Risk-dependent reward value signal in human prefrontal cortex

When making choices under uncertainty, people usually consider both the expected value and risk of each option, and choose the one with the higher utility. Expected value increases the expected utility of an option for all individuals. Risk increases the utility of an option for risk-seeking individuals, but decreases it for risk averse individuals. In 2 separate experiments, one involving imperative (no-choice), the other choice situations, we investigated how predicted risk and expected value aggregate into a common reward signal in the human brain. Blood oxygen level dependent responses in lateral regions of the prefrontal cortex increased monotonically with increasing reward value in the absence of risk in both experiments. Risk enhanced these responses in risk-seeking participants, but reduced them in risk-averse participants. The aggregate value and risk responses in lateral prefrontal cortex contrasted with pure value signals independent of risk in the striatum. These results demonstrate an aggregate risk and value signal in the prefrontal cortex that would be compatible with basic assumptions underlying the mean-variance approach to utility.

[1]  D. Stuss,et al.  Impulsivity and risk-taking behavior in focal frontal lobe lesions , 2008, Neuropsychologia.

[2]  Simon Hong,et al.  The Globus Pallidus Sends Reward-Related Signals to the Lateral Habenula , 2008, Neuron.

[3]  W. Schultz,et al.  Influence of Reward Delays on Responses of Dopamine Neurons , 2008, The Journal of Neuroscience.

[4]  Colin Camerer,et al.  A framework for studying the neurobiology of value-based decision making , 2008, Nature Reviews Neuroscience.

[5]  I. Tsuda,et al.  Reward prediction based on stimulus categorization in primate lateral prefrontal cortex , 2008, Nature Neuroscience.

[6]  M. Roesch,et al.  Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards , 2007, Nature Neuroscience.

[7]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[8]  J. O'Doherty,et al.  Orbitofrontal Cortex Encodes Willingness to Pay in Everyday Economic Transactions , 2007, The Journal of Neuroscience.

[9]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[10]  W. Schultz Multiple dopamine functions at different time courses. , 2007, Annual review of neuroscience.

[11]  Á. Pascual-Leone,et al.  Activation of Prefrontal Cortex by Transcranial Direct Current Stimulation Reduces Appetite for Risk during Ambiguous Decision Making , 2007, The Journal of Neuroscience.

[12]  A. Lüthi,et al.  Processing of Temporal Unpredictability in Human and Animal Amygdala , 2007, The Journal of Neuroscience.

[13]  R. Dolan,et al.  How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation , 2007, Science.

[14]  J. O'Doherty,et al.  Reward Value Coding Distinct From Risk Attitude-Related Uncertainty Coding in Human Reward Systems , 2006, Journal of neurophysiology.

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

[16]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[17]  J. Gläscher,et al.  Dissociable Systems for Gain- and Loss-Related Value Predictions and Errors of Prediction in the Human Brain , 2006, The Journal of Neuroscience.

[18]  S. Quartz,et al.  Neural Differentiation of Expected Reward and Risk in Human Subcortical Structures , 2006, Neuron.

[19]  Lorena R. R. Gianotti,et al.  Disruption of Right Prefrontal Cortex by Low-Frequency Repetitive Transcranial Magnetic Stimulation Induces Risk-Taking Behavior , 2006, The Journal of Neuroscience.

[20]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

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

[22]  K. Berman,et al.  Cerebral Cortex doi:10.1093/cercor/bhj004 Neural Coding of Distinct Statistical Properties of Reward Information in Humans , 2005 .

[23]  Evan M. Gordon,et al.  Neural Signatures of Economic Preferences for Risk and Ambiguity , 2006, Neuron.

[24]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[25]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[26]  Colin Camerer,et al.  Neural Systems Responding to Degrees of Uncertainty in Human Decision-Making , 2005, Science.

[27]  M. Platt,et al.  Risk-sensitive neurons in macaque posterior cingulate cortex , 2005, Nature Neuroscience.

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

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

[30]  W. Schultz,et al.  Adaptive Coding of Reward Value by Dopamine Neurons , 2005, Science.

