Skip to main content
SpringerLink
Log in

The effects of nicotine dependence and acute abstinence on the processing of drug and non-drug rewards

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Drug addiction may be characterised by a hypersensitivity to drug rewards and a hyposensitivity to non-drug rewards. This imbalance may become further polarised during acute abstinence.

Objectives

(i) Examine the differences between dependent and occasional smokers in choices for, motivation for and self-reported wanting and liking of cigarette and non-drug rewards. (ii) Examine the effects of 12-h nicotine abstinence on these metrics.

Methods

Dependent (n = 20) and occasional, non-dependent smokers (n = 20) were tested after ad libitum smoking and ≥12-h of nicotine abstinence. A novel task was developed (Drug, Reward and Motivation–Choice (DReaM-Choice)) in which different rewards (cigarettes, music and chocolate) could be won. In each trial, participants chose between two rewards and then could earn the chosen reward via repeated button-pressing. Participants subsequently ‘consumed’ and rated subjective liking of the rewards they had won.

Results

Compared with occasional smokers, dependent smokers made more choices for (p < 0.001), pressed more for (p = 0.046) and reported more wanting (p = 0.007) and liking (p < 0.001) of cigarettes, and also made fewer choices for chocolate (p = 0.005). There were no differences between the groups on button-pressing for chocolate or music. However, the balance between drug and non-drug reward processing was different between the groups across all metrics. Twelve-hour nicotine abstinence led to more cigarette choices (p < 0.001) and fewer music choices (p = 0.042) in both groups.

Conclusions

Nicotine dependence was associated with a hypersensitivity to cigarette rewards, but we found little evidence indicating a hyposensitivity to non-drug rewards. Our findings question the moderating influence of dependence on how acute nicotine abstinence affects reward processing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Notes

  1. It should be noted that the term ‘reward’ will refer to the options in the task (e.g. ‘large chocolate’, ‘small cigarette’), and the term ‘delivered reward’ will refer to the actual things participants get afterwards (e.g. 1.25 cigarettes, 3.5 min of music).

  2. If one of the rewards was never selected, e.g. ‘paper small’, the BP for that outcome was set to 0.

  3. Two participants did not complete the experiment due to having too high a CO reading on the abstinent session.

  4. Data for how many days per week participants listen to music and eat chocolate and liking ratings of these activities were missing for one participant in the dependent group

  5. Nineteen out of 140 data points were missing due to some participants not consuming all of their rewards.

References

  • Acker J, Mackillop J (2013) Behavioural economic analysis of cue-elicited craving for tobacco: a virtual reality study. Nicotine Tob Res 15:1409–1416

    Article  PubMed Central  PubMed  Google Scholar 

  • al’Absi M, Hatsukami D, Davis GL, Wittmers LE (2004) Prospective examination of effects of smoking abstinence on cortisol and withdrawal symptoms as predictors of early smoking relapse. Drug Alcohol Depend 73:267–278

    Article  PubMed  Google Scholar 

  • Al-Adawi S, Powell J (1997) The influence of smoking on reward responsiveness and cognitive functions: a natural experiment. Addiction 92:1773–1782

    Article  CAS  PubMed  Google Scholar 

  • American Psychiatric Association (2013) The diagnostic and statistical manual of mental disorders: DSM 5. Bookpoint US

  • Anselme P (2009) The effect of exposure to drugs on the processing of natural rewards. Neurosci Biobehav Rev 33:314–335

    Article  CAS  PubMed  Google Scholar 

  • Baddeley A, Emslie H, Nimmo-Smith I (1993) The Spot-the-Word test: a robust estimate of verbal intelligence based on lexical decision. Br J Clin Psychol 32:55–65

    Article  PubMed  Google Scholar 

  • Beck AT, Steer RA, Ball R, Ranieri WF (1996) Comparison of beck depression inventories-IA and-II in psychiatric outpatients. J Pers Assess 67:588–597

