Abstract
Rationale
In animals, nicotine enhances reinforcement from stimuli unrelated to nicotine intake. Human research is suggestive but has not clearly shown a similar influence of nicotine.
Objectives
We assessed acute effects of nicotine via smoking on enhancement of positive (money, music) or negative (termination of noise) reinforcers, or no “reward” (control). These different rewards determined the generalizability of nicotine effects.
Materials and methods
Dependent (n = 25) and nondependent (n = 27) smokers participated in three sessions, each after overnight abstinence. Using a within-subjects design, sessions involved no smoking or smoking denicotinized (0.05 mg) or nicotine (0.6 mg) QuestR brand cigarettes. For comparison, a fourth session involved no abstinence prior to smoking one's own brand to gauge responses under typical nicotine satiation. Reinforcement was assessed by responses on a simple operant computer task for the rewards, each available singly on a progressive ratio schedule during separate trials.
Results
The reinforcing effect of music, but not other rewards, was greater due to the nicotine cigarette, compared to the denicotinized cigarette or no smoking. Reinforcement enhancing effects of nicotine did not differ between dependent and nondependent groups, indicating no influence of withdrawal relief. Responding due to acute nicotine after abstinence was very similar to responding to one's own brand after no abstinence.
Conclusions
Acute nicotine intake per se from smoking after abstinence enhances the reinforcing value of rewards unassociated with smoking, perhaps in a manner comparable to ad lib smoking after no abstinence. Nicotine's reinforcement enhancing effects may be specific to certain rewards, perhaps those sensory in nature.
Similar content being viewed by others
References
Addicott MA, Baranger DAA, Kozink RV, Smoski MJ, Dichter GS, McClernon FJ (2012) Smoking withdrawal is associated with increases in brain activation during decision making and reward anticipation: a preliminary study. Psychopharmacology 219:563–573
American Psychiatric Association (APA) (1994) Diagnostic and statistical manual-IV. American Psychiatric Association, Washington DC
Attwood AS, Penton-Voak IS, Munafo MR (2009) Effects of acute nicotine administration on ratings of attractiveness of facial cues. Nic Tobacco Res 11:44–48
Baker TB, Piper ME, McCarthy DE, Majeskie MR, Fiore MC (2004) Addiction motivation reformulated: an affective processing model of negative reinforcement. Psychol Rev 1:33–51
Barr RS, Pizzagalli DA, Culhane MA, Goff DC, Evins AE (2008) A single dose of nicotine enhances reward responsiveness in nonsmokers: implications for development of dependence. Biol Psychiatr 63:1061–1065
Breslau N, Kilbey MM, Andreski P (1994) DSM-IIIR nicotine dependence in young adults: prevalence, correlates, and associated psychiatric disorders. Addiction 89:743–754
Caggiula AR, Donny EC, Palmatier M, Liu X, Chaudhri N, Sved A (2009) The role of nicotine in smoking: a dual-reinforcement model. In: Bevins RA, Caggiula AR (eds) The motivational impact of nicotine and its role in tobacco use, Nebraska symposium on motivation, vol 55. Springer-Verlag, New York, pp 91–109
Caggiula AR, Donny EC, White AR, Chaudhri N, Booth S, Gharib MA, Hoffman A, Perkins KA, Sved AF (2001) Cue dependency of nicotine self-administration and smoking. Pharmacol Biochem Behav 70:515–530
Chaudhri N, Caggiula AR, Donny EC, Palmatier MI, Liu X, Sved AF (2006) Complex interactions between nicotine and nonpharmacological stimuli reveal multiple roles for nicotine in reinforcement. Psychopharmacology 184:353–366
Cohen J (1988) Statistical power analysis for the social sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale NJ
Dawkins L, Acaster S, Powell JH (2007) The effects of smoking and abstinence on experience of happiness and sadness in response to positively valenced, negatively valenced, and neutral film clips. Addict Behav 32:425–431
Dawkins L, Powell JH, West R, Powell J, Pickering A (2006) A double-blind placebo controlled experimental study of nicotine: I—effects on incentive motivation. Psychopharmacology 189:355–367
Epstein LH, Bulik CM, Perkins KA, Caggiula AC, Rodefer J (1991) Behavioral economic analysis of smoking: money and food as alternatives. Pharmacol Biochem Behav 38:715–721
Evans DE, Drobes DJ (2009) Nicotine self-medication of cognitive-attentional processing. Addict Biol 14:32–42
Fowler H (1971) Implications of sensory reinforcement. In: Glaser R (ed) The nature of reinforcement. Academic Press, New York, pp 151–195
Guy EG, Fletcher PJ (2013) Nicotine-induced enhancement of responding for conditioned reinforcement in rats: role of prior nicotine exposure and α4β2 nicotinic receptors. Psychopharmacology 225:429–440
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 175:134–142
Hatsukami DK, Morgan SR, Pickens RW, Champagne SE (1990) Situational factors in cigarette smoking. Addict Behav 15:1–12
Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom K-O (1991) The fagerstrom test for nicotine dependence: a revision of the fagerstrom tolerance questionnaire. Br J Addiction 86:1119–1127
Honig WK, Staddon JER (1977) Handbook of operant behavior. Prentice-Hall, Englewood Cliffs NJ
Hughes JR, Hatsukami DK (2007) Instructions for use of the Minnesota Withdrawal Scale-Revised. Retrieved from www.uvm.edu/∼hbpl
