assessment of nicotinic acetylcholine receptor subunit contributions to nicotine self-administration in mutant mice. Psychopharmacology 147(1):25–26PubMedCrossRefGoogle Scholar
  73. Evans SE, Hoffman AC (2014) Electronic cigarettes: abuse liability, topography and subjective effects. Tob Control 23(suppl 2):ii23–ii29PubMedPubMedCentralCrossRefGoogle Scholar
  74. Expert Panel, The (2003) Abuse liability assessment of CNS drugs: conclusions, recommendations, and research priorities. Drug Alcohol Depend 70(3 suppl):S107–S114Google Scholar
  75. Feltenstein MW, Ghee SM, See RE (2012) Nicotine self-administration and reinstatement of nicotine-seeking in male and female rats. Drug Alcohol Depend 121(3):240–246PubMedCrossRefGoogle Scholar
  76. Food and Drug Administration (FDA) (1995) Regulations restricting the sale and distribution of cigarettes and smokeless tobacco products to portect children and adolescents; proposed rule analysis regarding FDA’s jurisdiction over nicotine-containing cigarettes and smokeless tobacco products; notice. Department of Health and Human Services, Food and Drug Administration. Federal Register, vol 60. Silver Spring, MD, pp 41314–41792.Google Scholar
  77. Food and Drug Administration (FDA) (1996) Regulations restricting the sale and distribution of cigarettes and smokeless tobacco to protect children and adolescents; final rule. Department of Health and Human Services, Food and Drug Administration. Federal Register, vol 61. Silver Spring, MD, pp 44396–45318Google Scholar
  78. Food and Drug Administration (FDA) (2010a) Guidance for industry: assessment of abuse potential of drugs, draft guidance. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research (CDER). Silver Spring, MDGoogle Scholar
  79. Food and Drug Administration (FDA) (2010b) Report to Congress: progress and effectiveness of the implementation of the Family Smoking Prevention and Tobacco Control Act. Department of Health and Human Services, Food and Drug Administration, Center for Tobacco Products. Silver Spring, MDGoogle Scholar
  80. Food and Drug Administration (FDA) (2012) Guidance for industry: modified risk tobacco product applications, draft guidance. Department of Health and Human Services, Food and Drug Administration, Center for Tobacco Products. Silver Spring, MDGoogle Scholar
  81. Food and Drug Administration (FDA) (2015) Abuse-deterrent opioids—evaluation and labeling, guidance for industry. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research. Silver Spring, MDGoogle Scholar
  82. Food and Drug Administration (FDA) (2016a) User fees. FDA. http://www.fda.gov/TobaccoProducts/GuidanceComplianceRegulatoryInformation/Manufacturing/ucm417012.htm. Accessed 31 Aug 2016
  83. Food and Drug Administration (FDA) (2016b) Deeming tobacco products to be subject to the Federal Food, Drug, and Cosmetic Act, as amended by the Family Smoking Prevention and Tobacco Control Act; restrictions on the sale and distribution of tobacco products and required warning statements for tobacco products. (Docket No. FDA-2014-N-0189). Federal Register. https://www.federalregister.gov/articles/2016/05/10/2016-10685/deeming-tobacco-products-to-be-subject-to-the-federal-food-drug-and-cosmetic-act-as-amended-by-the. Accessed 12 Sept 2016
  84. Forget B, Wertheim C et al (2010) Noradrenergic [alpha]1 receptors as a novel target for the treatment of nicotine addiction. Neuropsychopharmacology 35(8):1751–1760PubMedPubMedCentralGoogle Scholar
  85. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ (2011) Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471(7340):597–601PubMedPubMedCentralCrossRefGoogle Scholar
  86. Gamaleddin I, Wertheim C et al (2012) Cannabinoid receptor stimulation increases motivation for nicotine and nicotine seeking. Addict Biol 17(1):47–61PubMedCrossRefGoogle Scholar
  87. Gamaleddin I, Guranda M et al (2013) AM404 attenuates reinstatement of nicotine seeking induced by nicotine-associated cues and nicotine priming but does not affect nicotine- and food-taking. J Psychopharmacol 27(6):564–571PubMedPubMedCentralCrossRefGoogle Scholar
  88. Garcia KL, Le AD, Tyndale RF (2014) Effect of food training and training dose on nicotine self-administration in rats. Behav Brain Res 274:10–18PubMedCrossRefGoogle Scholar
  89. George O, Lloyd A et al (2011) Varenicline blocks nicotine intake in rats with extended access to nicotine self-administration. Psychopharmacology 213(4):715–722PubMedCrossRefGoogle Scholar
  90. Goldberg SR (1970) Relapse to opioid dependence: the role of conditioning. In: Harris RT, McIsaac WM, Schuster Jr CR (eds) Drug dependence. University of Austin Texas Press, Austin and London, pp. 170–197Google Scholar
  91. Goldberg SR (1973) Control of behavior by stimuli associated with drug injections. In: Goldberg L, Hoffmeister F (eds) Psychic dependence. Springer-Uerlag, Berlin, pp. 1–7CrossRefGoogle Scholar
  92. Goldberg SR (1976) The behavioral analysis of drug addiction. In: Glick SD, Goldfarb J (eds) Behavioral pharmacology. C. V. Mosby Company, Saint Louis, pp. 283–316Google Scholar
  93. Goldberg SR (1980) Histamine as a punisher in squirrel monkeys: effects of pentobarbital, chlordiazepoxide and H1- and H2-receptor antagonists on behavior and cardiovascular responses. J Pharmacol Exp Ther 214(3):726–736PubMedGoogle Scholar
  94. Goldberg SR, Henningfield JE (1988) Reinforcing effects of nicotine in humans and experimental animals responding under intermittent schedules of i.v. drug injection. Pharmacol Biochem Behav 30(1):227–234PubMedCrossRefGoogle Scholar