    Article  CAS  PubMed  Google Scholar 

  • Beck A, Schlagenhauf F, Wüstenberg T, Hein J, Kienast T, Kahnt T, Schmack K, Hägele C, Knutson B, Heinz A (2009) Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol Psychiatry 66:734–742

    Article  CAS  PubMed  Google Scholar 

  • Benowitz NL, Jacob P, Hall S, Tsoh J, Ahijevych K, Jarvis M, LeHouezec J, Hansson A, Lichtenstein E, Henningfield J (2002) Biochemical verification of tobacco use and cessation. Nicotine Tob Res 4:149–159

    Article  Google Scholar 

  • Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev 28:309–369

    Article  CAS  PubMed  Google Scholar 

  • Bjork JM, Smith AR, Hommer DW (2008) Striatal sensitivity to reward deliveries and omissions in substance dependent patients. Neuroimage 42:1609–1621

    Article  PubMed Central  PubMed  Google Scholar 

  • Blum K, Braverman ER, Holder JM, Lubar JF, Monastra VJ, Miller D, Lubar JO, Chen TJ, Comings DE (2000) The reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive and compulsive behaviors. J Psychoactive Drugs 32:1–112

    Article  Google Scholar 

  • Bühler M, Vollstädt-Klein S, Kobiella A, Budde H, Reed LJ, Braus DF, Büchel C, Smolka MN (2010) Nicotine dependence is characterized by disordered reward processing in a network driving motivation. Biol Psychiatry 67:745–752

    Article  PubMed  Google Scholar 

  • David SP, Munafò MR, Johansen-Berg H, Smith SM, Rogers RD, Matthews PM, Walton RT (2005) Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study. Biol Psychiatry 58:488–494

    Article  PubMed Central  PubMed  Google Scholar 

  • 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. Psychopharmacol (Berl) 189:355–367

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • de Wit H, Uhlenhuth E, Johanson C (1986) Individual differences in the reinforcing and subjective effects of amphetamine and diazepam. Drug Alcohol Depend 16:341–360

    Article  PubMed  Google Scholar 

  • Donny EC, Bigelow GE, Walsh SL (2003) Choosing to take cocaine in the human laboratory: effects of cocaine dose, inter-choice interval, and magnitude of alternative reinforcement. Drug Alcohol Depend 69:289–301

    Article  CAS  PubMed  Google Scholar 

  • Epstein LH, Bulik CM, Perkins KA, Caggiula AR, Rodefer J (1991) Behavioral economic analysis of smoking: money and food as alternatives. Pharmacol Biochem Behav 38:715–721

    Article  CAS  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489

    Article  CAS  PubMed  Google Scholar 

  • Fagerstrom K (2012) Determinants of tobacco use and renaming the FTND the Fagerstrom Test for Cigarette Dependence. Nicotine Tob Res 14:75–78

    Article  PubMed  Google Scholar 

  • Fergusson DM, Horwood LJ, Lynskey MT, Madden PA (2003) Early reactions to cannabis predict later dependence. Arch Gen Psychiatry 60:1033–1039

    Article  PubMed  Google Scholar 

  • Fiorino DF, Phillips AG (1999) Facilitation of sexual behavior and enhanced dopamine efflux in the nucleus accumbens of male rats after d-amphetamine-induced behavioral sensitization. J Neurosci 19:456–463

    CAS  PubMed  Google Scholar 

  • Freeman T, Morgan C, Beesley T, Curran H (2012) Drug cue induced overshadowing: selective disruption of natural reward processing by cigarette cues amongst abstinent but not satiated smokers. Psychol Med 42:161

    Article  CAS  PubMed  Google Scholar 

  • Freeman TP, Morgan CJ, Brandner B, Almahdi B, Curran HV (2013) Dopaminergic involvement in effort-based but not impulsive reward processing in smokers. Drug Alcohol Depend 130:109–114