[31]  P. Glimcher,et al.  Neuroeconomics: The Consilience of Brain and Decision , 2004, Science.

[32]  H. Levy,et al.  Prospect Theory and Mean-Variance Analysis , 2004 .

[33]  R. Hertwig,et al.  Decisions from Experience and the Effect of Rare Events in Risky Choice , 2004, Psychological science.

[34]  T. Robbins,et al.  The neuropsychology of ventral prefrontal cortex: Decision-making and reversal learning , 2004, Brain and Cognition.

[35]  D. Barraclough,et al.  Prefrontal cortex and decision making in a mixed-strategy game , 2004, Nature Neuroscience.

[36]  E. Weber,et al.  Predicting Risk-Sensitivity in Humans and Lower Animals: Risk as Variance or Coefficient of Variation , 2004, Psychological review.

[37]  John F. Kalaska,et al.  Faculty Opinions recommendation of Neuronal correlates of a perceptual decision in ventral premotor cortex. , 2004 .

[38]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

[39]  Leslie G. Ungerleider,et al.  Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys , 2004, Experimental Brain Research.

[40]  Reid Hastie,et al.  Phineas gauged: decision-making and the human prefrontal cortex , 2003, Neuropsychologia.

[41]  J. C. Crowley,et al.  Saccade Reward Signals in Posterior Cingulate Cortex , 2003, Neuron.

[42]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[43]  M. Delgado,et al.  Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations , 2003, Cognitive, affective & behavioral neuroscience.

[44]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[45]  J. Deakin,et al.  Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement , 2002, Psychopharmacology.

[46]  O. Hikosaka,et al.  Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex. , 2002, Journal of neurophysiology.

[47]  J. Sanes,et al.  Improved Detection of Event-Related Functional MRI Signals Using Probability Functions , 2001, NeuroImage.

[48]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[49]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[50]  H. Damasio,et al.  Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. , 2000, Brain : a journal of neurology.

[51]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  Richard Gonzalez,et al.  On the Shape of the Probability Weighting Function , 1999, Cognitive Psychology.

[53]  D. Kahneman,et al.  Back to Bentham? Explorations of experience utility , 1997 .

[54]  Anna Nagurney,et al.  Foundations of Financial Economics , 1997 .

[55]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

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

[57]  P. Wakker Separating marginal utility and probabilistic risk aversion , 1994 .

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

[59]  K Tanaka,et al.  Neuronal mechanisms of object recognition. , 1993, Science.

[60]  H. Barbas,et al.  Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey , 1990, The Journal of comparative neurology.

[61]  T. Caraco,et al.  Risk-sensitivity: ambient temperature affects foraging choice , 1990, Animal Behaviour.

[62]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[63]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[64]  J. Ingersoll Theory of Financial Decision Making , 1987 .

[65]  P. Goldman-Rakic,et al.  Organization of the nigrothalamocortical system in the rhesus monkey , 1985, The Journal of comparative neurology.

[66]  Thomas Caraco,et al.  ON FORAGING TIME ALLOCATION IN A STOCHASTIC ENVIRONMENT , 1980 .

[67]  H. Levy,et al.  Approximating Expected Utility by a Function of Mean and Variance , 1979 .

[68]  Stephen A. Ross,et al.  Equilibrium and Agency--Inadmissible Agents in the Public Agency Problem , 1979 .

[69]  M. Rothschild,et al.  Increasing risk: I. A definition , 1970 .

[70]  J. Pratt RISK AVERSION IN THE SMALL AND IN THE LARGE11This research was supported by the National Science Foundation (grant NSF-G24035). Reproduction in whole or in part is permitted for any purpose of the United States Government. , 1964 .

[71]  A. Stuart,et al.  Portfolio Selection: Efficient Diversification of Investments , 1959 .

[72]  J. Tobin Liquidity Preference as Behavior towards Risk , 1958 .

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

[74]  G. Stigler The Development of Utility Theory. I , 1950, Journal of Political Economy.

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

[76]  J. Neumann,et al.  Theory of games and economic behavior , 1945, 100 Years of Math Milestones.