Influence of neurobehavioral incentive valence and magnitude on alcohol drinking behavior

The monetary incentive delay (MID) task is a widely used probe for isolating neural circuitry in the human brain associated with incentive motivation. In the present functional magnetic resonance imaging (fMRI) study, 82 young adults, characterized along dimensions of impulsive sensation seeking, completed a MID task. fMRI and behavioral incentive functions were decomposed into incentive valence and magnitude parameters, which were used as predictors in linear regression to determine whether mesolimbic response is associated with problem drinking and recent alcohol use. Alcohol use was best explained by higher fMRI response to anticipation of losses and feedback on high gains in the thalamus. In contrast, problem drinking was best explained by reduced sensitivity to large incentive values in mesolimbic regions in the anticipation phase and increased sensitivity to small incentive values in the dorsal caudate nucleus in the feedback phase. Altered fMRI responses to monetary incentives in mesolimbic circuitry, particularly those alterations associated with problem drinking, may serve as potential early indicators of substance abuse trajectories.

[1]  Donald R. Lynam,et al.  Understanding the role of impulsivity and externalizing psychopathology in alcohol abuse: Application of the UPPS Impulsive Behavior Scale. , 2009 .

[2]  Brian Knutson,et al.  Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics , 2009, Biological Psychiatry.

[3]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[4]  Gang Chen,et al.  Mesolimbic recruitment by nondrug rewards in detoxified alcoholics: Effort anticipation, reward anticipation, and reward delivery , 2012, Human brain mapping.

[5]  T. Kelly,et al.  The reinforcing, subject-rated, performance, and cardiovascular effects of d-amphetamine: influence of sensation-seeking status. , 2007, Addictive behaviors.

[6]  R. Turner,et al.  Detecting Latency Differences in Event-Related BOLD Responses: Application to Words versus Nonwords and Initial versus Repeated Face Presentations , 2002, NeuroImage.

[7]  P. Conrod,et al.  Long-term effects of a personality-targeted intervention to reduce alcohol use in adolescents. , 2011, Journal of consulting and clinical psychology.

[8]  Ashley R. Smith,et al.  Incentive-elicited mesolimbic activation and externalizing symptomatology in adolescents. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[9]  K. Preston,et al.  The reinforcing and subjective effects of morphine in post-addicts: a dose-response study. , 1991, The Journal of pharmacology and experimental therapeutics.

[10]  Melissa A. Cyders,et al.  The role of personality dispositions to risky behavior in predicting first-year college drinking. , 2009, Addiction.

[11]  Brian Knutson,et al.  Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics , 2007, NeuroImage.

[12]  Brian Knutson,et al.  Incentive-Elicited Brain Activation in Adolescents: Similarities and Differences from Young Adults , 2004, The Journal of Neuroscience.

[13]  M. Le Moal,et al.  Addiction and the brain antireward system. , 2008, Annual review of psychology.

[14]  Samantha J. Broyd,et al.  An electrophysiological monetary incentive delay (e-MID) task: A way to decompose the different components of neural response to positive and negative monetary reinforcement , 2012, Journal of Neuroscience Methods.

[15]  Nora D Volkow,et al.  Neurocircuitry of Addiction , 2010, Neuropsychopharmacology.

[16]  Ashley R. Smith,et al.  Striatal sensitivity to reward deliveries and omissions in substance dependent patients , 2008, NeuroImage.

[17]  H. Skinner,et al.  Diagnostic validity of the MAST and the alcohol dependence scale in the assessment of DSM-III alcohol disorders. , 1990, Journal of studies on alcohol.

[18]  D. Metzger,et al.  The Fifth Edition of the Addiction Severity Index. , 1992, Journal of substance abuse treatment.

[19]  C. Colder,et al.  Differentiating between sensation seeking and impulsivity through their mediated relations with alcohol use and problems. , 2007, Addictive behaviors.

[20]  Carrie L. Masten,et al.  Behavioral alterations in reward system function: the role of childhood maltreatment and psychopathology. , 2006, Journal of the American Academy of Child and Adolescent Psychiatry.

[21]  H. Hong,et al.  Personality and alcohol use: the role of impulsivity. , 2012, Addictive behaviors.

[22]  Preeti G. Samudra,et al.  Nucleus Accumbens Response to Incentive Stimuli Anticipation in Children of Alcoholics: Relationships with Precursive Behavioral Risk and Lifetime Alcohol Use , 2012, The Journal of Neuroscience.

