Nicotine enhances the expression of a sucrose or cocaine conditioned place preference in adult male rats

Pharmacology Biochemistry and Behavior

Volumn 124, Issue , 2014, Pages 320-325

  Buffalari, Deanne M ^a   Marfo, Nana Yaa A ^a   Smith, Tracy T ^a   Levin, Melissa E ^a   Weaver, Matthew T ^b   Thiels, Edda ^a   Sved, Alan F ^a   Donny, Eric C ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MERCYHURST COLLEGE   (United States)

Author keywords

Cocaine; Conditioned place preference; Enhancement; Nicotine; Reinforcement; Sucrose

Indexed keywords

COCAINE; NICOTINE; SUCROSE;

ADULT; ADULT ANIMAL; ANIMAL EXPERIMENT; ARTICLE; CONDITIONED PLACE PREFERENCE TEST; CONTROLLED STUDY; FOOD DRUG INTERACTION; MALE; MOTIVATION; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; REINFORCEMENT; ANIMAL; CONDITIONED REFLEX; SPRAGUE DAWLEY RAT;

ANIMALS; COCAINE; CONDITIONING, CLASSICAL; MALE; NICOTINE; RATS; RATS, SPRAGUE-DAWLEY; SUCROSE;

EID: 84904545511     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2014.06.013     Document Type: Article

References (71)