    Article  CAS  PubMed  Google Scholar 

  • Freeman TP, Das RK, Kamboj SK, Curran HV (2014) Dopamine, urges to smoke, and the relative salience of drug versus non-drug reward. Social cognitive and affective neuroscience: nsu026

  • Galaj E, Cruz I, Schachar J, Koziolek M, Ranaldi R (2013) Differential effects on natural reward processing in rats after repeated heroin. Psychopharmacol (Berl) 229:125–132

    Article  CAS  Google Scholar 

  • Garavan H, Pankiewicz J, Bloom A, Cho J-K, Sperry L, Ross TJ, Salmeron BJ, Risinger R, Kelley D, Stein EA (2000) Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatr 157:1789–1798

    Article  CAS  PubMed  Google Scholar 

  • Gard DE, Gard MG, Kring AM, John OP (2006) Anticipatory and consummatory components of the experience of pleasure: a scale development study. J Res Pers 40:1086–1102

    Article  Google Scholar 

  • Goldstein RZ, Volkow ND (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatr 159:1642–1652

    Article  PubMed Central  PubMed  Google Scholar 

  • Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652–669

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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. Psychopharmacol (Berl) 175:134–142

    Article  CAS  Google Scholar 

  • Heatherton TF, Kozlowski LT, Frecker RC, FAGERSTROM KO (1991) The Fagerström test for nicotine dependence: a revision of the Fagerstrom tolerance questionnaire. Br J Addict 86:1119–1127

    Article  CAS  PubMed  Google Scholar 

  • Heinz A, Wrase J, Kahnt T, Beck A, Bromand Z, Grüsser SM, Kienast T, Smolka MN, Flor H, Mann K (2007) Brain activation elicited by affectively positive stimuli is associated with a lower risk of relapse in detoxified alcoholic subjects. Alcohol Clin Exp Res 31:1138–1147

    Article  PubMed  Google Scholar 

  • Hogarth L (2012) Goal-directed and transfer-cue-elicited drug-seeking are dissociated by pharmacotherapy: evidence for independent additive controllers. J Exp Psychol Anim Behav Process 38:266

    Article  PubMed  Google Scholar 

  • Hogarth L, Chase HW (2011) Parallel goal-directed and habitual control of human drug-seeking: implications for dependence vulnerability. J Exp Psychol Anim Behav Process 37:261

    Article  PubMed  Google Scholar 

  • Hogarth L, Chase HW (2012) Evaluating psychological markers for human nicotine dependence: tobacco choice, extinction, and Pavlovian-to-instrumental transfer. Exp Clin Psychopharmacol 20:213

    Article  PubMed  Google Scholar 

  • Hughes J, Hatsukami D (2007) Instructions for use of the Minnesota Withdrawal Scale-Revised. Retrieved from www/uvm edu/~ hbpl

  • Jia Z, Worhunsky PD, Carroll KM, Rounsaville BJ, Stevens MC, Pearlson GD, Potenza MN (2011) An initial study of neural responses to monetary incentives as related to treatment outcome in cocaine dependence. Biol Psychiatry 70:553–560

    Article  PubMed Central  PubMed  Google Scholar 

  • Kalamboka N, Remington B, Glautier S (2009) Nicotine withdrawal and reward responsivity in a card-sorting task. Psychopharmacol (Berl) 204:155–163

    Article  CAS  Google Scholar 

  • Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatr 162:1403–1413

    Article  PubMed  Google Scholar 

  • Killen JD, Fortmann SP (1997) Craving is associated with smoking relapse: findings from three prospective studies. Exp Clin Psychopharmacol 5:137

    Article  CAS  PubMed  Google Scholar 

  • Koob GF, le Moal M (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278:52–58

    Article  CAS  PubMed  Google Scholar 

  • Koob GF, le Moal M (2008) Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans Roy Soc B: Biol Sci 363:3113–3123

    Article  Google Scholar 

  • Koob GF, Volkow ND (2009) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed Central  Google Scholar 

