Dissociating the Role of the Orbitofrontal Cortex and the Striatum in the Computation of Goal Values and Prediction Errors

To make sound economic decisions, the brain needs to compute several different value-related signals. These include goal values that measure the predicted reward that results from the outcome generated by each of the actions under consideration, decision values that measure the net value of taking the different actions, and prediction errors that measure deviations from individuals' previous reward expectations. We used functional magnetic resonance imaging and a novel decision-making paradigm to dissociate the neural basis of these three computations. Our results show that they are supported by different neural substrates: goal values are correlated with activity in the medial orbitofrontal cortex, decision values are correlated with activity in the central orbitofrontal cortex, and prediction errors are correlated with activity in the ventral striatum.

[1]  M. Degroot,et al.  Measuring utility by a single-response sequential method. , 1964, Behavioral science.

[2]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[3]  Andrew G. Barto,et al.  Reinforcement learning , 1998 .

[4]  J. Hollerman,et al.  Dopamine neurons report an error in the temporal prediction of reward during learning , 1998, Nature Neuroscience.

[5]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[6]  M. Preul.  The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

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

[8]  N. Logothetis.  The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[10]  Samuel M. McClure,et al.  Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum , 2003, Neuron.

[11]  Karl J. Friston,et al.  Temporal Difference Models and Reward-Related Learning in the Human Brain , 2003, Neuron.

[12]  W. van den Brink,et al.  Substance use disorders and the orbitofrontal cortex: systematic review of behavioural decision-making and neuroimaging studies. , 2005, The British journal of psychiatry : the journal of mental science.

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

[14]  Simon J Graham,et al.  Functional neuroanatomical substrates of altered reward processing in major depressive disorder revealed by a dopaminergic probe. , 2005, Archives of general psychiatry.

[15]  N. Volkow,et al.  The neural basis of addiction: a pathology of motivation and choice. , 2005, The American journal of psychiatry.

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

[17]  A. Hariri,et al.  Preference for Immediate over Delayed Rewards Is Associated with Magnitude of Ventral Striatal Activity , 2006, The Journal of Neuroscience.

[18]  C. Carter,et al.  Reward-related decision-making in pediatric major depressive disorder: an fMRI study. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[19]  J. O'Doherty,et al.  Predictive Neural Coding of Reward Preference Involves Dissociable Responses in Human Ventral Midbrain and Ventral Striatum , 2006, Neuron.

[20]  J. O'Doherty,et al.  Human Neural Learning Depends on Reward Prediction Errors in the Blocking Paradigm , 2005, Journal of neurophysiology.

[21]  R. Poldrack,et al.  Ventral–striatal/nucleus–accumbens sensitivity to prediction errors during classification learning , 2006, Human brain mapping.

[22]  Arno Villringer,et al.  Dysfunction of ventral striatal reward prediction in schizophrenia , 2006, NeuroImage.

[23]  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.

[24]  Samuel M. McClure,et al.  Policy Adjustment in a Dynamic Economic Game , 2006, PloS one.

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

[26]  P. Glimcher,et al.  Statistics of midbrain dopamine neuron spike trains in the awake primate. , 2007, Journal of neurophysiology.

[27]  Michael Rotte,et al.  Favorite brands as cultural objects modulate reward circuit , 2007, Neuroreport.

[28]  Martin P Paulus,et al.  Decision-Making Dysfunctions in Psychiatry—Altered Homeostatic Processing? , 2007, Science.

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

[30]  J. O'Doherty,et al.  Neural coding of reward-prediction error signals during classical conditioning with attractive faces. , 2007, Journal of neurophysiology.

[31]  G. Loewenstein,et al.  Neural Predictors of Purchases , 2007, Neuron.

[32]  J. Gläscher,et al.  Gene–gene interaction associated with neural reward sensitivity , 2007, Proceedings of the National Academy of Sciences.

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

[34]  E T Bullmore,et al.  Substantia nigra/ventral tegmental reward prediction error disruption in psychosis , 2008, Molecular Psychiatry.

[35]  E. Rolls,et al.  Cerebral Cortex Advance Access published June 22, 2007 Expected Value, Reward Outcome, and Temporal Difference Error Representations in a Probabilistic Decision Task , 2022 .