[23]  G. Koob Allostatic view of motivation: implications for psychopathology. , 2004, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[24]  Thomas J. H. Chen,et al.  The Reward Deficiency Syndrome: A Biogenetic Model for the Diagnosis and Treatment of Impulsive, Addictive and Compulsive Behaviors , 2000, Journal of psychoactive drugs.

[25]  Gang Chen,et al.  Adolescents, Adults and Rewards: Comparing Motivational Neurocircuitry Recruitment Using fMRI , 2010, PloS one.

[26]  J. Zubieta,et al.  Accumbens functional connectivity during reward mediates sensation-seeking and alcohol use in high-risk youth. , 2013, Drug and alcohol dependence.

[27]  Brian Knutson,et al.  Valence and salience contribute to nucleus accumbens activation , 2008, NeuroImage.

[28]  Arthur MacNeill Horton,et al.  Wechsler Memory Scale III , 1999 .

[29]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[30]  Stefan Kaiser,et al.  Neural reward processing is modulated by approach- and avoidance-related personality traits , 2010, NeuroImage.

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

[32]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[33]  C. Colder,et al.  The UPPS Impulsive Behavior Scale: Factor structure and associations with college drinking , 2007 .

[34]  B. Ostafin,et al.  Testing the incentive-sensitization theory with at-risk drinkers: wanting, liking, and alcohol consumption. , 2010, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[35]  Brian Knutson,et al.  Splitting the Difference , 2007, Annals of the New York Academy of Sciences.

[36]  K. Cropsey,et al.  Sensation seeking and drinking game participation in heavy-drinking college students. , 2000, Addictive behaviors.

[37]  M. Hojat,et al.  Personality and specialty interest in medical students , 2008, Medical teacher.

[38]  A. Cooper,et al.  Impulsivity-related personality traits and adolescent alcohol use: a meta-analytic review. , 2013, Clinical psychology review.

[39]  R. Solomon The opponent-process theory of acquired motivation: the costs of pleasure and the benefits of pain. , 1980, The American psychologist.

[40]  Ashley R. Smith,et al.  Psychosocial problems and recruitment of incentive neurocircuitry: Exploring individual differences in healthy adolescents , 2011, Developmental Cognitive Neuroscience.

[41]  Thomas E. Nichols,et al.  Everything You Never Wanted to Know about Circular Analysis, but Were Afraid to Ask , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[42]  S. Huettel,et al.  Activation in the VTA and Nucleus Accumbens Increases in Anticipation of Both Gains and Losses , 2009, Front. Behav. Neurosci..

[43]  T B Conley,et al.  Construct validity of the MAST and AUDIT with multiple offender drunk drivers. , 2001, Journal of substance abuse treatment.

[44]  Dirk J. Heslenfeld,et al.  Activity in human reward-sensitive brain areas is strongly context dependent , 2005, NeuroImage.

[45]  Brian Knutson,et al.  Incentive-elicited Striatal Activation in Adolescent Children of Alcoholics , 2022 .

[46]  M L Selzer,et al.  A self-administered Short Michigan Alcoholism Screening Test (SMAST). , 1975, Journal of studies on alcohol.

[47]  S. Whiteside,et al.  The Five Factor Model and impulsivity: using a structural model of personality to understand impulsivity , 2001 .

[48]  Marc N. Potenza,et al.  Individuals Family History Positive for Alcoholism Show Functional Magnetic Resonance Imaging Differences in Reward Sensitivity That Are Related to Impulsivity Factors , 2011, Biological Psychiatry.

[49]  R. Ruff,et al.  The Ruff 2 and 7 Selective Attention Test: A Neuropsychological Application , 1992, Perceptual and motor skills.

[50]  M. Zuckerman,et al.  A comparison of three structural models for personality: the big three , 1993 .

[51]  Felix Breuer,et al.  Neural response to reward anticipation is modulated by Gray's impulsivity , 2009, NeuroImage.

[52]  M. Rietschel,et al.  Determinants of Early Alcohol Use In Healthy Adolescents: The Differential Contribution of Neuroimaging and Psychological Factors , 2012, Neuropsychopharmacology.

[53]  G. Pagnoni,et al.  Human Striatal Response to Salient Nonrewarding Stimuli , 2003, The Journal of Neuroscience.

[54]  P. Conrod,et al.  Response inhibition and reward response bias mediate the predictive relationships between impulsivity and sensation seeking and common and unique variance in conduct disorder and substance misuse. , 2011, Alcoholism, clinical and experimental research.

[55]  A. Mack,et al.  Risk Taking and the Adolescent Reward System: A Potential Common Link to Substance Abuse , 2013 .