  • Levin ED, McClernon FJ, Rezvani AH (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacol (Berl) 184:523–539

    Article  CAS  Google Scholar 

  • Lieblich I, Yirmiya R, Liebeskind JC (1991) Intake of and preference for sweet solutions are attenuated in morphine-withdrawn rats. Behav Neurosci 105:965

    Article  CAS  PubMed  Google Scholar 

  • Lubman DI, Yücel M, Kettle JW, Scaffidi A, MacKenzie T, Simmons JG, Allen NB (2009) Responsiveness to drug cues and natural rewards in opiate addiction: associations with later heroin use. Arch Gen Psychiatry 66:205–212

    Article  PubMed  Google Scholar 

  • MacKillop J, Murphy JG (2007) A behavioral economic measure of demand for alcohol predicts brief intervention outcomes. Drug Alcohol Depend 89:227–233

    Article  PubMed  Google Scholar 

  • MacKillop J, Murphy JG, Ray LA, Eisenberg DT, Lisman SA, Lum JK, Wilson DS (2008) Further validation of a cigarette purchase task for assessing the relative reinforcing efficacy of nicotine in college smokers. Exp Clin Psychopharmacol 16:57

    Article  PubMed  Google Scholar 

  • Martin-Sölch C, Magyar S, Künig G, Missimer J, Schultz W, Leenders K (2001) Changes in brain activation associated with reward processing in smokers and nonsmokers. Exp Brain Res 139:278–286

    Article  PubMed  Google Scholar 

  • Murphy JG, Mackillop J, Tidy JW, Brazil LA, Colby SM (2011) Validity of a demand curve measure of nicotine reinforcement with adolescent smokers. Drug Alcohol Depend 133:207–214

    Article  Google Scholar 

  • Nestor L, Hester R, Garavan H (2010) Increased ventral striatal BOLD activity during non-drug reward anticipation in cannabis users. Neuroimage 49:1133–1143

    Article  PubMed Central  PubMed  Google Scholar 

  • Nocjar C, Panksepp J (2002) Chronic intermittent amphetamine pretreatment enhances future appetitive behavior for drug-and natural-reward: interaction with environmental variables. Behav Brain Res 128:189–203

    Article  CAS  PubMed  Google Scholar 

  • Nocjar C, Panksepp J (2007) Prior morphine experience induces long-term increases in social interest and in appetitive behavior for natural reward. Behav Brain Res 181:191–199

    Article  CAS  PubMed  Google Scholar 

  • Pergadia ML, Der-Avakian A, D’Souza MS, Madden P, Heath AC, Shiffman S, Markou A, Pizzagalli DA (2014) Association between nicotine withdrawal and reward responsiveness in humans and rats. JAMA psychiatry

  • Perkins KA, Karelitz JL (2013) Reinforcement enhancing effects of nicotine via smoking. Psychopharmacol (Berl) 228:479–486

    Article  CAS  Google Scholar 

  • Perkins KA, Epstein LH, Grobe J, Fonte C (1994) Tobacco abstinence, smoking cues, and the reinforcing value of smoking. Pharmacol Biochem Behav 47:107–112

    Article  CAS  PubMed  Google Scholar 

  • Perkins KA, Karelitz JL, Jao NC, Stratton E (2012) Possible reinforcement enhancing effects of bupropion during initial smoking abstinence. Nicotine & Tobacco Research: 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

    Article  PubMed  Google Scholar 

  • Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 18:247–291

    Article  CAS  PubMed  Google Scholar 

  • Robinson TE, Berridge KC (2008) The incentive sensitization theory of addiction: some current issues. Philos Trans Roy Soc B: Biol Sci 363:3137–3146

    Article  Google Scholar 

  • Sescousse G, Redouté J, Dreher J-C (2010) The architecture of reward value coding in the human orbitofrontal cortex. J Neurosci 30:13095–13104

