Hostname: page-component-76d6cb85b7-8p85h Total loading time: 0 Render date: 2026-07-16T02:15:51.339Z Has data issue: false hasContentIssue false
  • English
  • Français

Drug cue induced overshadowing: selective disruption of natural reward processing by cigarette cues amongst abstinent but not satiated smokers

Published online by Cambridge University Press:  07 July 2011

T. P. Freeman ,
C. J. A. Morgan ,
T. Beesley  and
H. V. Curran
T. P. Freeman*
Affiliation:
Clinical Psychopharmacology Unit, Clinical Health Psychology, University College London, London, UK
C. J. A. Morgan
Affiliation:
Clinical Psychopharmacology Unit, Clinical Health Psychology, University College London, London, UK
T. Beesley
Affiliation:
Division of Psychology and Language Sciences, University College London, London, UK
H. V. Curran
Affiliation:
Clinical Psychopharmacology Unit, Clinical Health Psychology, University College London, London, UK
*
*Address for correspondence: T. P. Freeman, B.Sc., Clinical Psychopharmacology Unit, Clinical Health Psychology, University College London, Gower St, London WC1E 6BT, UK. (Email: tom.freeman@ucl.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Addicts show both reward processing deficits and increased salience attribution to drug cues. However, no study to date has demonstrated that salience attribution to drug cues can directly modulate inferences of reward value to non-drug cues. Associative learning depends on salience: a more salient predictor of an outcome will ‘overshadow’ a less salient predictor of the same outcome. Similarly, blocking, a demonstration that learning depends on prediction error, can be influenced by the salience of the cues employed.

Method

This study investigated whether salient drug cues might interact with neutral cues predicting financial reward in an associative learning task indexing blocking and overshadowing in satiated smokers (n=24), abstaining smokers (n=24) and non-smoking controls (n=24). Attentional bias towards drug cues, craving and expired CO were also indexed.

Results

Abstaining smokers showed drug cue induced overshadowing, attributing higher reward value to drug cues than to neutral cues that were equally predictive of reward. Overshadowing was positively correlated with expired CO levels, which, in turn, were correlated with craving in abstainers. An automatic attentional bias towards cigarette cues was found in abstainers only.

Conclusions

These findings provide the first evidence that drug cues interact with reward processing in a drug dependent population.