  95. Goldberg SR, Kelleher RT (1976) Behavior controlled by scheduled injections of cocaine in squirrel and rhesus monkeys. J Exp Anal Behav 25:93–104PubMedPubMedCentralCrossRefGoogle Scholar
  96. Goldberg SR, Schuster CR (1970) Conditioned nalorphine-induced abstinence changes: persistence in post morphine-dependent monkeys. J Exp Anal Behav 14(1):33–46PubMedPubMedCentralCrossRefGoogle Scholar
  97. Goldberg SR, Spealman RD (1982) Maintenance and suppression of responding by intravenous nicotine injections in squirrel monkeys. Fed Proc 41:216–220PubMedGoogle Scholar
  98. Goldberg SR, Spealman RD (1983) Suppression of behavior by intravenous injections of nicotine or by electric shocks in squirrel monkeys: effects of chlordiazepoxide and mecamylamine. J Pharmacol Exp Ther 224(2):334–339PubMedGoogle Scholar
  99. Goldberg SR, Tang AH (1977) Behavior maintained under second-order schedules of intravenous morphine injection in squirrel and rhesus monkeys. Psychopharmacology 51(3):235–242PubMedCrossRefGoogle Scholar
  100. Goldberg SR, Hoffmeister F, Schlichting UU, Wuttke W (1971) A comparison of pentobarbital and cocaine self-administration in rhesus monkeys: effects of dose and fixed-ratio parameter. J Pharmacol Exp Ther 179(2):277–283PubMedGoogle Scholar
  101. Goldberg SR, Kelleher RT, Morse WH (1975) Second-order schedules of drug injection. Fed Proc 34(9):1771–1776PubMedGoogle Scholar
  102. Goldberg SR, Morse WH, Goldberg DM (1976) Behavior maintained under a second-order schedule by intramuscular injection of morphine or cocaine in rhesus monkeys. J Pharm Exp Ther 199:278–286Google Scholar
  103. Goldberg SR, Spealman RD, Kelleher RT (1979) Enhancement of drug-seeking behavior by environmental stimuli associated with cocaine or morphine injections. Neuropharmacology 18:1015–1017PubMedCrossRefGoogle Scholar
  104. Goldberg SR, Spealman RD, Goldberg DM (1981) Persistent high-rate behavior maintained by intravenous self-administration of nicotine. Science 214:573–575PubMedCrossRefGoogle Scholar
  105. Grebenstein PE, Burroughs D et al (2013) Sex differences in nicotine self-administration in rats during progressive unit dose reduction: implications for nicotine regulation policy. Pharmacol Biochem Behav 114–115:70–81PubMedCrossRefGoogle Scholar
  106. Grebenstein PE, Burroughs D, Roiko SA, Pentel PR, LeSage MG (2015) Predictors of the nicotine reinforcement threshold, compensation, and elasticity of demand in a rodent model of nicotine reduction policy. Drug Alcohol Depend 151:181–193PubMedPubMedCentralCrossRefGoogle Scholar
  107. Griffiths RR, Brady JV, Bradford LD (1979) Predicting the abuse liability of drugs with animal drug self-administration procedures: psychomotor stimulants and hallucinogens. In: Thompson T, Dews PB (eds) Advances in behavioral pharmacology, vol 2. Academic Press, New York, pp. 163–208Google Scholar
  108. Griffiths RR, Bigelow GE, Henningfield JE (1980) Similarities in animal and human drug taking behavior. In: Mello NK (ed) Advances in substance abuse. JAI Press, Greenwich, CT, pp. 1–90Google Scholar
  109. Gritz ER (1978) Patterns of puffing in cigarette smokers. In: Krasnegor NA (ed) Self-administration of abused substances: methods for study. U.S. Government Printing Office, Washington, D. C, pp. 221–235Google Scholar
  110. Hanson HM, Ivester CA, Morton BR (1979) Nicotine self-administration in rats. In: Krasnegor NA (ed) Cigarette smoking as a dependence process. U.S. Government Printing Office, Washington, D. C, pp. 70–90Google Scholar
  111. Harvey DM, Yasar S, Heishman SJ, Panlilio LV, Henningfield JE, Goldberg SR (2004) Nicotine serves as an effective reinforcer of intravenous drug-taking behavior in human cigarette smokers. Psychopharmacology 175:134–142PubMedCrossRefGoogle Scholar
  112. Hatsukami DK, Kotlyar M, Hertsgaard LA, Zhang Y, Carmella SG, Jensen JA, Allen SS, Shields PG, Murphy SE, Stepanov I, Hecht SS (2010) Reduced nicotine content cigarettes: effects on toxicant exposure, dependence and cessation. Addiction 105(2):343–355PubMedPubMedCentralCrossRefGoogle Scholar
  113. Hatsukami DK, Hertsgaard LA, Vogel RI, Jensen JA, Murphy SE, Hecht SS, Carmella SG, al’Absi M, Joseph AM, Allen SS (2013) Reduced nicotine content cigarettes and nicotine patch. Cancer Epidemiol Biomark Prev 22(6):1015–1024CrossRefGoogle Scholar
  114. Henningfield JE (1984) Behavioral pharmacology of cigarette smoking. In: Thompson T, Dews PB, Barrett JE (eds) Advances in behavioral pharmacology, vol 4. Academic Press, Inc., New York, pp. 132–198Google Scholar
  115. Henningfield JE (1994a) Statement of David A. Kessler, Commissioner of Food and Drugs, Food and Drug Administration, accompanied by Jack E. Henningfield, chief, clinical pharmacology branch, National Institute on Drug Abuse. In: Regulation of Tobacco Products (part 1) Hearings before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representatives, One Hundred Third Congress, Second Session. March 25 and April 14, 1994. Serial no. 103–149. U. S. Government Printing Office, Washington, D. C. pp 28–71Google Scholar
  116. Henningfield JE (1994b) Letter to Henry Waxman, May 3, 1994. In: Regulation of Tobacco Products (part 1) Hearings before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representatives, One Hundred Third Congress, Second Session. March 25 and April 14, 1994. Serial no. 103–149. U. S. Government Printing Office, Washington, D. C. p 37Google Scholar