    Article  CAS  PubMed  Google Scholar 

  • Shiffman S, Paty JA, Gnys M, Kassel JD, Elash C (1995) Nicotine withdrawal in chippers and regular smokers: subjective and cognitive effects. Health Psychol 14:301

    Article  CAS  PubMed  Google Scholar 

  • Snaith R, Hamilton M, Morley S, Humayan A, Hargreaves D, Trigwell P (1995) A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. Br J Psychiatry 167:99–103

    Article  CAS  PubMed  Google Scholar 

  • Spring B, Pagoto S, McChargue D, Hedeker D, Werth J (2003) Altered reward value of carbohydrate snacks for female smokers withdrawn from nicotine. Pharmacol Biochem Behav 76:351–360

    Article  CAS  PubMed  Google Scholar 

  • Sweitzer MM, Geier CF, Joel DL, McGurrin P, Denlinger RL, Forbes EE, Donny EC (2013) Dissociated effects of anticipating smoking versus monetary reward in the caudate as a function of smoking abstinence. Biol Psychiatry

  • Treadway MT, Buckholtz JW, Schwartzmann AN, Lambert WE, Zald DH (2009) Worth the ‘EEfRT’? The effort expenditure for rewards task as an objective measure of motivation and anhedonia. PLoS One 4(8)

  • van Hell HH, Vink M, Ossewaarde L, Jager G, Kahn RS, Ramsey NF (2010) Chronic effects of cannabis use on the human reward system: an fMRI study. Eur Neuropsychopharmacol 20:153–163

    Article  PubMed  Google Scholar 

  • Versace F, Lam CY, Engelmann JM, Robinson JD, Minnix JA, Brown VL, Cinciripini PM (2012) Beyond cue reactivity: blunted brain responses to pleasant stimuli predict long-term smoking abstinence. Addict Biol 17:991–1000

    Article  PubMed Central  PubMed  Google Scholar 

  • Vezina P (2004) Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci Biobehav Rev 27:827–839

    Article  CAS  PubMed  Google Scholar 

  • Volkow ND, Wang G-J, Ma Y, Fowler JS, Wong C, Ding Y-S, Hitzemann R, Swanson JM, Kalivas P (2005) Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J Neurosci 25:3932–3939

    Article  CAS  PubMed  Google Scholar 

  • Wrase J, Schlagenhauf F, Kienast T, Wüstenberg T, Bermpohl F, Kahnt T, Beck A, Ströhle A, Juckel G, Knutson B (2007) Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage 35:787–794

    Article  PubMed  Google Scholar 

  • Zhang D, Zhou X, Wang X, Xiang X, Chen H, Hao W (2007) PRECLINICAL STUDY: morphine withdrawal decreases responding reinforced by sucrose self-administration in progressive ratio. Addict Biol 12:152–157

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Nonnemaker J, Sherrill B, Gilsenan AW, Coste F, West R (2009) Attempts to quit smoking and relapse: factors associated with success or failure from the ATTEMPT cohort study. Addict Behav 34:365–373

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by a BBSRC studentship to W Lawn.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Clinical Psychopharmacology Unit, Research Department of Clinical, Educational and Health Psychology, University College London, Gower Street, London, WC1E 6BT, UK

    W. Lawn, T. P. Freeman, C. Hindocha, C. Mokrysz, R. K. Das, C. J. A. Morgan & H. V. Curran

  2. School of Psychology, University of Exeter, Washington Singer Building, Perry Road, Exeter, EX4 4QG, UK

    C. J. A. Morgan

Authors
  1. W. Lawn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. P. Freeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Hindocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Mokrysz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. K. Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. J. A. Morgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. V. Curran
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. Lawn.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

(DOCX 99 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lawn, W., Freeman, T.P., Hindocha, C. et al. The effects of nicotine dependence and acute abstinence on the processing of drug and non-drug rewards. Psychopharmacology 232, 2503–2517 (2015). https://doi.org/10.1007/s00213-015-3883-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-015-3883-4

Keywords

Search

Navigation