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

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.

[1]  T. George,et al.  The potential of dopamine agonists in drug addiction , 2002, Expert opinion on investigational drugs.

[2]  B. Everitt,et al.  Disrupting Reconsolidation of Drug Memories Reduces Cocaine-Seeking Behavior , 2005, Neuron.

[3]  P. Solomon,et al.  Disruption of selective attention in the rat following chronic d-amphetamine administration: relationship to schizophrenic attention disorder. , 1982, Biological psychiatry.

[4]  P. Moran,et al.  Evidence for dopamine D1 receptor involvement in the stimulus selection task: overshadowing in the rat , 2002, Psychopharmacology.

[5]  N. Mackintosh Overshadowing and stimulus intensity , 1976, Animal learning & behavior.

[6]  J. Kruschke,et al.  Eye gaze and individual differences consistent with learned attention in associative blocking and highlighting. , 2005, Journal of experimental psychology. Learning, memory, and cognition.

[7]  Rita Z. Goldstein,et al.  Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. , 2002, The American journal of psychiatry.

[8]  Jang-Han Lee,et al.  Use of Eye Movement to Measure Smokers' Attentional Bias to Smoking-Related Cues , 2007, Cyberpsychology Behav. Soc. Netw..

[9]  N. Mackintosh,et al.  Loss of control by a less valid or by a less salient stimulus compounded with a better predictor of reinforcement , 1977 .

[10]  K. Mogg,et al.  Attentional and evaluative biases for smoking cues in nicotine dependence: component processes of biases in visual orienting , 2004, Behavioural pharmacology.

[11]  R. E. Lubow,et al.  Latent inhibition : cognition, neuroscience, and applications to schizophrenia , 2010 .

[12]  S. Mitchell,et al.  Effects of short-term nicotine deprivation on decision-making: delay, uncertainty and effort discounting. , 2004, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[13]  S. Shiffman,et al.  First lapses to smoking: within-subjects analysis of real-time reports. , 1996, Journal of consulting and clinical psychology.

[14]  K. Berridge,et al.  The neural basis of drug craving: An incentive-sensitization theory of addiction , 1993, Brain Research Reviews.

[15]  M. Jarvik,et al.  Nicotine abstinence produces content-specific stroop interference , 2005, Psychopharmacology.

[16]  Matt Field,et al.  Eye movements to smoking-related pictures in smokers: relationship between attentional biases and implicit and explicit measures of stimulus valence. , 2003, Addiction.

[17]  Jesse Dallery,et al.  Delay discounting predicts cigarette smoking in a laboratory model of abstinence reinforcement , 2007, Psychopharmacology.

[18]  R. Ehrman,et al.  Integrating systemic cue exposure with standard treatment in recovering drug dependent patients. , 1990, Addictive behaviors.

[19]  H. Cassaday,et al.  Latent Inhibition: Latent inhibition and other salience modulation effects: same neural substrates? , 2010 .

[20]  G. Chiara Role of dopamine in the behavioural actions of nicotine related to addiction. , 2000 .

[21]  R. R. Miller,et al.  Test question modulates cue competition between causes and between effects. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[22]  Ute Leonards,et al.  Attentional bias training and cue reactivity in cigarette smokers. , 2008, Addiction.

[23]  G. Koob,et al.  Plasticity of reward neurocircuitry and the 'dark side' of drug addiction , 2005, Nature Neuroscience.

[24]  Matt Field,et al.  A meta-analytic investigation of the relationship between attentional bias and subjective craving in substance abuse. , 2009, Psychological bulletin.

[25]  Jennifer A. Kaminski,et al.  Differential Cue Salience, Blocking and Learned Inattention , 2006 .

[26]  Matt Field,et al.  Attentional bias in drug dependence: vigilance for cigarette-related cues in smokers. , 2003, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[27]  J. Powell,et al.  Smoking, reward responsiveness, and response inhibition: tests of an incentive motivational model , 2002, Biological Psychiatry.