  117. Henningfield JE (2004) Testimony in United States of America v. Philip Morris USA, Inc. In: Litigation Against Tobacco Companies Home. U. S. Department of Justice. https://www.justice.gov/sites/default/files/civil/legacy/2014/09/11/Henningfield%20Written%20Direct_0.pdf. Accessed 31 Aug 2016
  118. Henningfield JE (2011) Tobacco psychopharmacology and public health policy: it takes a community. Exp Clin Psychopharmacol 19(4):249–262PubMedCrossRefGoogle Scholar
  119. Henningfield JE (2014) The tobacco endgame: It’s all about behavior. Prev Med 68:11–16PubMedCrossRefGoogle Scholar
  120. Henningfield JE (2015) Pharmacokinetic and dynamic factors in abuse potential: Historical perspectives from research on opioids, stimulants and nicotine. In: Symposium X: The interplay of pharmacokinetics and pharmacodynamics in abuse potential: Modeling madness? College on Problems of Drug Dependence annual meeting. Arizona Biltmore, Phoenix. June 13–18, 2015Google Scholar
  121. Henningfield JE, Goldberg SR (1983a) Nicotine as a reinforcer in human subjects and laboratory animals. Pharmacol Biochem Behav 19(6):989–992PubMedCrossRefGoogle Scholar
  122. Henningfield JE, Goldberg SR (1983b) Control of behavior by intravenous nicotine injections in human subjects. Pharmacol Biochem Behav 19:1021–1026PubMedCrossRefGoogle Scholar
  123. Henningfield JE, Zeller M (2006) Nicotine psychopharmacology research contributions to United States and global tobacco regulation: a look back and a look forward. Psychopharmacology 184:286–291PubMedCrossRefGoogle Scholar
  124. Henningfield JE, Griffiths RR, Jasinski DR (1981) Human dependence on tobacco and opioids: common factors. In: Thompson T, Johanson CE (eds) Behavioral pharmacology of human drug dependence. U. S. Government Printing Office, Washington, D.C., pp. 210–234Google Scholar
  125. Henningfield JE, Miyasato K, Jasinski DR (1983) Cigarette smokers self-administer intravenous nicotine. Pharmacol Biochem Behav 19:887–890PubMedCrossRefGoogle Scholar
  126. Henningfield JE, Nemeth-Coslett R, Katz JL, Goldberg SR (1987) Intravenous cocaine self-administration by human volunteers: second-order schedules of reinforcement. In: Harris LS (ed) Problems of drug dependence, 1986. NIDA research monograph 76, Department of Health and Human Services. U. S. Government Printing Office, Washington, D. C, pp. 266–273Google Scholar
  127. Henningfield JE, Benowitz NL et al (1998) Reducing the addictiveness of cigarettes. Council on scientific affairs, American Medical Association. Tob Control 7(3):281–293PubMedPubMedCentralCrossRefGoogle Scholar
  128. Henningfield JE, Stolerman IP, Miczek KA (2006a) Nicotine psychopharmacology research: advancing science, public health, and global policy. Psychopharmacology 184:263–265PubMedCrossRefGoogle Scholar
  129. Henningfield JE, Rose CA, Zeller M (2006b) Tobacco industry litigation position on addiction: continued dependence on past views. Tob Control 15(Suppl 4):iv27–iv36PubMedPubMedCentralGoogle Scholar
  130. Henningfield JE, Shiffman S et al (2009) Tobacco dependence and withdrawal: science base, challenges and opportunities for pharmacotherapy. Pharmacol Ther 123(1):1–16PubMedPubMedCentralCrossRefGoogle Scholar
  131. Henningfield JE, Hatsukami DK, Zeller M, Peters E (2011) Conference on abuse liability and appeal of tobacco products: conclusions and recommendations. Drug Alcohol Depend 116(1–3):1–7PubMedPubMedCentralCrossRefGoogle Scholar
  132. Howell LL, Fantegrossi WE (2009) Intravenous drug self-administration in nonhuma primates. In: Buccafusco JJ (ed) Methods of behavior analysis in neuroscience, 2nd edn. CRC Press/Taylor & Francis, Boca Raton Chapter 9Google Scholar
  133. Hursh SR, Roma PG (2013) Behavioral economics and empirical public policy. J Exp Anal Behav 99(1):98–124PubMedCrossRefGoogle Scholar
  134. Hurt RD, Ebbert JO, Muggli ME, Lockhart NJ, Robertson CR (2009) Open doorway to the truth: legacy of the Minnesota tobacco trial. Mayo Clin Proc 84(5):446–456PubMedPubMedCentralCrossRefGoogle Scholar
  135. Jamal A, Agaku IT, O’Connor E, King BA, Kenemer JB, Neff L (2014) Current cigarette smoking among adults—United States, 2005–2013. MMWR Morb Mortal Wkly Rep 63(47):1108–1112PubMedGoogle Scholar
  136. Jarvik ME, JW Cullen, ER Gritz, TM Vogt, and LJ West (1979) Research on smoking behavior. NIDA research monograph 17. Department of Health, Education and Welfare, Washington, D.CGoogle Scholar
  137. Justinova Z, Panlilio LV et al (2015) Effects of fatty acid amide hydrolase (FAAH) inhibitors in non-human primate models of nicotine reward and relapse. Neuropsychopharmacology 40(9):2185–2197PubMedPubMedCentralCrossRefGoogle Scholar
  138. Justinova Z, Le Foll B et al (2016) Differential effects of the metabotropic glutamate 2/3 receptor agonist LY379268 on nicotine versus cocaine self-administration and relapse in squirrel monkeys. Psychopharmacology 233(10):1791–1800PubMedCrossRefGoogle Scholar
  139. Kessler D (1994) Statement of David A. Kessler, Commissioner of Food and Drugs, Food and Drug Administration, accompanied by Jack E. Henningfield, chief, clinical pharmacology branch, National Institute on Drug Abuse. In: Regulation of Tobacco Products (part 1) Hearings before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representatives, One Hundred Third Congress, Second Session. March 25 and April 14, 1994. Serial no. 103–149. U. S. Government Printing Office, Washington, D. C. pp 28–71Google Scholar
  140. Kessler D (1999) Where there’s smoke… Talk November 1999: 183–192, 229Google Scholar
