Risk prediction and aversion by anterior cingulate cortex

The recently proposed error-likelihood hypothesis suggests that anterior cingulate cortex (ACC) and surrounding areas will become active in proportion to the perceived likelihood of an error. The hypothesis was originally derived from a computational model prediction. The same computational model now makes a further prediction that ACC will be sensitive not only to predicted error likelihood, but also to the predicted magnitude of the consequences, should an error occur. The product of error likelihood and predicted error consequence magnitude collectively defines the general “expected risk” of a given behavior in a manner analogous but orthogonal to subjective expected utility theory. New fMRI results from an incentive change signal task now replicate the errorlikelihood effect, validate the further predictions of the computational model, and suggest why some segments of the population may fail to show an error-likelihood effect. In particular, error-likelihood effects and expected risk effects in general indicate greater sensitivity to earlier predictors of errors and are seen in risk-averse but not risktolerant individuals. Taken together, the results are consistent with an expected risk model of ACC and suggest that ACC may generally contribute to cognitive control by recruiting brain activity to avoid risk.

[1]  E. Rowland Theory of Games and Economic Behavior , 1946, Nature.

[2]  D. Bernoulli Exposition of a New Theory on the Measurement of Risk , 1954 .

[3]  G. Schwartz,et al.  Consciousness and Self-Regulation , 1976 .

[4]  A. Tversky,et al.  Prospect theory: analysis of decision under risk , 1979 .

[5]  D. Norman,et al.  Attention to action: Willed and automatic control , 1980 .

[6]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[7]  A. Tversky,et al.  The framing of decisions and the psychology of choice. , 1981, Science.

[8]  G. Logan,et al.  On the ability to inhibit simple and choice reaction time responses: a model and a method. , 1984, Journal of experimental psychology. Human perception and performance.

[9]  V. B. Brooks,et al.  ‘Error’ potentials in limbic cortex (anterior cingulate area 24) of monkeys during motor learning , 1986, Neuroscience Letters.

[10]  H. Lesieur,et al.  The South Oaks Gambling Screen (SaGS): A New Instrument for the Identification of Pathological Gamblers , 2010 .

[11]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[12]  Derek W. Johnston,et al.  The relationship between cardiovascular responses in the laboratory and in the field. , 1990, Psychophysiology.

[13]  W. Schultz,et al.  Responses of monkey dopamine neurons during learning of behavioral reactions. , 1992, Journal of neurophysiology.

[14]  Karl J. Friston,et al.  Patterns of Cerebral Blood Flow in Schizophrenia , 1992, British Journal of Psychiatry.

[15]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[16]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[17]  J. Mazziotta,et al.  Automated image registration , 1993 .

[18]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[19]  M. Zuckerman Behavioral Expressions and Biosocial Bases of Sensation Seeking , 1994 .

[20]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[21]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[22]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[23]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[24]  C. Frith,et al.  How do we predict the consequences of our actions? a functional imaging study , 1998, Neuropsychologia.

[25]  A M Dale,et al.  Randomized event‐related experimental designs allow for extremely rapid presentation rates using functional MRI , 1998, Neuroreport.

[26]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[27]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[28]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[29]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[30]  J. Schall,et al.  Performance monitoring by the supplementary eye ® eld , 2000 .

[31]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  David P. Farrington,et al.  Some benefits of dichotomization in psychiatric and criminological research , 2000 .

[33]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[34]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[35]  M. Coles,et al.  Performance monitoring in a confusing world: error-related brain activity, judgments of response accuracy, and types of errors. , 2000, Journal of experimental psychology. Human perception and performance.

[36]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[37]  C. Carter,et al.  Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study. , 2001, The American journal of psychiatry.

[38]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

[39]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

[40]  C. Carter,et al.  Anterior Cingulate Metabolism Correlates with Stroop Errors in Paranoid Schizophrenia Patients , 2001, Neuropsychopharmacology.