1. J.U. Adams, J.M. Careri, T.R. Efferen, and J. Rotrosen Differential effects of dopamine antagonists on locomotor activity, conditioned activity and conditioned place preference induced by cocaine in rats Behav Pharmacol 12 2001 603 611 (Pubitemid 34017106)
2. A. Agmo, A. Galvan, and B. Talamantes Reward and reinforcement produced by drinking sucrose: two processes that may depend on different neurotransmitters Pharmacol Biochem Behav 52 1995 403 414
3. M.A. Aguilar, M. Rodriguez-Arias, and J. Minarro Neurobiological mechanisms of the reinstatement of drug-conditioned place preference Brain Res Rev 59 2009 253 277
4. J.C. Anthony, A.L. Warner, and R.C. Kessler Comparative epidemiology of dependence on tobacco, alcohol, controlled substances, and inhalants: basic findings from the national comorbidity survey Exp Clin Psychopharmacol 2 1994 224 268
5. S.T. Barret, and R.A. Bevins Nicotine enhances operant responding for qualitatively distinct reinforcers under maintenance and extinction conditions Pharmacol Biochem Behav 114-115 2013 9 15
6. S.T. Barrett, and R.A. Bevins A quantitative analysis of the reward-enhancing effects of nicotine using reinforcer demand Behav Pharmacol 23 2012 781 789
7. L. Bellinger, A. Cepeda-Benito, and P.J. Wellman Meal patterns in male rats during and after intermittent nicotine administration Pharmacol Biochem Behav 74 2003 495 504 (Pubitemid 35449536)
8. L.L. Bellinger, P.J. Wellman, A. Cepeda-Benito, P.R. Kramer, G. Guan, and C.M. Tillberg et al. Meal patterns in female rats during and after intermittent nicotine administration Pharmacol Biochem Behav 80 2005 437 444 (Pubitemid 40299345)
9. R.A. Bevins, and A.R. Caggiula Nicotine, tobacco use, and the 55th Nebraska Symposium on Motivation Nebr Symp Motiv 55 2009 1 3
10. V. Blaha, Z.J. Yang, M. Meguid, J.K. Chai, and Z. Zadak Systemic nicotine administration suppresses food intake via reduced meal sizes in both male and female rats Acta Medica (Hradec Kralove) 41 1998 167 173
11. A.J. Brewer III, J.J. Mahoney III, C.S. Nerumalla, T.F. Newton, and R. De la Garza II The influence of smoking cigarettes on the high and desire for cocaine among active cocaine users Pharmacol Biochem Behav 106 2013 132 136
12. A.J. Budney, S.T. Higgins, J.R. Hughes, and W.K. Bickel Nicotine and caffeine use in cocaine-dependent individuals J Subst Abuse 5 1993 117 130
13. B. Budzynska, and G. Biala Effects of bupropion on the reinstatement of nicotine-induced conditioned place preference by drug priming in rats Pharmacol Rep 63 2011 362 371
14. A.R. Caggiula, E.C. Donny, A.R. White, N. Chaudhri, S. Booth, and M.A. Gharib et al. Cue dependency of nicotine self-administration and smoking Pharmacol Biochem Behav 70 2001 515 530 (Pubitemid 34131646)
15. A.R. Caggiula, E.C. Donny, M.I. Palmatier, X. Liu, N. Chaudhri, and A.F. Sved The role of nicotine in smoking: a dual-reinforcement model Nebr Symp Motiv 55 2009 91 109
16. R.N. Cassidy, and J. Dallery Effects of economy type and nicotine on the essential value of food in rats J Exp Anal Behav 97 2012 183 202
17. N. Chaudhri, A.R. Caggiula, E.C. Donny, S. Booth, M. Gharib, and L. Craven et al. Operant responding for conditioned and unconditioned reinforcers in rats is differentially enhanced by the primary reinforcing and reinforcement-enhancing effects of nicotine Psychopharmacology (Berl) 189 2006 27 36 (Pubitemid 44607257)
18. N. Chaudhri, A.R. Caggiula, E.C. Donny, M.I. Palmatier, X. Liu, and A.F. Sved Complex interactions between nicotine and nonpharmacological stimuli reveal multiple roles for nicotine in reinforcement Psychopharmacology (Berl) 184 2006 353 366 (Pubitemid 43255852)
19. C. Chiamulera, C. Borgo, S. Falchetto, E. Valerio, and M. Tessari Nicotine reinstatement of nicotine self-administration after long-term extinction Psychopharmacology (Berl) 127 1996 102 107 (Pubitemid 26298006)
20. C.A. Conklin, and S.T. Tiffany The impact of imagining personalized versus standardized urge scenarios on cigarette craving and autonomic reactivity Exp Clin Psychopharmacol 9 2001 399 408 (Pubitemid 33117491)
21. R.I. Desai, and P. Terry Evidence of cross-tolerance between behavioural effects of nicotine and cocaine in mice Psychopharmacology (Berl) 166 2003 111 119 (Pubitemid 36313117)
22. E.C. Donny, N. Chaudhri, A.R. Caggiula, F.F. Evans-Martin, S. Booth, and M.A. Gharib et al. Operant responding for a visual reinforcer in rats is enhanced by noncontingent nicotine: implications for nicotine self-administration and reinforcement Psychopharmacology (Berl) 169 2003 68 76 (Pubitemid 37088616)
23. E.C. Donny, A.R. Caggiula, M.T. Weaver, M.E. Levin, and A.F. Sved The reinforcement-enhancing effects of nicotine: implications for the relationship between smoking, eating and weight Physiol Behav 104 2011 143 148