Keywords

Addictionassociative learningattentionprediction errorrewardtobacco

Information

Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 1 , January 2012 , pp. 161 - 171
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Al-Adawi, S, Powell, J (1997). The influence of smoking on reward responsiveness and cognitive functions: a natural experiment. Addiction 92, 1773–1782.CrossRefGoogle ScholarPubMed
Attwood, AS, O'Sullivan, H, Leonards, U, Mackintosh, B, Munafo, MR (2008). Attentional bias training and cue reactivity in cigarette smokers. Addiction 103, 1875–1882.CrossRefGoogle ScholarPubMed
Beesley, T, Le Pelley, ME (2011). The influence of blocking on overt attention and associability in human learning. Journal of Experimental Psychology: Animal Behaviour Processes 37, 114–120.Google ScholarPubMed
Bradley, B, Field, M, Mogg, K, De Houwer, J (2004). Attentional and evaluative biases for smoking cues in nicotine dependence: component processes of biases in visual orienting. Behavioural Pharmacology 15, 29–36.Google Scholar
Bradley, BP, Mogg, K, Wright, T, Field, M (2003). Attentional bias in drug dependence: vigilance for cigarette-related cues in smokers. Psychology of Addictive Behaviours 17, 66–72.Google Scholar
Cassaday, J, Moran, PM (2010). Latent inhibition and other salience modulation effects: same neural substrates? In: Latent Inhibition: Cognition, Neuroscience, and Applications to Schizophrenia (ed. Lubow, R. E. and Weiner, I.). Cambridge University Press: Cambridge.Google Scholar
Crider, A, Solomon, PR, Mcmahon, MA (1982). Disruption of selective attention in the rat following chronic d-amphetamine administration – relationship to Schizophrenic Attention Disorder. Biological Psychiatry 17, 351–361.Google Scholar
Curran, HV, Drummond, C (2005). State of Science Review: Psychological Treatments for Substance Misuse and Dependence (http://www.foresight.gov.uk).Google Scholar
Dallery, J, Raiff, BR (2007). Delay discounting predicts cigarette smoking in a laboratory model of abstinence reinforcement. Psychopharmacology 190, 485–496.CrossRefGoogle 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. Addictive Behaviours 32, 425–431.CrossRefGoogle ScholarPubMed
Denton, SE, Kruschke, JK (2006). Attention and salience in associative blocking. Learning Behaviour 34, 285–304.Google Scholar
di Chiara, G (2000). Role of dopamine in the behavioural actions of nicotine related to addiction. European Journal of Pharmacology 393, 295–314.CrossRefGoogle ScholarPubMed
Due, DL, Huettel, SA, Hall, WG, Rubin, DC (2002). Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. American Journal of Psychiatry 159, 954–960.CrossRefGoogle ScholarPubMed
Ehrman, RN, Robbins, SJ, Bromwell, MA, Lankford, ME, Monterosso, JR, O'Brien, CP (2002). Comparing attentional bias to smoking cues in current smokers, former smokers, and non-smokers using a dot-probe task. Drug and Alcohol Dependence 67, 185–191.CrossRefGoogle ScholarPubMed
Field, M, Cox, WM (2008). Attentional bias in addictive behaviours: a review of its development, causes, and consequences. Drug and Alcohol Dependence 97, 1–20.CrossRefGoogle ScholarPubMed
Field, M, Mogg, K, Bradley, BP (2004). Eye movements to smoking-related cues: effects of nicotine deprivation. Psychopharmacology 173, 116–123.Google Scholar
Field, M, Munafò, MR, Franken, IHA (2009). A meta-analytic investigation of the relationship between attentional bias and subjective craving in substance abuse. Psychological Bulletin 135, 589–637.CrossRefGoogle ScholarPubMed
Field, M, Santarcangelo, M, Sumnall, H, Goudie, A, Cole, J (2006). Delay discounting and the behavioural economics of cigarette purchases in smokers: the effects of nicotine deprivation. Psychopharmacology 186, 255–263.CrossRefGoogle ScholarPubMed
Goldstein, R, Volkow, N (2002). Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. American Journal of Psychiatry 159, 1642–1652.CrossRefGoogle ScholarPubMed
Granon, S, Passetti, F, Thomas, KL, Dalley, JW, Everitt, BJ, Robbins, TW (2000). Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. Journal of Neuroscience 20, 1208–1215.CrossRefGoogle ScholarPubMed
Gross, TM, Jarvik, ME, Rosenblatt, MR (1993). Nicotine abstinence produces content-specific Stroop interference. Psychopharmacology 110, 333–336.Google Scholar
Hall, G, Mackintosh, NJ, Goodall, G, Dal Martello, M (1977). Loss of control by a less valid or less salient stimulus compounded with a better predictor of reinforcement. Learning and Motivation 8, 145–158.Google Scholar
Heatherton, TF, Kozlowski, LT, Frecker, RC, Fagerstrom, KO (1991). The Fagerstrom Test for nicotine dependence – a revision of the Fagerstrom Tolerance Questionnaire. British Journal of Addiction 86, 1119–1127.Google Scholar
Heckler, AF, Kaminski, JA, Sloutsky, VM (2006). Differential cue salience, blocking, and learned inattention. In Proceedings of the XXVIII Annual Conference of the Cognitive Science Society (ed. Sun, R. and Miyake, N.), pp. 1476–1481. Cognitive Science Society: Austin, TX.Google Scholar
Heishman, SJ, Singleton, EG, Moolchan, ET (2003). Tobacco Craving Questionnaire: reliability and validity of a new multifactorial instrument. Nicotine Tobacco Research 5, 645–654.Google ScholarPubMed