  141. Kessler D (2001) A question of intent: a great American battle with a deadly industry. Public Affairs, New YorkGoogle Scholar
  142. Kluger R (1996) Ashes to ashes: America’s hundred-year cigarette war, the public health, and the unabashed triumph of Philip Morris. Alfred A. Knopf, New YorkGoogle Scholar
  143. Knopick P (1980) Memo Re: National Institute of Drug Abuse desire to have ‘addictive’ added to cigarette warnings. http://www.tobaccofreedom.org/issues/documents/landman/addictive/. Accessed 12 Sept 2016
  144. Koop CE (2003) Tobacco addiction: accomplishments and challenges in science, health, and policy. Nicotine Tob Res 5:613–619PubMedCrossRefGoogle Scholar
  145. Koop CE (2010) Tobacco: the public health disaster of the twentieth century. In: Boyle P, Gray N, Henningfield JE, Seffrin J, Zatonski W (eds) Tobacco an public health: science and policy, 2nd edn. Oxford University Press, Oxford, pp. v–xviiGoogle Scholar
  146. Krasnegor NA (ed) (1978) Self-administration of abused substances: methods for study. NIDA research monograph 20. National Institute on Drug Abuse, Rockville, MDGoogle Scholar
  147. Krasnegor NA (1979a) Cigarette smoking as a dependence process. NIDA research monograph 23. U. S. Department of Health, Education, and Welfare, Public Health Service, Washington, D. CGoogle Scholar
  148. Krasnegor NA (1979b) The behavioral aspects of smoking. NIDA research monograph 26. U. S. Department of Health, Education, and Welfare, Public Health Service, Washington, D. CGoogle Scholar
  149. Lamb RJ, Preston KL, Schindler CW, Meisch RA, Davis F, Katz JL, Henningfield JE, Goldberg SR (1991) The reinforcing and subjective effects of morphine in post-addicts: a dose-response study. J Pharmacol Exp Ther 259(3):1165–1173PubMedGoogle Scholar
  150. Lang WJ, Latiff AA, McQueen A, Singer G (1977) Self-administration of nicotine with and without a food delivery schedule. Pharmacol Biochem Behav 7:65–70PubMedCrossRefGoogle Scholar
  151. Laties VG (2003) Behavior analysis and the growth of behavioral pharmacology. Behav Anal 26(2):235–252PubMedPubMedCentralGoogle Scholar
  152. Latiff AA, Smith LA, Lang WJ (1980) Effects of changing dosage and urinary pH in rats self-administering nicotine on a food delivery schedule. Pharmacol Biochem Behav 13:209–213PubMedCrossRefGoogle Scholar
  153. Le Foll B, Goldberg SR (2005) Cannabinoid CB1 receptor antagonists as promising new medications for drug dependence. J Pharmacol Exp Ther 312(3):875–883PubMedCrossRefGoogle Scholar
  154. Le Foll B, Chefer SI et al (2009) Baseline expression of α4β2* nicotinic acetylcholine receptors predicts motivation to self-administer nicotine. Biol Psychiatry 65(8):714–716PubMedCrossRefGoogle Scholar
  155. Le Foll B, Chakraborty-Chatterjee M et al (2012) Varenicline decreases nicotine self-administration and nicotine- and cue-induced reinstatement of nicotine-seeking behavior in rats when a long pretreatment time is used. Int J Neuropsychopharmacol 15(9):1265–1274PubMedCrossRefGoogle Scholar
  156. Lee AM, Arreola AC et al (2014) Administration of the nicotinic acetylcholine receptor agonists ABT-089 and ABT-107 attenuates the reinstatement of nicotine-seeking behavior in rats. Behav Brain Res 274:168–175PubMedCrossRefGoogle Scholar
  157. LeSage MG, Keyler DE et al (2002) Continuous nicotine infusion reduces nicotine self-administration in rats with 23-h/day access to nicotine. Pharmacol Biochem Behav 72(1–2):279–289PubMedCrossRefGoogle Scholar
  158. LeSage MG, Keyler DE et al (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 170(3):278–228PubMedCrossRefGoogle Scholar
  159. Levin ED, Rezvani AH, Montoya D, Rose JE, Swartzwelder HS (2003) Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology 169(2):141–149PubMedCrossRefGoogle Scholar
  160. Levin ED, Slade S, Johnson M, Petro A, Horton K, Williams P, Rezvani AH, Rose JE (2008) Ketanserin, a 5-HT2 receptor antagonist, decreases nicotine self-administration in rats. Eur J Pharmacol 600(1–3):93–97PubMedPubMedCentralCrossRefGoogle Scholar
  161. Levin ED, Rezvani AH, Xiao Y, Slade S, Cauley M, Wells C, Hampton D, Petro A, Rose JE, Brown ML, Paige MA, McDowell BE, Kellar KJ (2010) Sazetidine—a, a selective alpha4beta2 nicotinic receptor desensitizing agent and partial agonist, reduces nicotine self-administration in rats. J Pharmacol Exp Ther 332(3):933–939PubMedCrossRefGoogle Scholar
  162. Levin ED, Johnson JE, Slade S, Wells C, Cauley M, Petro A, Rose JE (2011) Lorcaserin, a 5-HT2C agonist, decreases nicotine self-administration in female rats. J Pharmacol Exp Ther 338(3):890–896PubMedPubMedCentralCrossRefGoogle Scholar
  163. Li S, Zou S, Coen K, Funk D, Shram MJ, Le AD (2014) Sex differences in yohimbine-induced increases in the reinforcing efficacy of nicotine in adolescent rats. Addict Biol 19(2):156–164PubMedCrossRefGoogle Scholar
  164. Lucchesi BR, Schuster CR, Emley GS (1967) The role of nicotine as a determinant of cigarette smoking frequency in man with observations of certain cardiovascular effects associated with the tobacco alkaloid. Clin Pharmacol Ther 8(6):789–796PubMedCrossRefGoogle Scholar
  165. Lynch WJ (2009) Sex and ovarian hormones influence vulnerability and motivation for nicotine during adolescence in rats. Pharmacol Biochem Behav 94(1):43–50PubMedPubMedCentralCrossRefGoogle Scholar
  166. Manzardo AM, Stein L, Belluzzi JD (2002) Rats prefer cocaine over nicotine in a two-lever self-administration choice test. Brain Res 924(1):10–19PubMedCrossRefGoogle Scholar
  167. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology 190(3):269–319PubMedCrossRefGoogle Scholar
