Neural mechanisms of risk taking and relationships with hazardous drinking.

BACKGROUND Impulsivity, particularly risk taking, is believed to play a significant role in alcohol use disorders (AUDs). While risk taking has been measured using questionnaires, recent performance-based tasks such as the Balloon Analog Risk Task (BART) have shown considerable promise in understanding risky decision-making processes in drinkers. While the number of studies using the BART has grown significantly over the past decade, the neural mechanisms that underlie risky choices on the BART have only begun to be explored. The current study was designed to assess both the neural mechanisms of risk taking on the BART and to explore relationships between risk taking and hazardous drinking. METHODS Seventy-nine individuals with an AUD completed an fMRI compatible version of the BART that required pumping simulated air into risky or nonrisky balloons to earn points on each trial, and deciding when to terminate pumping to earn points accumulated. Hazardous drinking was assessed with the Alcohol Use Disorder Identification Test (AUDIT). RESULTS Comparison of risky and nonrisky decisions revealed differences in the dorsal anterior cingulate cortex (dACC), anterior insula, and striatum. Comparison of Cashout responses and Explosions revealed increased responses in lateral prefrontal cortex, insula, ACC, and middle temporal gyrus during Explosions and greater response in inferior parietal lobe and caudate during Cashouts. When examining relationships between hazardous drinking and neural measures of risk taking, we found significant negative relationships with insula, striatum, and dACC. CONCLUSIONS The current results suggest that risk taking is associated with increased response in the dACC and anterior insula, regions previously implicated in representing error likelihood and negative outcome magnitudes, respectively. In addition, hazardous drinking was associated with responses in the dACC, possibly suggesting a reduced ability to predict the likelihood of errors and to predict negative outcomes associated with risk taking.

[1]  Marie T. Banich,et al.  Risky Decisions and Their Consequences: Neural Processing by Boys with Antisocial Substance Disorder , 2010, PloS one.

[2]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

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

[4]  John A. Detre,et al.  Neural correlates of voluntary and involuntary risk taking in the human brain: An fMRI Study of the Balloon Analog Risk Task (BART) , 2008, NeuroImage.

[5]  J. Steinmetz,et al.  Early-onset alcoholism with conduct disorder: go/no go learning deficits, working memory capacity, and personality. , 2002, Alcoholism, clinical and experimental research.

[6]  K. Kiehl,et al.  Neural and behavioral mechanisms of impulsive choice in alcohol use disorder. , 2011, Alcoholism, clinical and experimental research.

[7]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[8]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[9]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Woojae Kim,et al.  Cognitive Mechanisms Underlying Risky Decision-Making in Chronic Cannabis Users. , 2010, Journal of mathematical psychology.

[11]  W. Schultz.  Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

[12]  Martin P. Paulus,et al.  Anterior insular cortex anticipates impending stimulus significance , 2009, NeuroImage.

[13]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[14]  N. Petry,et al.  Delay discounting of money and alcohol in actively using alcoholics, currently abstinent alcoholics, and controls , 2001, Psychopharmacology.

[15]  Joshua W. Brown,et al.  Risk prediction and aversion by anterior cingulate cortex , 2007, Cognitive, affective & behavioral neuroscience.

[16]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[17]  Ashley R. Smith,et al.  Developmental Differences in Posterior Mesofrontal Cortex Recruitment by Risky Rewards , 2007, The Journal of Neuroscience.

[18]  Will M Aklin,et al.  The Balloon Analogue Risk Task (BART) differentiates smokers and nonsmokers. , 2003, Experimental and clinical psychopharmacology.

[19]  Gregory L. Stuart,et al.  Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). , 2002, Journal of experimental psychology. Applied.

[20]  G. McCarthy,et al.  Decisions under Uncertainty: Probabilistic Context Influences Activation of Prefrontal and Parietal Cortices , 2005, The Journal of Neuroscience.

[21]  C. X. Poulos,et al.  Impulsivity predicts individual susceptibility to high levels of alcohol self‐administration , 1995, Behavioural pharmacology.

[22]  M. Frank,et al.  Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. , 2006, Psychological review.

[23]  M. Delgado,et al.  Reward‐Related Responses in the Human Striatum , 2007, Annals of the New York Academy of Sciences.

[24]  Stephan F. Taylor,et al.  Decision-related loss: Regret and disappointment , 2009, NeuroImage.

[25]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[26]  P. Donovick,et al.  Multidimensional assessment of impulsivity in undergraduate hazardous drinkers and controls. , 2007, Journal of studies on alcohol and drugs.

[27]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[28]  T. Robbins,et al.  Differences in orbitofrontal activation during decision-making between methadone-maintained opiate users, heroin users and healthy volunteers , 2006, Psychopharmacology.

[29]  B. Gold,et al.  Functional Dissociation in Frontal and Striatal Areas for Processing of Positive and Negative Reward Information , 2007, The Journal of Neuroscience.

[30]  N. Heather,et al.  Development of a scale for measuring impaired control over alcohol consumption: a preliminary report. , 1993, Journal of studies on alcohol.

[31]  Ashley R. Smith,et al.  Reduced posterior mesofrontal cortex activation by risky rewards in substance-dependent patients. , 2008, Drug and alcohol dependence.

[32]  Maristela Monteiro,et al.  AUDIT - The alcohol use disorders identification test: guidelines for use in primary care. , 2001 .

[33]  N. Heather,et al.  Impaired Control Scale: cross-validation and relationships with treatment outcome. , 1998, Addiction.

[34]  Corianne Rogalsky,et al.  Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism , 2003, NeuroImage.

[35]  E. Claus,et al.  Identifying Neurobiological Phenotypes Associated with Alcohol Use Disorder Severity , 2011, Neuropsychopharmacology.

[36]  Linda C. Sobell,et al.  Timeline Follow-Back A Technique for Assessing Self-Reported Alcohol Consumption , 1992 .

[37]  Richard B. Ivry,et al.  The influence of feedback valence in associative learning , 2009, NeuroImage.

[38]  C. Lejuez,et al.  Differences in risk-taking propensity across inner-city adolescent ever- and never-smokers. , 2005, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[39]  Gang Chen,et al.  Functional imaging analysis contest (FIAC) analysis according to AFNI and SUMA , 2006, Human brain mapping.

[40]  W. Gehring,et al.  Medial Frontal Cortex Activity and Loss-Related Responses to Errors , 2006, The Journal of Neuroscience.

[41]  Matt Field,et al.  Risk-taking but not response inhibition or delay discounting predict alcohol consumption in social drinkers. , 2010, Drug and alcohol dependence.

[42]  JaneR . Taylor,et al.  Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli , 1999, Psychopharmacology.

[43]  Bruno Rossion,et al.  Category Specificity in Early Perception: Face and Word N170 Responses Differ in Both Lateralization and Habituation Properties , 2008, Frontiers in human neuroscience.

[44]  A. Rodríguez-Fornells,et al.  Functional Connectivity of Reward Processing in the Brain , 2008, Front. Hum. Neurosci..

[45]  S. Quartz,et al.  Human Insula Activation Reflects Risk Prediction Errors As Well As Risk , 2008, The Journal of Neuroscience.

[46]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.