[28]  Roger Ratcliff,et al.  Methods for Dealing With Reaction Time Outliers , 1992 .

[29]  D. Rubin,et al.  Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. , 2002, The American journal of psychiatry.

[30]  Stephen E. Denton,et al.  Attention and salience in associative blocking , 2006, Learning & behavior.

[31]  J. Lessiter,et al.  Cigarette smoking and attention to signals of reward and threat in the Stroop paradigm. , 2002, Addiction.

[32]  M. Field,et al.  Attentional bias in addictive behaviors: a review of its development, causes, and consequences. , 2008, Drug and alcohol dependence.

[33]  J. Powell,et al.  The influence of smoking on reward responsiveness and cognitive functions: a natural experiment. , 1997, Addiction.

[34]  N. Mackintosh,et al.  One-Trial Overshadowing , 1979 .

[35]  Lee Hogarth,et al.  Attentional orienting towards smoking-related stimuli , 2003, Behavioural pharmacology.

[36]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[37]  Karin Mogg,et al.  Selective processing of smoking-related cues in smokers: manipulation of deprivation level and comparison of three measures of processing bias , 2002, Journal of psychopharmacology.

[38]  Gonneke Willemsen,et al.  Heritability of Smoking Initiation and Nicotine Dependence , 2005, Behavior genetics.

[39]  S. Heishman,et al.  Tobacco Craving Questionnaire: reliability and validity of a new multifactorial instrument. , 2003, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[40]  K. Mogg,et al.  Attentional and approach biases for smoking cues in smokers: an investigation of competing theoretical views of addiction , 2005, Psychopharmacology.

[41]  J. Monterosso,et al.  Comparing attentional bias to smoking cues in current smokers, former smokers, and non-smokers using a dot-probe task. , 2002, Drug and alcohol dependence.

[42]  R. Rescorla A theory of pavlovian conditioning: The effectiveness of reinforcement and non-reinforcement , 1972 .

[43]  J. Swanson,et al.  Dopamine in drug abuse and addiction: results from imaging studies and treatment implications , 2004, Molecular Psychiatry.

[44]  L. Kozlowski,et al.  The Fagerström Test for Nicotine Dependence: a revision of the Fagerström Tolerance Questionnaire. , 1991, British journal of addiction.

[45]  Matthew Garner,et al.  Anxiety and orienting of gaze to angry and fearful faces , 2007, Biological Psychology.

[46]  Matt Field,et al.  Eye movements to smoking-related cues: effects of nicotine deprivation , 2004, Psychopharmacology.

[47]  Andrew Goudie,et al.  Delay discounting and the behavioural economics of cigarette purchases in smokers: the effects of nicotine deprivation , 2006, Psychopharmacology.

[48]  Andy J. Wills,et al.  Predictive Learning, Prediction Errors, and Attention: Evidence from Event-related Potentials and Eye Tracking , 2007, Journal of Cognitive Neuroscience.

[49]  S. Heishman,et al.  Reliability and validity of a Short Form of the Tobacco Craving Questionnaire. , 2008, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[50]  Trevor W. Robbins,et al.  Enhanced and Impaired Attentional Performance After Infusion of D1 Dopaminergic Receptor Agents into Rat Prefrontal Cortex , 2000, The Journal of Neuroscience.

[51]  S. Acaster,et al.  The effects of smoking and abstinence on experience of happiness and sadness in response to positively valenced, negatively valenced, and neutral film clips. , 2007, Addictive behaviors.

[52]  N. Volkow,et al.  Unmanageable Motivation in Addiction: A Pathology in Prefrontal-Accumbens Glutamate Transmission , 2005, Neuron.

[53]  Hv Curran,et al.  State of Science Review: Psychological Treatments for substance misuse and dependence , 2005 .

[54]  M. L. Le Pelley,et al.  The influence of blocking on overt attention and associability in human learning. , 2011, Journal of experimental psychology. Animal behavior processes.