  168. May EL, Jacobson AE (1989) The committee on problems of drug dependence: a legacy of the National Academy of Sciences. A historical account. Drug Alcohol Depend 23(3):183–218PubMedCrossRefGoogle Scholar
  169. McGarity TD, Wagner WE (2008) Bending science: how special interests corrupt public health research. Harvard University Press, Cambridge and LondonGoogle Scholar
  170. Meisch RA (1977) Ethanol self-administration: infrahuman studies. In: Thompson T, Dews PB (eds) Advances in behavioral pharmacology, vol 1. Academic Press, New YorkGoogle Scholar
  171. Meisch RA (2001) Oral drug self-administration: an overview of laboratory animal studies. Alcohol 24(2):117–128PubMedCrossRefGoogle Scholar
  172. Meisch RA, Lemaire GA (1993) Drug self-administration. In: van Haaren F (ed) Methods in behavioral pharmacology. Elsevier Science Publishers B.V, Amsterdam, pp. 257–300CrossRefGoogle Scholar
  173. Meisch RA, Thompson T (1974) Ethanol as a reinforcer: an operant analysis of ethanol dependence. In: Singh JM, Lal H (eds) Drug addiction, vol 3: neurobiology and influences on behavior. Symposia Specialists, Miami, pp. 117–133Google Scholar
  174. Mele PC (1994) Testimony of Victor John DeNoble, senior behavior analyst, Delaware Community Mental Retardation Program, accompanied by Paul C. Mele, Armed Forces Radiobiology Research Institute. In: Regulation of Tobacco Products (Part 2) Hearings before the Subcommittee on Health and the Environment of the Committee on Energy and Commerce, House of Representations, One Hundred Third Congress, Second Session (Serial No. 103–153). U. S. Government Printing Office, Washington, D. C., pp 4–156Google Scholar
  175. National Cancer Institute (2008) The role of the media in promoting and reducing tobacco use. Tobacco control monograph no. 19. U. S. Department of Health and Human Services, National Institutes of Health, National Cancer Institute. NIH pub. no. 07–6242. Bethesda, MDGoogle Scholar
  176. National Institute on Drug Abuse (NIDA) (2014) The science of drug abuse and addiction: the basics. https://www.drugabuse.gov/publications/media-guide/science-drug-abuse-addiction-basics. Accessed 30 Aug 2016
  177. Natividad LA, Torres OV, Friedman TC, O’Dell LE (2013) Adolescence is a period of development characterized by short- and long-term vulnerability to the rewarding effects of nicotine and reduced sensitivity to the anorectic effects of this drug. Behav Brain Res 257:275–285PubMedPubMedCentralCrossRefGoogle Scholar
  178. O’Connor EC, Parker D et al (2010) The alpha4beta2 nicotinic acetylcholine-receptor partial agonist varenicline inhibits both nicotine self-administration following repeated dosing and reinstatement of nicotine seeking in rats. Psychopharmacology 208(3):365–376PubMedCrossRefGoogle Scholar
  179. O’Dell LE, Chen SA, Smith RT, Specio SE, Balster RL, Paterson NE, Markou A, Zorrilla EP, Koob GF (2007) Extended access to nicotine self-administration leads to dependence: circadian measures, withdrawal measures, and extinction behavior in rats. J Pharmacol Exp Ther 320(1):180–193PubMedCrossRefGoogle Scholar
  180. Palmatier MI, Liu X, Matteson GL, Donny EC, Caggiula AR, Sved AF (2007) Conditioned reinforcement in rats established with self-administered nicotine and enhanced by noncontingent nicotine. Psychopharmacology 195(2):235–243PubMedPubMedCentralCrossRefGoogle Scholar
  181. Palmatier MI, Levin ME, Mays KL, Donny EC, Caggiula AR, Sved AF (2009) Bupropion and nicotine enhance responding for nondrug reinforcers via dissociable pharmacological mechanisms in rats. Psychopharmacology 207(3):381–390PubMedPubMedCentralCrossRefGoogle Scholar
  182. Panlilio LV, Goldberg SR (2007) Self-administration of drugs in animals and humans as a model and an investigative tool. Addiction 102(12):1863–1870PubMedPubMedCentralCrossRefGoogle Scholar
  183. Panlilio LV, Yasar S et al (2005) Human cocaine-seeking behavior and its control by drug-associated stimuli in the laboratory. Neuropsychopharmacology 30(2):433–443PubMedCrossRefGoogle Scholar
  184. Panlilio LV, Justinova Z et al (2012) Novel use of a lipid-lowering fibrate medication to prevent nicotine reward and relapse: preclinical findings. Neuropsychopharmacology 37(8):1838–1847PubMedPubMedCentralCrossRefGoogle Scholar
  185. Panlilio LV, Zanettini C, Barnes C, Solinas M, Goldberg SR (2013) Prior exposure to THC increases the addictive effects of nicotine in rats. Neuropsychopharmacology 38(7):1198–1208PubMedPubMedCentralCrossRefGoogle Scholar
  186. Panlilio LV, Hogarth L et al (2015) Concurrent access to nicotine and sucrose in rats. Psychopharmacology 232(8):1451–1460PubMedCrossRefGoogle Scholar
  187. Paterson NE, Markou A (2004) Prolonged nicotine dependence associated with extended access to nicotine self-administration in rats. Psychopharmacology 173(1–2):64–72PubMedCrossRefGoogle Scholar
  188. Perkins KA, Karelitz JL (2013a) Influence of reinforcer magnitude and nicotine amount on smoking’s acute reinforcement enhancing effects. Drug Alcohol Depend 133(1):167–171PubMedPubMedCentralCrossRefGoogle Scholar
  189. Perkins KA, Karelitz JL (2013b) Reinforcement enhancing effects of nicotine via smoking. Psychopharmacology 228(3):479–486PubMedPubMedCentralCrossRefGoogle Scholar
  190. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391(6663):173–177PubMedCrossRefGoogle Scholar
  191. Pickens R, Thompson T (1968) Cocaine-reinforced behavior in rats: effects of reinforcement magnitude and fixed-ratio size. J Pharmacol Exp Ther 161(1):122–129PubMedGoogle Scholar