Heishman, SJ, Singleton, EG, Pickworth, WB (2008). Reliability and validity of a short form of the tobacco craving questionnaire. Nicotine Tobacco Research 10, 643–651.CrossRefGoogle Scholar
Hogarth, LC, Mogg, K, Bradley, BP, Duka, T, Dickinson, A (2003). Attentional orienting towards smoking-related stimuli. Behavioural Pharmacology 14, 153–160.Google Scholar
Kalivas, PW, Volkow, N, Seamans, J (2005). Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 45, 647–650.CrossRefGoogle ScholarPubMed
Kamin, LJ (1969). Selective association and conditioning. In Fundamental Issues in Associative Learning (ed. Mackintosh, N. J. and Honig, W. K.), pp. 42–64. Dalhousie University Press: Halifax.Google Scholar
Koob, GF, Le Moal, M (2005). Plasticity of reward neurocircuitry and the ‘dark side’ of drug addiction. Nature Neuroscience 8, 1442–1444.Google Scholar
Kosten, TR, George, TP, Kosten, TA (2002). The potential of dopamine agonists in drug addiction. Expert Opinion on Investigational Drugs 11, 491–499.Google ScholarPubMed
Kruschke, JK, Kappenman, ES, Hetrick, WP (2005). Eye gaze and individual differences consistent with learned attention in associative blocking and highlighting. Journal of Experimental Psychology-Learning Memory and Cognition 31, 830–845.CrossRefGoogle ScholarPubMed
Kwak, SM, Na, DL, Kim, G, Kim, GS, Lee, JH (2007). Use of eye movement to measure smokers' attentional bias to smoking-related cues. Cyberpsychology Behaviour 10, 299–304.CrossRefGoogle ScholarPubMed
Lee, JL, Di Ciano, P, Thomas, KL, Everitt, BJ (2005). Disrupting reconsolidation of drug memories reduces cocaine seeking behaviour. Neuron 47, 795–801.Google Scholar
Mackintosh, NJ (1976). Overshadowing and stimulus-intensity. Animal Learning Behaviour 4, 186–192.CrossRefGoogle ScholarPubMed
Mackintosh, NJ, Reese, B (1979). One-trial overshadowing. Quarterly Journal of Experimental Psychology 31, 519–526.CrossRefGoogle Scholar
Matute, H, Arcediano, F, Miller, RR (1996). Test question modulates cue competition between causes and between effects. Journal of Experimental Psychology: Learning Memory and Cognition 22, 182–196.Google Scholar
Mitchell, SH (2004). Effects of short-term nicotine deprivation on decision making: delay, uncertainty, and effort discounting. Nicotine and Tobacco Research 6, 819–828.Google Scholar
Mogg, K, Bradley, BP (2002). Selective processing of smoking-related cues in smokers: manipulation of deprivation level and comparison of three measures of processing bias. Journal of Psychopharmacology 16, 385–392.Google Scholar
Mogg, K, Bradley, BP, Field, M, de Houwer, J (2003). Eye movements to smoking-related pictures in smokers: relationship between attentional biases and implicit and explicit measures of stimulus valence. Addiction 98, 825–836.CrossRefGoogle ScholarPubMed
Mogg, K, Field, M, Bradley, BP (2005). Attentional and approach biases for smoking cues in smokers: an investigation of competing theoretical views of addiction. Psychopharmacology 180, 333–341.CrossRefGoogle ScholarPubMed
Mogg, K, Garner, M, Bradley, BP (2007). Anxiety and orienting of gaze to angry and fearful faces. Biological Psychology 76, 163–169.CrossRefGoogle ScholarPubMed
O'Brien, CP, Childress, AR, McLellan, T, Ehrman, R (1990). Integrating systematic cue exposure with standard treatment in recovering drug dependent patients. Addictive Behaviours 15, 355–365.Google Scholar
O'Tuathaigh, CMP, Moran, PM (2002). Evidence for dopamine D-1 receptor involvement in the stimulus selection task: overshadowing in the rat. Psychopharmacology 162, 225–231.Google ScholarPubMed
Powell, J, Dawkins, L, Davis, RE (2002 a). Smoking, reward responsiveness, and response inhibition: tests of an incentive motivational model. Biological Psychiatry 51, 151–163.CrossRefGoogle ScholarPubMed
Powell, J, Tait, S, Lessiter, J (2002 b). Cigarette smoking and attention to signals of reward and threat in the Stroop paradigm. Addiction 97, 1163–1170.CrossRefGoogle ScholarPubMed
Ratcliff, R (1993). Methods for dealing with reaction time outliers. Psychological Bulletin 114, 510–532.Google Scholar
Rescorla, RA, Wagner, AR (1972). A theory of Pavlovian conditioning: variations in the effectiveness of reinforcenment and non-reinforcement. In Classical Conditioning II: Current Research and Theory (ed. Black, A. H. and Prokasy, W. F.), pp. 64–99. Appleton-Century-Crofts: New York.Google Scholar
Robinson, TE, Berridge, KC (1993). The neural basis of drug craving – an incentive-sensitization theory of addiction. Brain Research Reviews 18, 247–291.CrossRefGoogle ScholarPubMed
Shiffman, S, Paty, JA, Gnys, M, Kassel, JD, Hickcox, M (1996). First lapses to smoking: within-subjects analysis of real time reports. Journal of Consulting and Clinical Psychology 2, 366–379.Google Scholar
Vink, J, Willemsen, G, Boomsma, D (2005). Heritability of smoking initiation and nicotine dependence. Behaviour Genetics 35, 397–406.Google Scholar
Volkow, ND, Fowler, JS, Wang, G-J, Swanson, JM (2004). Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Molecular Psychiatry 9, 557–569.CrossRefGoogle ScholarPubMed
Wechsler, DA (2001). Wechsler Test of Adult Reading Test. Harcourt: New York.Google Scholar
Wills, AJ, Lavric, A, Croft, GS, Hodgson, TL (2007). Predictive learning, prediction errors, and attention: evidence from event-related potentials and eye tracking. Journal of Cognitive Neuroscience 19, 843–854.Google Scholar