Huitema B (1980) Analysis of covariance and alternatives. John Wiley & Sons, New York
Kenny PJ, Markou A (2006) Nicotine self-administration acutely activates brain reward systems and induces a long-lasting increase in reward sensitivity. Neuropsychopharmacol 31:1203–1211
Klinkenberg I, Blokland A, Riedel AJ, Sambeth A (2013) Cholinergic modulation of auditory processing, sensory gating and novelty detection in human participants. Psychopharmacology 225:903–921
Lee EM, Malson JL, Waters AJ, Moolchan ET, Pickworth WB (2003) Smoking topography: reliability and validity in dependent smokers. Nic Tobacco Res 5:673–679
LeFoll B, Goldberg SR (2006) Nicotine as a typical drug of abuse in experimental animals and humans. Psychopharmacology 184:367–381
Lloyd DR, Kausch MA, Gancarz AM, Beyley LJ, Richards JB (2012) Effects of novelty and methamphetamine on conditioned and sensory reinforcement. Behav Brain Res 234:312–322
McGrath DS, Barrett SP, Stewart SH, Schmid EA (2012) The effects of acute doses of nicotine on video lottery terminal gambling in daily smokers. Psychopharmacology 220:155–161
Norman WD, Jongerius JL (1985) Apple picker: computer software for studying human responding on concurrent and multiple schedules. Behav Res Meth Instr Comput 17:222–225
O’Dell LE, Khroyan TV (2009) Rodent models of nicotine reward: what do they tell us about tobacco abuse in humans? Pharmacol Biochem Behav 91:481–488
Olausson P, Jentsch JD, Taylor JR (2004) Nicotine enhances responding with conditioned reinforcement. Psychopharmacology 171:173–178
Palmatier MI, O’Brien LC, Hall MJ (2012) The role of conditioning history and reinforcer strength in the reinforcement enhancing effects of nicotine in rats. Psychopharmacology 219:1119–1131
Paterson NE (2009) The neuropharmacological substrates of nicotine reward: reinforcing versus reinforcement-enhancing effects of nicotine. Behav Pharmacol 20:211–225
Perkins KA, Epstein LH, Grobe JE, Fonte C (1994) Tobacco abstinence, smoking cues, and the reinforcing value of smoking. Pharmacol Biochem Behav 47:107–112
Perkins KA, Grobe JE, Fonte C (1997) The influence of acute smoking exposure on the subsequent reinforcing value of smoking. Exper Clin Psychopharmacol 5:277–285
Perkins KA, Grottenthaler A, Wilson AS (2009) Lack of reinforcement-enhancing effects of nicotine in non-dependent smokers. Psychopharmacology 205:635–645
Perkins KA, Karelitz JL, Conklin CA, Sayette MA, Giedgowd GE (2010) Acute negative affect relief from smoking depends on the affect measure and situation, but not on nicotine. Biol Psychiatry 67:707–714
Perkins KA, Karelitz JL, Giedgowd GE, Conklin CA (2012) The reliability of puff topography and subjective responses during ad lib smoking of a single cigarette. Nic Tobacco Res 14:490–494
Perkins KA, Karelitz JL, Jao NC, Stratton E (2013). Possible reinforcement enhancing effects of bupropion during initial smoking abstinence. Nic Tobacco Res, in press. Online access. doi:10.1093/ntr/nts224.
Powell J, Dawkins L, Davis RE (2002) Smoking, reward responsiveness, and response inhibition: tests of an incentive motivational model. Biol Psychiatry 51:151–163
Raiff BR, Dallery J (2008) The generality of nicotine as a reinforcer enhancer in rats: effects on responding maintained by primary and conditioned reinforcers and resistance to extinction. Psychopharmacology 201:305–314
Raiff BR, Jarvis BP, Rapoza D (2012) Prevalence of video game use, cigarette smoking, and acceptability of a video-game based smoking cessation intervention among online adults. Nic Tobacco Res 14:63–77
Rose JE, Salley A, Behm FM, Bates JE, Westman EC (2010) Reinforcing effects of nicotine and non-nicotine components of cigarette smoke. Psychopharmacology 210:1–12
Salamone JD (2006) Will the last person who uses the term “reward” please turn out the lights? Comments on processes related to reinforcement, learning, motivation, and effort. Addiction Biol 11:43–44
Shadel WG, Martino SC, Setodji C, Cervone D, Witkiewitz K, Beckjord EG, Scharf D, Shih R (2011) Lapse-induced surges in craving influence relapse in adult smokers: an experimental investigation. Health Psychol 30:588–596
Sheppard AB, Gross SC, Pavelka SA, Hall MJ, Palmatier MI (2012) Caffeine increases the motivation to obtain nondrug reinforcers in rats. Drug Alc Depend 124:216–222
Shiffman S (1989) Tobacco “chippers”—individual differences in tobacco dependence. Psychopharmacology 97:539–547
Snuggs S, Hajek P (2013) Responsiveness to reward following cessation of smoking. Psychopharmacology 225:869–873
SRNT subcommittee, (2002) Biochemical verification of tobacco use and cessation. Nic Tobacco Res 4:149–159
Van Gucht D, Van den Bergh O, Beckers T, Vansteenwagen D (2010) Smoking behavior in context: where and when do people smoke? J Behav Ther Exp Psychiatry 41:172–177
Van Voorhees EE, Mitchell JT, McClernon FJ, Beckham JC, Kollins SH (2012) Sex, ADHD, and smoking outcomes: an integrative model. Med Hypoth 78:585–593
Wise R (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend 51:13–22
Acknowledgment
This research was supported by NIH Grant DA31218 (KAP). Neither author has any potential conflicts of interest to report.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Perkins, K.A., Karelitz, J.L. Reinforcement enhancing effects of nicotine via smoking. Psychopharmacology 228, 479–486 (2013). https://doi.org/10.1007/s00213-013-3054-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-013-3054-4