  192. Pickens R, Thompson T (1970) Cocaine-reinforced behavior in rats: effects of reinforcement magnitude and fixed-ratio size. In: Thompson T, Pickens R, Meisch RA (eds) Readings in behavioral pharmacology. Meredith Corporation, New York, pp. 298–309Google Scholar
  193. Pinney JM (1979) Preface. In: Krasnegor NA (ed) Cigarette smoking as a dependence process, NIDA research monograph 23. U. S. Department of Health, Education, and Welfare, Washington, D. CGoogle Scholar
  194. Poling A, Byrne T (2000) Introduction to behavioral pharmacology. Context Press, RenoGoogle Scholar
  195. Pollin W. (1982) Statement of William Pollin, M. D., Director, National Institute on Drug Abuse. In: Comprehensive Smoking Prevention Education Act of 1981, Hearing before the Committee on Labor and Human Resources, United States Senate, Ninety-Seventh Congress, Second Session on S. 1929, To amend the Public Health Service Act and the Federal Cigarette Labeling and Advertising Act to increase the availability to the American public of information on the health consequences of smoking and thereby improve informed choice, and for other purposes, March 16, 1982. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  196. Pons S, Fattore L, Cossu G, Tolu S, Porcu E, McIntosh JM, Changeux JP, Maskos U, Fratta W (2008) Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 28(47):12318–12327PubMedPubMedCentralCrossRefGoogle Scholar
  197. Proctor RN (2012) Golden holocaust: origins of the cigarette catastrophe and the case for abolition. University of California Pres, Berkeley, CAGoogle Scholar
  198. Rauhut AS, Neugebauer N, Dwoskin LP, Bardo MT (2003) Effect of bupropion on nicotine self-administration in rats. Psychopharmacology 169(1):1–9PubMedCrossRefGoogle Scholar
  199. Rauhut AS, Dwoskin LP, Bardo MT (2005) Tolerance does not develop to the decrease in nicotine self-administration produced by repeated bupropion administration. Nicotine Tob Res 7(6):901–907PubMedCrossRefGoogle Scholar
  200. Risner ME, Goldberg SR (1983) A comparison of nicotine and cocaine self-administration in the dog: fixed-ratio and progressive-ratio schedules of intravenous drug infusion. J Pharmacol Exp Ther 224:319–326PubMedGoogle Scholar
  201. Roane HS (2008) On the applied use of progressive-ratio schedules of reinforcement. J Appl Behav Anal 41(2):155–161PubMedPubMedCentralCrossRefGoogle Scholar
  202. Rollema H, Coe JW et al (2007a) Rationale, pharmacology and clinical efficacy of partial agonists of alpha4beta2 nACh receptors for smoking cessation. Trends Pharmacol Sci 28(7):316–325PubMedCrossRefGoogle Scholar
  203. Rollema H, Chambers LK et al (2007b) Pharmacological profile of the alpha4beta2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid. Neuropharmacology 52(3):985–994PubMedCrossRefGoogle Scholar
  204. Rupprecht LE, Smith TT, Schassburger RL, Buffalari DM, Sved AF, Donny EC (2015) Behavioral mechanisms underlying nicotine reinforcement. Curr Top Behav Neurosci 24:19–53PubMedPubMedCentralCrossRefGoogle Scholar
  205. Russell MAH (1979) Tobacco dependence: is nicotine rewarding or aversive? In: Karsnegor NA (ed) Cigarette smoking as a dependence process, NIDA research monograph 23, Department of Health, Education, and Welfare. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  206. Schassburger RL, Levin ME, Weaver MT, Palmatier MI, Caggiula AR, Donny EC, Sved AF (2015) Differentiating the primary reinforcing and reinforcement-enhancing effects of varenicline. Psychopharmacology 232(5):975–983PubMedCrossRefGoogle Scholar
  207. Schassburger, R. L., E. M. Pitzer, T. T. Smith, L. E. Rupprecht, E. Thiels, E. C. Donny and A. F. Sved (2016) Adolescent rats self-administer less nicotine than adults at low doses. Nicotine Tob ResGoogle Scholar
  208. Scherma M, Panlilio LV et al (2008) Inhibition of anandamide hydrolysis by URB597 reverses abuse-related behavioral and neurochemical effects of nicotine in rats. J Pharmacol Exp Ther 327(2):482–490PubMedPubMedCentralCrossRefGoogle Scholar
  209. Scherma M, Muntoni AL et al (2016) Interactions between the endocannabinoid and nicotinic cholinergic systems: preclinical evidence and therapeutic perspectives. Psychopharmacology 233(10):1765–1177PubMedCrossRefGoogle Scholar
  210. Schindler CW, Redhi GH et al (2016) Blockade of nicotine and cannabinoid reinforcement and relapse by a cannabinoid CB1-receptor neutral antagonist AM4113 and inverse agonist rimonabant in squirrel monkeys. Neuropsychopharmacology 41(9):2283–2293PubMedCrossRefGoogle Scholar
  211. Schultz WB (1997) The FDA’s decision to regulate tobacco products. Pace L Rev 18(1):27–39Google Scholar
  212. Schuster CR (1991) Interview with Dr. Charles R. Schuster, interviewed by Dr. Robert Balster. In: The Centennial Project. American Psychological Association, Division of Psychopharmacology and Drug Abuse. http://apadivisions.org/division-28/about/history/centennial/schuster.pdf. Accessed 31 Aug 2016
  213. Schuster CR, Henningfield JE (2003) Conference on abuse liability assessment of CNS drugs. Drug Alcohol Depend 70(3 Suppl):S1–S4PubMedCrossRefGoogle Scholar
  214. Schuster CR, Thompson T (1962) Self-administration of morphine in physically dependent monkeys. University of Maryland, Laboratory of Psychopharmacology Technical Report no. 62–29Google Scholar
  215. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR) (2010) Addictiveness and attractiveness of tobacco additives. European Commission, Directorate-General for Health and Consumers, Scientific Committee on Emerging and Newly Identified Health Risks, European UnionGoogle Scholar