[41]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[42]  Jonathan D. Cohen,et al.  Anterior Cingulate Cortex, Conflict Monitoring, and Levels of Processing , 2001, NeuroImage.

[43]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. , 2001, Cerebral cortex.

[44]  Carl R. Olson,et al.  Neuronal activity related to rule and conflict in macaque supplementary eye field , 2002, Physiology & Behavior.

[45]  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.

[46]  Jeremy R. Gray,et al.  Personality predicts working-memory—related activation in the caudal anterior cingulate cortex , 2002, Cognitive, affective & behavioral neuroscience.

[47]  M. Walton,et al.  The Role of Rat Medial Frontal Cortex in Effort-Based Decision Making , 2002, The Journal of Neuroscience.

[48]  Gregory G. Brown,et al.  Error Rate and Outcome Predictability Affect Neural Activation in Prefrontal Cortex and Anterior Cingulate during Decision-Making , 2002, NeuroImage.

[49]  E. Weber,et al.  A Domain-Specific Risk-Attitude Scale: Measuring Risk Perceptions and Risk Behaviors , 2002 .

[50]  Kristopher J Preacher,et al.  On the practice of dichotomization of quantitative variables. , 2002, Psychological methods.

[51]  B. Richmond,et al.  Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy , 2002, Science.

[52]  Jonathan D. Cohen,et al.  A computational model of anterior cingulate function in speeded response tasks: Effects of frequency, sequence, and conflict , 2002, Cognitive, affective & behavioral neuroscience.

[53]  Will M Aklin,et al.  Evaluation of the Balloon Analogue Risk Task (BART) as a predictor of adolescent real-world risk-taking behaviours. , 2003, Journal of adolescence.

[54]  Geraint Rees,et al.  Self-control during response conflict by human supplementary eye field , 2003, Nature Neuroscience.

[55]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[56]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[57]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[58]  Howard L Fields,et al.  Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal , 2004, Nature Neuroscience.

[59]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[60]  Michael J. Frank,et al.  Error-Related Negativity Predicts Reinforcement Learning and Conflict Biases , 2005, Neuron.

[61]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[62]  C. Lejuez,et al.  Construct Validity of the Balloon Analog Risk Task (BART) , 2005, Assessment.

[63]  Camelia M. Kuhnen,et al.  The Neural Basis of Financial Risk Taking , 2005, Neuron.

[64]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[65]  E. Procyk,et al.  Anterior cingulate error‐related activity is modulated by predicted reward , 2005, The European journal of neuroscience.

[66]  P. Glimcher,et al.  Midbrain Dopamine Neurons Encode a Quantitative Reward Prediction Error Signal , 2005, Neuron.

[67]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[68]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[69]  J. O'Doherty,et al.  Is Avoiding an Aversive Outcome Rewarding? Neural Substrates of Avoidance Learning in the Human Brain , 2006, PLoS biology.

[70]  John J. Foxe,et al.  The Anterior Cingulate and Error Avoidance , 2006, The Journal of Neuroscience.

[71]  D. Kumaran,et al.  Frames, Biases, and Rational Decision-Making in the Human Brain , 2006, Science.

[72]  Lawrence R. Frank,et al.  Anterior cingulate activity modulates nonlinear decision weight function of uncertain prospects , 2006, NeuroImage.

[73]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

[74]  E. Procyk,et al.  Reward encoding in the monkey anterior cingulate cortex. , 2006, Cerebral cortex.

[75]  A. Tversky,et al.  Prospect theory: an analysis of decision under risk — Source link , 2007 .

[76]  M. Botvinick,et al.  Error-likelihood prediction in the medial frontal cortex: a critical evaluation. , 2007, Cerebral cortex.

[77]  Johannes Hewig,et al.  Decision-making in Blackjack: an electrophysiological analysis. , 2007, Cerebral cortex.

[78]  Joshua W. Brown,et al.  A computational model of risk, conflict, and individual difference effects in the anterior cingulate cortex , 2008, Brain Research.