24. W.M. Doyon, A.M. Thomas, A. Ostroumov, Y. Dong, and J.A. Dani Potential substrates for nicotine and alcohol interactions: a focus on the mesocorticolimbic dopamine system Biochem Pharmacol 86 2013 1181 1193
25. D.H. Epstein, G.F. Marrone, S.J. Heishman, J. Schmittner, and K.L. Preston Tobacco, cocaine, and heroin: craving and use during daily life Addict Behav 35 2010 318 324
26. H. Frenk, and R. Dar Reward potentiation or behavioral activation? A comment on Donny et al. Psychopharmacology (Berl) 171 2004 472 473 [author reply 474-476]
27. A. Geier, R.F. Mucha, and P. Pauli Appetitive nature of drug cues confirmed with physiological measures in a model using pictures of smoking Psychopharmacology (Berl) 150 2000 283 291 (Pubitemid 30447848)
28. S.R. Goldberg, R.D. Spealman, and D.M. Goldberg Persistent behavior at high rates maintained by intravenous self-administration of nicotine Science 214 1981 573 575 (Pubitemid 12206158)
29. R.W. Gould, P.W. Czoty, S.H. Nader, and M.A. Nader Effects of varenicline on the reinforcing and discriminative stimulus effects of cocaine in rhesus monkeys J Pharmacol Exp Ther 339 2011 678 686
30. S.M. Graves, and T.C. Napier Mirtazapine alters cue-associated methamphetamine seeking in rats Biol Psychiatry 69 2011 275 281
31. N.E. Grunberg, S.E. Winders, and K.A. Popp Sex differences in nicotine's effects on consummatory behavior and body weight in rats Psychopharmacology (Berl) 91 1987 221 225 (Pubitemid 17002278)
32. G.C. Harris, and G. Aston-Jones Critical role for ventral tegmental glutamate in preference for a cocaine-conditioned environment Neuropsychopharmacology 28 2003 73 76
33. J.E. Henningfield, R. Clayton, and W. Pollin Involvement of tobacco in alcoholism and illicit drug use Br J Addict 85 1990 279 291
34. Y.Y. Huang, D.B. Kandel, E.R. Kandel, and A. Levine Nicotine primes the effect of cocaine on the induction of LTP in the amygdala Neuropharmacology 74 2013 126 134
35. Y.H. Jo, D.A. Talmage, and L.W. Role Nicotinic receptor-mediated effects on appetite and food intake J Neurobiol 53 2002 618 632 (Pubitemid 35375591)
36. A. Levine, Y. Huang, B. Drisaldi, E.A. Griffin Jr., D.D. Pollak, and S. Xu et al. Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine Sci Transl Med 3 2011 107 109
37. H. Li, Q. Bu, B. Chen, X. Shao, Z. Hu, P. Deng, L. Lv, Y. Deng, R. Zhu, Y. Li, B. Zhang, J. Hou, C. Du, Q. Zhao, D. Fu, Y. Zhao, and X. Cen Mechanisms of metabonomic for a gateway drug: nicotine priming enhances behavioral response to cocaine with modification in energy metabolism and neurotransmitter level PLoS One 9 2014 e87040
38. N.K. Mello, and J.L. Newman Discriminative and reinforcing stimulus effects of nicotine, cocaine, and cocaine + nicotine combinations in rhesus monkeys Exp Clin Psychopharmacol 19 2011 203 214
39. G. Miyata, M.M. Meguid, M. Varma, S.O. Fetissov, and H.J. Kim Nicotine alters the usual reciprocity between meal size and meal number in female rat Physiol Behav 74 2001 169 176 (Pubitemid 32879374)
40. D. Mueller, and J. Stewart Cocaine-induced conditioned place preference: reinstatement by priming injections of cocaine after extinction Behav Brain Res 115 2000 39 47
41. S.G. Nair, S.M. Gray, and U.E. Ghitza Role of food type in yohimbine- and pellet-priming-induced reinstatement of food seeking Physiol Behav 88 2006 559 566 (Pubitemid 44109874)
42. P. Olausson, J.D. Jentsch, and J.R. Taylor Nicotine enhances responding with conditioned reinforcement Psychopharmacology (Berl) 171 2004 173 178 (Pubitemid 38134654)
43. M.I. Palmatier, F.F. Evans-Martin, A. Hoffman, A.R. Caggiula, N. Chaudhri, and E.C. Donny et al. Dissociating the primary reinforcing and reinforcement-enhancing effects of nicotine using a rat self-administration paradigm with concurrently available drug and environmental reinforcers Psychopharmacology (Berl) 184 2006 391 400 (Pubitemid 43255855)
44. M.I. Palmatier, X. Liu, A.R. Caggiula, E.C. Donny, and A.F. Sved The role of nicotinic acetylcholine receptors in the primary reinforcing and reinforcement-enhancing effects of nicotine Neuropsychopharmacology 32 2007 1098 1108 (Pubitemid 46631984)
45. M.I. Palmatier, X. Liu, G.L. Matteson, E.C. Donny, A.R. Caggiula, and A.F. Sved Conditioned reinforcement in rats established with self-administered nicotine and enhanced by noncontingent nicotine Psychopharmacology (Berl) 195 2007 235 243 (Pubitemid 350045848)
46. M.I. Palmatier, G.L. Matteson, J.J. Black, X. Liu, A.R. Caggiula, and L. Craven et al. The reinforcement enhancing effects of nicotine depend on the incentive value of non-drug reinforcers and increase with repeated drug injections Drug Alcohol Depend 89 2007 52 59 (Pubitemid 46604860)