  216. Shihadeh A, Eissenberg T (2015) Electronic cigarette effectiveness and abuse liability: predicting and regulating nicotine flux. Nicotine Tob Res 17(2):158–162PubMedCrossRefGoogle Scholar
  217. Shoaib M (2008) The cannabinoid antagonist AM251 attenuates nicotine self-administration and nicotine-seeking behaviour in rats. Neuropharmacology 54(2):438–444PubMedCrossRefGoogle Scholar
  218. Shoaib M, Buhidma Y (2016) How can we improve on modeling nicotine addiction to develop better smoking cessation treatments? Int Rev Neurobiol 126:121–156PubMedCrossRefGoogle Scholar
  219. Shoaib M, Schindler WC et al (1997) Nicotine self-administration in rats: strain and nicotine pre-exposure effects on acquisition. Psychopharmacology 129(1):35–43PubMedCrossRefGoogle Scholar
  220. Shoaib M, Swanner LS, Yasar S, Goldberg SR (1999) Chronic caffeine exposure potentiates nicotine self-administration in rats. Psychopharmacology 142(4):327–333PubMedCrossRefGoogle Scholar
  221. Shoaib M, Sidhpura N et al (2003) Investigating the actions of bupropion on dependence-related effects of nicotine in rats. Psychopharmacology 165(4):405–412PubMedCrossRefGoogle Scholar
  222. Shram MJ, Funk D et al (2008) Nicotine self-administration, extinction responding and reinstatement in adolescent and adult male rats: evidence against a biological vulnerability to nicotine addiction during adolescence. Neuropsychopharmacology 33(4):739–748PubMedCrossRefGoogle Scholar
  223. Singer G, Simpson F, Lang WJ (1978) Schedule-induced self injections of nicotine with recovered body weight. Pharmacol Biochem Behav 9:387–389PubMedCrossRefGoogle Scholar
  224. Singer G, Wallace M, Hall R (1982) Effects of dopaminergic nucleus accumbens lesions on the acquisition of schedule induced self injections of nicotine in the rat. Pharmacol Biochem Behav 17:579–581PubMedCrossRefGoogle Scholar
  225. Smith LA, Lang WJ (1980) Changes occurring in self administration of nicotine by rats over a 28-day period. Pharmacol Biochem Behav 13:215–220PubMedCrossRefGoogle Scholar
  226. Smith TT, Levin ME, Schassburger RL, Buffalari DM, Sved AF, Donny EC (2013) Gradual and immediate nicotine reduction result in similar low-dose nicotine self-administration. Nicotine Tob Res 15(11):1918–1925PubMedPubMedCentralCrossRefGoogle Scholar
  227. Smith TT, Schassburger RL, Buffalari DM, Sved AF, Donny EC (2014) Low-dose nicotine self-administration is reduced in adult male rats naive to high doses of nicotine: implications for nicotine product standards. Exp Clin Psychopharmacol 22(5):453–459PubMedPubMedCentralCrossRefGoogle Scholar
  228. Smith TT, Schaff MB, Rupprecht LE, Schassburger RL, Buffalari DM, Murphy SE, Sved AF, Donny EC (2015) Effects of MAO inhibition and a combination of minor alkaloids, beta-carbolines, and acetaldehyde on nicotine self-administration in adult male rats. Drug Alcohol Depend 155:243–252PubMedPubMedCentralCrossRefGoogle Scholar
  229. Sorge RE, Clarke PBS (2009) Rats self-administer intravenous nicotine delivered in a novel smoking-relevant procedure: effects of dopamine antagonists. J Pharmacol Exp Ther 330(2):633–640PubMedCrossRefGoogle Scholar
  230. Spealman RD (1979) Behavior maintained by termination of a schedule of self-administered cocaine. Science 204:1231–1233PubMedCrossRefGoogle Scholar
  231. Spealman RD, Goldberg SR (1978) Drug self-administration by laboratory animals: control by schedules of reinforcement. Annu Rev Pharmacol Toxicol 18:313–339PubMedCrossRefGoogle Scholar
  232. Spealman RD, Goldberg SR (1982) Maintenance of schedule-controlled behavior by intravenous injections of nicotine in squirrel monkeys. J Pharmacol Exp Ther 223:402–408PubMedGoogle Scholar
  233. Spillane J, McAllister WB (2003) Keeping the lid on: a century of drug regulation and control. Drug Alcohol Depend 70:S5–S12PubMedCrossRefGoogle Scholar
  234. Stafford D, LeSage MG, Glowa JR (1998) Progressive-ratio schedules of drug delivery in the analysis of drug self-administration: a review. Psychopharmacology 139:169–184PubMedCrossRefGoogle Scholar
  235. Thompson T, Schuster CR (1964) Morphine self-administration, food-reinforced and avoidance behaviors in rhesus monkeys. Psychopharmacologia 5:87–94PubMedCrossRefGoogle Scholar
  236. Thompson T, Schuster CR (1968) Behavioral pharmacology. Prentice-Hall, Inc., Englewood Cliffs, NJGoogle Scholar
  237. Truth Initiative (2015) The truth about: electronic nicotine delivery systems. http://truthinitiative.org/sites/default/files/The_Truth_About_Electronic_Nicotine_Delivery_Systems.pdf. Accessed 20 Apr 2016
  238. U. S. Congress (2009) H.R. 1256: Family Smoking Prevention and Tobacco Control Act. 111th Congress, First SessionGoogle Scholar
  239. U. S. Department of Health and Human Services (1984a) Why people smoke cigarettes. Department of Health and Human Services, Public Health Service. U. S. Government Printing Office, Washington, D.CGoogle Scholar
