Pavlovian-to-Instrumental Transfer in Alcohol Dependence: A Pilot Study

Background: Pavlovian processes are thought to play an important role in the development, maintenance and relapse of alcohol dependence, possibly by influencing and usurping ongoing thought and behavior. The influence of pavlovian stimuli on ongoing behavior is paradigmatically measured by pavlovian-to-instrumental transfer (PIT) tasks. These involve multiple stages and are complex. Whether increased PIT is involved in human alcohol dependence is uncertain. We therefore aimed to establish and validate a modified PIT paradigm that would be robust, consistent and tolerated by healthy controls as well as by patients suffering from alcohol dependence, and to explore whether alcohol dependence is associated with enhanced PIT. Methods: Thirty-two recently detoxified alcohol-dependent patients and 32 age- and gender-matched healthy controls performed a PIT task with instrumental go/no-go approach behaviors. The task involved both pavlovian stimuli associated with monetary rewards and losses, and images of drinks. Results: Both patients and healthy controls showed a robust and temporally stable PIT effect. Strengths of PIT effects to drug-related and monetary conditioned stimuli were highly correlated. Patients more frequently showed a PIT effect, and the effect was stronger in response to aversively conditioned CSs (conditioned suppression), but there was no group difference in response to appetitive CSs. Conclusion: The implementation of PIT has favorably robust properties in chronic alcohol-dependent patients and in healthy controls. It shows internal consistency between monetary and drug-related cues. The findings support an association of alcohol dependence with an increased propensity towards PIT. 2014 S. Karger AG, Basel

[1]  L. Robins,et al.  How permanent was Vietnam drug addiction? , 1974, American journal of public health.

[2]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[3]  C. Naranjo,et al.  Assessment of alcohol withdrawal: the revised clinical institute withdrawal assessment for alcohol scale (CIWA-Ar). , 1989, British journal of addiction.

[4]  E. Peli Contrast in complex images. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[5]  H. Wittchen Computer scoring of CIDI diagnoses , 1993 .

[6]  B. Jones,et al.  Negative alcohol expectancy predicts post-treatment abstinence survivorship: the whether, when and why of relapse to a first drink. , 1994, Addiction.

[7]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  P. Pini Addiction , 1996, The Lancet.

[9]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[10]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[11]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[12]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[13]  B. Carter,et al.  Is craving the source of compulsive drug use? , 1998, Journal of psychopharmacology.

[14]  G. Di Chiara Drug addiction as dopamine-dependent associative learning disorder. , 1999, European journal of pharmacology.

[15]  T. Robbins,et al.  Drug addiction: bad habits add up , 1999, Nature.

[16]  G. Chiara Drug addiction as dopamine-dependent associative learning disorder , 1999 .

[17]  J. Mirenowicz,et al.  Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. , 2000, Behavioral neuroscience.

[18]  J. Mirenowicz,et al.  Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. , 2000, Behavioral neuroscience.

[19]  B T Jones,et al.  A review of expectancy theory and alcohol consumption. , 2001, Addiction.

[20]  D. Shanks,et al.  The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications. , 2002, Journal of experimental psychology. Animal behavior processes.

[21]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[22]  Paul L Doering,et al.  Acamprosate for the treatment of alcohol dependence. , 2005, Clinical therapeutics.

[23]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[24]  P. Dayan,et al.  Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control , 2005, Nature Neuroscience.

[25]  B. Balleine,et al.  Double Dissociation of Basolateral and Central Amygdala Lesions on the General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer , 2005, The Journal of Neuroscience.

[26]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[27]  R. Room,et al.  Alcohol use disorders in EU countries and Norway: An overview of the epidemiology , 2005, European Neuropsychopharmacology.

[28]  R. Spanagel,et al.  [One drink, one drunk--controlled drinking by alcoholics? 3-year-outcome after intensive outpatient treatment]. , 2007, Psychotherapie, Psychosomatik, medizinische Psychologie.

[29]  Elizabeth L. Ogburn,et al.  Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions. , 2007, Archives of general psychiatry.

[30]  P. Janak,et al.  Ethanol-associated cues produce general pavlovian-instrumental transfer. , 2007, Alcoholism: Clinical and Experimental Research.

[31]  K. Berridge,et al.  The incentive sensitization theory of addiction: some current issues , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  B. Balleine,et al.  The Neural Mechanisms Underlying the Influence of Pavlovian Cues on Human Decision Making , 2008, The Journal of Neuroscience.

[33]  Wolfgang Hauber,et al.  Dopamine D1 and D2 receptors in the nucleus accumbens core and shell mediate Pavlovian-instrumental transfer. , 2008, Learning & memory.

[34]  P. Dayan,et al.  Human Pavlovian–Instrumental Transfer , 2008, The Journal of Neuroscience.

[35]  Adam Johnson,et al.  Computing motivation: Incentive salience boosts of drug or appetite states , 2008, Behavioral and Brain Sciences.