47. M.I. Palmatier, L.C. O'Brien, and M.J. Hall The role of conditioning history and reinforcer strength in the reinforcement enhancing effects of nicotine in rats Psychopharmacology (Berl) 219 2012 1119 1131
48. L.A. Parker, and K. Doucet The effects of nicotine and nicotine withdrawal on taste reactivity Pharmacol Biochem Behav 52 1995 125 129
49. K.A. Perkins, L.H. Epstein, J. Grobe, and C. Fonte Tobacco abstinence, smoking cues, and the reinforcing value of smoking Pharmacol Biochem Behav 47 1994 107 112
50. B.R. Raiff, and J. Dallery Effects of acute and chronic nicotine on responses maintained by primary and conditioned reinforcers in rats Exp Clin Psychopharmacol 14 2006 296 305 (Pubitemid 44267473)
51. A.S. Rauhut, L. Fenton, and M.T. Bardo Renewal of sucrose-seeking behavior in rats: role of D(2) dopamine receptors Pharmacol Biochem Behav 96 2010 354 362
52. M.S. Reid, J.D. Mickalian, K.L. Delucchi, S.M. Hall, and S.P. Berger An acute dose of nicotine enhances cue-induced cocaine craving Drug Alcohol Depend 49 1998 95 104 (Pubitemid 28111896)
53. M.E. Rice, and S.J. Cragg Nicotine amplifies reward-related dopamine signals in striatum Nat Neurosci 7 2004 583 584 (Pubitemid 38691894)
54. K.P. Richter, H.K. Ahluwalia, M.C. Mosier, N. Nazir, and J.S. Ahluwalia A population-based study of cigarette smoking among illicit drug users in the United States Addiction 97 2002 861 869 (Pubitemid 34729101)
55. J.E. Rose, and F.M. Behm Psychophysiological interactions between caffeine and nicotine Pharmacol Biochem Behav 38 1991 333 337
56. J.E. Rose, and W.A. Corrigall Nicotine self-administration in animals and humans: similarities and differences Psychopharmacology (Berl) 130 1997 28 40 (Pubitemid 27107782)
57. J.E. Rose, and E.D. Levin Inter-relationships between conditioned and primary reinforcement in the maintenance of cigarette smoking Br J Addict 86 1991 605 609
58. J.E. Rose, F.M. Behm, E.C. Westman, and M. Johnson Dissociating nicotine and nonnicotine components of cigarette smoking Pharmacol Biochem Behav 67 2000 71 81
59. R.L. Schassburger, L.E. Rupprecht, T.T. Smith, D.M. Buffalari, E. Thiels, and E.C. Donny et al. Nicotine enhances the rewarding properties of sucrose, program no. 545.30 Neuroscience 2013 [Abstracts 2013; San Diego, California: Online]
60. Y. Shaham, U. Shalev, L. Lu, H. De Wit, and J. Stewart The reinstatement model of drug relapse: history, methodology and major findings Psychopharmacology (Berl) 168 2003 3 20 (Pubitemid 36851158)
61. S. Shoptaw, M.E. Jarvik, W. Ling, and R.A. Rawson Contingency management for tobacco smoking in methadone-maintained opiate addicts Addict Behav 21 1996 409 412 (Pubitemid 26162235)
62. J.A. Simms, J.K. Richards, D. Mill, I. Kanholm, J.Y. Holgate, and S.E. Bartlett Induction of multiple reinstatements of ethanol- and sucrose-seeking behavior in Long - Evans rats by the alpha-2 adrenoreceptor antagonist yohimbine Psychopharmacology (Berl) 218 2011 101 110
63. M.A. Sullivan, and L.S. Covey Current perspectives on smoking cessation among substance abusers Curr Psychiatry Rep 4 2002 388 396
64. H. Sun, M.L. Shen, Y.P. Pang, O. Lockridge, and S. Brimijoin Cocaine metabolism accelerated by a re-engineered human butyrylcholinesterase J Pharmacol Exp Ther 302 2002 710 716 (Pubitemid 34787239)
65. K.J. Thiel, F. Sanabria, and J.L. Neisewander Synergistic interaction between nicotine and social rewards in adolescent male rats Psychopharmacology (Berl) 204 2009 391 402
66. U.S. Department of Health and Human Services The Health Consequences of Smoking - 50 years of progress: A report of the Surgeon General 2014 GA Centers for Disease Control and Prevention Atlanta
67. F. Weiss, C.S. Maldonado-Vlaar, L.H. Parsons, T.M. Kerr, D.L. Smith, and O. Ben-Shahar Control of cocaine-seeking behavior by drug-associated stimuli in rats: effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens Proc Natl Acad Sci U S A 97 2000 4321 4326 (Pubitemid 30226131)
68. P.J. Wellman, L.L. Bellinger, A. Cepeda-Benito, A. Susabda, D.H. Ho, and K.W. Davis Meal patterns and body weight after nicotine in male rats as a function of chow or high-fat diet Pharmacol Biochem Behav 82 2005 627 634 (Pubitemid 43184038)
69. N.M. White, and G.D. Carr The conditioned place preference is affected by two independent reinforcement processes Pharmacol Biochem Behav 23 1985 37 42 (Pubitemid 15048986)
70. V.C. Wing, and M. Shoaib A second-order schedule of food reinforcement in rats to examine the role of CB1 receptors in the reinforcement-enhancing effects of nicotine Addict Biol 15 2010 380 392
71. W. Zhou, F. Zhang, S. Tang, H. Liu, J. Gu, and G. Yang The dissociation of heroin-seeking patterns induced by contextual, discriminative, or discrete conditioned cues in a model of relapse to heroin in rats Psychopharmacology (Berl) 181 2005 197 206 (Pubitemid 41492189)