  240. U. S. Department of Health and Human Services (1984b) Drug abuse and drug abuse research: the first in a series of triennial reports to Congress from the secretary, Department of Health and Human Services. Department of Health and Human Services, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute on Drug Abuse. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  241. U. S. Department of Health and Human Services (1988) The health consequences of smoking: nicotine addiction: a report of the Surgeon General. Department of Health and Human Services, Public Health Service, Centers for Disease Control, Center for Health Promotion and Education, Office on Smoking and Health. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  242. U. S. Department of Health and Human Services (2010) How tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the Surgeon General. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  243. U. S. Department of Health and Human Services (2014) The health consequences of smoking—50 years of progress: a report of the Surgeon General. Department of Health and Human Services, Public Health Service, Office of the Surgeon General. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  244. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health (2014) The health consequences of smoking – 50 years of progress: a report of the Surgeon General. – Atlanta, GAGoogle Scholar
  245. U. S. Department of Health, Education, and Welfare (1964) Smoking and health: report of the advisory committee to the Surgeon General of the Public Health Service. Department of Health, Education, and Welfare, Public Health Service. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  246. U. S. Department of Health, Education, and Welfare (1979) Smoking and health: a report of the Surgeon General. Department of Health, Education, and Welfare, Public Health Service, Office of the Assistant Secretary for Health, Office on Smoking and Health. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  247. U. S. House of Representatives (1982) Comprehensive Smoking Prevention Education Act: hearings before the Subcommittee on Health and Environment of the Committee on Energy and Commerce, House of Representatives, ninety-seventh Congress, second session on H. R. 5653 and H. R. 4957. March 5, 11, and 12, 1982. U. S. Government Printing Office, Washington, D. CGoogle Scholar
  248. U.S. District Court (2006) Amended Final Opinion. http://publichealthlawcenter.org/sites/default/files/resources/doj-final-opinion.pdf. Accessed 28 Apr 2016
  249. Vansickel AR, Weaver MF, Eissenberg T (2012) Clinical laboratory assessment of the abuse liability of an electronic cigarette. Addiction 107(8):1493–1500PubMedPubMedCentralCrossRefGoogle Scholar
  250. Wikler A (1965) Conditioning factors in opiate addiction and relapse. In: Wilner DI, Kassenbaum GG (eds) Narcotics. McGraw-Hill, New YorkGoogle Scholar
  251. Wikler A (1973) Dynamics of drug dependence: implications of a conditioning theory for research and treatment. Arch Gen Psychiatry 28:611–616PubMedCrossRefGoogle Scholar
  252. Wing VC, Shoaib M (2013) Effect of infusion rate on intravenous nicotine self-administration in rats. Behav Pharmacol 24(5 and 6):517–522PubMedCrossRefGoogle Scholar
  253. World Health Organization (WHO) (1994) International classification of diseases, 10 (ICD-10). Geneva, SwitzerlandGoogle Scholar
  254. World Health Organization (WHO) (2001) Monograph: advancing knowledge on regulating tobacco products. Geneva, SwitzerlandGoogle Scholar
  255. World Health Organization (WHO) (2007) The scientific basis of tobacco product regulation. WHO technical report series 945. Geneva, SwitzerlandGoogle Scholar
  256. World Health Organization (WHO) (2012) WHO study group on tobacco product regulation: Report on the scientific basis of tobacco product regulation: Fourth report of a WHO study group. WHO technical report series 967. Geneva, SwitzerlandGoogle Scholar
  257. World Health Organization (WHO) (2015) Global Nicotine Reduction Strategy: WHO study group on tobacco regulation. http://www.who.int/tobacco/publications/prod_regulation/nicotine-reduction/en/. Accessed 6 Sept 2016
  258. World Health Organization (WHO) (2016a) WHO Framework Convention on Tobacco Control. http://apps.who.int/iris/bitstream/10665/42811/1/9241591013.pdf. Accessed 21 Apr 2016
  259. World Health Organization (WHO) (2016b) WHO Expert Committee on Drug Dependence. http://www.who.int/medicines/access/controlled-substances/ecdd/en/. Accessed 12 Sept 2016
  260. Yan Y, Pushparaj A et al (2012) Blockade of dopamine D4 receptors attenuates reinstatement of extinguished nicotine-seeking behavior in rats. Neuropsychopharmacology 37(3):685–696PubMedCrossRefGoogle Scholar
  261. Yanagita T, Deneau MH, Seevers MH (1963) Methods for studying psychogenic dependence to opiates in the monkey. Bulletin, Drug Addiction and Narcotics, Appendix 16:3379–3385Google Scholar
  262. Yanagita T, Ando K, N Oinuma, K Ishida (1974) Intravenous self-administration of nicotine and an attempt to produce smoking behavior in monkeys. Proceedings of the 36th Annual Scientific Meeting, Committee on Problems of Drug Dependence, National Academy of SciencesGoogle Scholar
  263. Zilio D (2016) Who, what, and when: Skinner’s critiques of neuroscience and his main targets. The Behavior Analyst:1–22Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Jack E. Henningfield
    • 1
    • 2
    Email author
  • Tracy T. Smith
    • 3
    • 4
  • Bethea A. Kleykamp
    • 1
  • Reginald V. Fant
    • 1
  • Eric C. Donny
    • 5
  1. 1.Pinney AssociatesBethesdaUSA
  2. 2.Department of Psychiatry and Behavioral SciencesThe Johns Hopkins University School of MedicineBaltimoreUSA
  3. 3.University of Pittsburgh Cancer InstitutePittsburghUSA
  4. 4.Department of Epidemiology, Graduate School of Public HealthUniversity of PittsburghPittsburghUSA
  5. 5.Department of PsychologyUniversity of PittsburghPittsburghUSA

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