Neural correlates of feedback processing in decision-making under risk

Introduction: Event-related brain potentials (ERPs) provide important information about the sensitivity of the brain to process varying risks. The aim of the present study was to determine how different risk levels are reflected in decision-related ERPs, namely the feedback-related negativity (FRN) and the P300. Materials and Methods: Twenty participants conducted a probabilistic two-choice gambling task while an electroencephalogram (EEG) was recorded. Choices were provided between a low-risk option yielding low rewards and low losses and a high-risk option yielding high rewards and high losses. While options differed in expected risks, they were equal in expected values and in feedback probabilities. Results: At the behavioral level, participants were generally risk-averse but modulated their risk-taking behavior according to reward history. An early positivity (P200) was enhanced on negative feedbacks in high-risk compared to low-risk choices. With regard to the FRN, there were significant amplitude differences between positive and negative feedbacks on high-risk choices, but not on low-risk choices. While the FRN on negative feedbacks did not vary with decision riskiness, reduced amplitudes were found for positive feedbacks in high-risk relative to low-risk choices. P300 amplitudes were larger in high-risk decisions, and in an additive way, after negative compared to positive feedback. Discussion: The present study revealed significant influences of risk and valence processing on ERPs. FRN findings suggest that the reward prediction error signal is increased after high-risk decisions. The increased P200 on negative feedback in risky decisions suggests that large negative prediction errors are already processed in the P200 time range. The later P300 amplitude is sensitive to feedback valence as well as to the risk associated with a decision. Thus, the P300 carries additional information for reward processing, mainly the enhanced motivational significance of risky decisions.

[1]  Isidore Nabi It wasn't me , 1981, Nature.

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

[3]  M. Machina "Expected Utility" Analysis without the Independence Axiom , 1982 .

[4]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[5]  D. Tucker,et al.  Medial Frontal Cortex in Action Monitoring , 2000, The Journal of Neuroscience.

[6]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[7]  L Carretié,et al.  Emotion, attention, and the 'negativity bias', studied through event-related potentials. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[9]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[10]  B. Vogt,et al.  Structural and functional dichotomy of human midcingulate cortex , 2003, The European journal of neuroscience.

[11]  Clay B. Holroyd,et al.  Errors in reward prediction are re£ected in the event-related brain potential , 2003 .

[12]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[13]  Jeff T. Larsen,et al.  Context dependence of the event-related brain potential associated with reward and punishment. , 2004, Psychophysiology.

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

[15]  Christopher S. Monk,et al.  Choice selection and reward anticipation: an fMRI study , 2004, Neuropsychologia.

[16]  Rogier B. Mars,et al.  De Bruijn ERA, Mars RB, & Hulstijn W It wasn't me... or was it? How false feedback affects performance , 2004 .

[17]  A. Sanfey,et al.  Independent Coding of Reward Magnitude and Valence in the Human Brain , 2004, The Journal of Neuroscience.

[18]  M. Platt,et al.  Expectations and outcomes: decision-making in the primate brain , 2005, Journal of Comparative Physiology A.

[19]  A. Engel,et al.  Trial-by-Trial Coupling of Concurrent Electroencephalogram and Functional Magnetic Resonance Imaging Identifies the Dynamics of Performance Monitoring , 2005, The Journal of Neuroscience.

[20]  Clay B. Holroyd,et al.  Brain potentials associated with expected and unexpected good and bad outcomes. , 2005, Psychophysiology.

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

[22]  H. Murohashi,et al.  Discrepancy between feedback negativity and subjective evaluation in gambling , 2005, Neuroreport.

[23]  Takashi Hanakawa,et al.  Functional activity related to risk anticipation during performance of the Iowa gambling task , 2005, NeuroImage.

[24]  Atsushi Sato,et al.  Effects of value and reward magnitude on feedback negativity and P300 , 2005, Neuroreport.

[25]  Luis Carretié,et al.  Cortical response to subjectively unconscious danger , 2005, NeuroImage.

[26]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

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

[28]  Clay B. Holroyd,et al.  The feedback-related negativity reflects the binary evaluation of good versus bad outcomes , 2006, Biological Psychology.

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

[30]  Matthias Brand,et al.  Neuropsychological correlates of decision-making in ambiguous and risky situations , 2006, Neural Networks.

[31]  H. Walter,et al.  Electrophysiological correlates of error processing in borderline personality disorder , 2006, Biological Psychology.

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

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

[34]  Michael X. Cohen,et al.  Reward expectation modulates feedback-related negativity and EEG spectra , 2007, NeuroImage.

[35]  Clay B. Holroyd,et al.  It's worse than you thought: the feedback negativity and violations of reward prediction in gambling tasks. , 2007, Psychophysiology.

[36]  Giuseppe Sartori,et al.  Predicting outcomes of decisions in the brain , 2008, Behavioural Brain Research.

[37]  B. Eppinger,et al.  Better or worse than expected? Aging, learning, and the ERN , 2008, Neuropsychologia.

[38]  Clay B. Holroyd,et al.  The feedback correct-related positivity: sensitivity of the event-related brain potential to unexpected positive feedback. , 2008, Psychophysiology.

[39]  Scott A. Huettel,et al.  Rapid Electrophysiological Brain Responses are Influenced by Both Valence and Magnitude of Monetary Rewards , 2008, Journal of Cognitive Neuroscience.

[40]  I. Daum,et al.  Learning‐related changes in reward expectancy are reflected in the feedback‐related negativity , 2008, The European journal of neuroscience.

[41]  R. Simons,et al.  The Neural Consequences of Flip-flopping: the Feedback- Related Negativity and Salience of Reward Prediction the Authors Thank Jenna Dietz and Natalie Shroyer for Their Help with Data Collection. We Also Thank , 2022 .

[42]  Sidney J Segalowitz,et al.  The error-related negativity is related to risk taking and empathy in young men. , 2009, Psychophysiology.

[43]  Xiaolin Zhou,et al.  The P300 and reward valence, magnitude, and expectancy in outcome evaluation , 2009, Brain Research.

[44]  Maarten A. S. Boksem,et al.  The Importance of Failure: Feedback Related Negativity Predicts Motor Learning Efficiency , 2009, NeuroImage.

[45]  Giuseppe Sartori,et al.  Brain correlates of risky decision-making , 2010, NeuroImage.

[46]  Christian Bellebaum,et al.  It was not MY fault: event-related brain potentials in active and observational learning from feedback. , 2010, Cerebral cortex.

[47]  Uta Sailer,et al.  Manipulation of feedback expectancy and valence induces negative and positive reward prediction error signals manifest in event-related brain potentials. , 2011, Psychophysiology.

[48]  N Kathmann,et al.  Impaired decision making and feedback evaluation in borderline personality disorder , 2011, Psychological Medicine.

[49]  Qingguo Ma,et al.  How an uncertain cue modulates subsequent monetary outcome evaluation: An ERP study , 2011, Neuroscience Letters.