[36]  N. Volkow,et al.  Imaging dopamine's role in drug abuse and addiction , 2009, Neuropharmacology.

[37]  Huda Akil,et al.  Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction , 2009, Neuropharmacology.

[38]  M. Roesch,et al.  A new perspective on the role of the orbitofrontal cortex in adaptive behaviour , 2009, Nature Reviews Neuroscience.

[39]  X. Zhuang,et al.  Faculty Opinions recommendation of A selective role for dopamine in stimulus-reward learning. , 2010 .

[40]  E. Coutureau,et al.  Pavlovian to instrumental transfer: A neurobehavioural perspective , 2010, Neuroscience & Biobehavioral Reviews.

[41]  T. Robinson,et al.  An Animal Model of Genetic Vulnerability to Behavioral Disinhibition and Responsiveness to Reward-Related Cues: Implications for Addiction , 2010, Neuropsychopharmacology.

[42]  Raymond J. Dolan,et al.  Disentangling the Roles of Approach, Activation and Valence in Instrumental and Pavlovian Responding , 2011, PLoS Comput. Biol..

[43]  B. Balleine,et al.  Differential dependence of Pavlovian incentive motivation and instrumental incentive learning processes on dopamine signaling. , 2011, Learning & memory.

[44]  M. Delgado,et al.  Pavlovian to instrumental transfer of control in a human learning task. , 2011, Emotion.

[45]  Rajita Sinha,et al.  Sex differences in neural responses to stress and alcohol context cues , 2011, Human brain mapping.

[46]  A. Meyer-Lindenberg,et al.  Cognitive and neurobiological mechanisms of alcohol-related aggression , 2011, Nature Reviews Neuroscience.

[47]  Alice M Stamatakis,et al.  Neural correlates of Pavlovian‐to‐instrumental transfer in the nucleus accumbens shell are selectively potentiated following cocaine self‐administration , 2011, European Journal of Neuroscience.

[48]  L. Hogarth,et al.  Prediction and uncertainty in human Pavlovian to instrumental transfer. , 2011, Journal of experimental psychology. Learning, memory, and cognition.

[49]  Robert C. Wilson,et al.  Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex , 2011, Nature Neuroscience.

[50]  Y. Niv,et al.  Ventral Striatum and Orbitofrontal Cortex Are Both Required for Model-Based, But Not Model-Free, Reinforcement Learning , 2011, The Journal of Neuroscience.

[51]  S. Ostlund,et al.  Pavlovian-to-instrumental transfer in cocaine seeking rats. , 2012, Behavioral neuroscience.

[52]  Mimi Liljeholm,et al.  Neural Correlates of Specific and General Pavlovian-to-Instrumental Transfer within Human Amygdalar Subregions: A High-Resolution fMRI Study , 2012, The Journal of Neuroscience.

[53]  T. Robbins,et al.  Neurocognitive endophenotypes of impulsivity and compulsivity: towards dimensional psychiatry , 2012, Trends in Cognitive Sciences.

[54]  Y. Niv,et al.  The impact of orbitofrontal dysfunction on cocaine addiction , 2012, Nature Neuroscience.

[55]  Roshan Cools,et al.  Serotonin and Aversive Pavlovian Control of Instrumental Behavior in Humans , 2013, The Journal of Neuroscience.

[56]  B. Balleine,et al.  Associative learning mechanisms underpinning the transition from recreational drug use to addiction , 2013, Annals of the New York Academy of Sciences.

[57]  Michael W. Shiflett,et al.  The effects of amphetamine sensitization on conditioned inhibition during a Pavlovian–instrumental transfer task in rats , 2013, Psychopharmacology.

[58]  L. Hogarth,et al.  Phasic transition from goal‐directed to habitual control over drug‐seeking produced by conflicting reinforcer expectancy , 2013, Addiction biology.

[59]  S. Ostlund,et al.  Repeated Cocaine Exposure Facilitates the Expression of Incentive Motivation and Induces Habitual Control in Rats , 2013, PloS one.

[60]  G. Baldassarre,et al.  The three principles of action: a Pavlovian-instrumental transfer hypothesis , 2013, Front. Behav. Neurosci..

[61]  F. Kiefer,et al.  New approaches to addiction treatment based on learning and memory. , 2013, Current topics in behavioral neurosciences.

[62]  P. Dayan,et al.  Goals and Habits in the Brain , 2013, Neuron.

[63]  Josiah R. Boivin,et al.  A Causal Link Between Prediction Errors, Dopamine Neurons and Learning , 2013, Nature Neuroscience.

[64]  Mehdi Khamassi,et al.  Modelling Individual Differences in the Form of Pavlovian Conditioned Approach Responses: A Dual Learning Systems Approach with Factored Representations , 2014, PLoS Comput. Biol..

[65]  P. Tobler,et al.  The role of learning-related dopamine signals in addiction vulnerability. , 2014, Progress in brain research.