Differential Encoding of Losses and Gains in the Human Striatum

Studies on human monetary prediction and decision making emphasize the role of the striatum in encoding prediction errors for financial reward. However, less is known about how the brain encodes financial loss. Using Pavlovian conditioning of visual cues to outcomes that simultaneously incorporate the chance of financial reward and loss, we show that striatal activation reflects positively signed prediction errors for both. Furthermore, we show functional segregation within the striatum, with more anterior regions showing relative selectivity for rewards and more posterior regions for losses. These findings mirror the anteroposterior valence-specific gradient reported in rodents and endorse the role of the striatum in aversive motivational learning about financial losses, illustrating functional and anatomical consistencies with primary aversive outcomes such as pain.

[1]  Richard Hunter Integrative activity of the brain. An interdisciplinary approach , 1969 .

[2]  R. W. Schulz The Psychology of Fear and Stress , 1974 .

[3]  A G Barto,et al.  Toward a modern theory of adaptive networks: expectation and prediction. , 1981, Psychological review.

[4]  D. Amaral,et al.  The amygdalostriatal projections in the monkey. An anterograde tracing study , 1985, Brain Research.

[5]  R. Dantzer The Psychology of Fear and Stress, J.A. Gray (Ed.). Cambridge University Press, Cambridge (1987), viii and 422 pp, ISBN 0-521-27098-7 , 1989 .

[6]  Richard S. Sutton,et al.  Time-Derivative Models of Pavlovian Reinforcement , 1990 .

[7]  M. Gabriel,et al.  Learning and Computational Neuroscience: Foundations of Adaptive Networks , 1990 .

[8]  O. Hikosaka Models of information processing in the basal Ganglia edited by James C. Houk, Joel L. Davis and David G. Beiser, The MIT Press, 1995. $60.00 (400 pp) ISBN 0 262 08234 9 , 1995, Trends in Neurosciences.

[9]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[11]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[12]  J. Feldon,et al.  Behavioral neurochemistry reveals a new functional dichotomy in the shell subregion of the nucleus accumbens , 1999, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[13]  T. Robbins,et al.  Associative Processes in Addiction and Reward The Role of Amygdala‐Ventral Striatal Subsystems , 1999, Annals of the New York Academy of Sciences.

[14]  S. Ikemoto,et al.  The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking , 1999, Brain Research Reviews.

[15]  M. Molliver,et al.  Dual Serotonin (5-HT) Projections to the Nucleus Accumbens Core and Shell: Relation of the 5-HT Transporter to Amphetamine-Induced Neurotoxicity , 2000, The Journal of Neuroscience.

[16]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[17]  J. Horvitz Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

[18]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[19]  D. Kahneman,et al.  Functional Imaging of Neural Responses to Expectancy and Experience of Monetary Gains and Losses tasks with monetary payoffs , 2001 .

[20]  H. Breiter,et al.  Reward Circuitry Activation by Noxious Thermal Stimuli , 2001, Neuron.

[21]  K. Berridge,et al.  Fear and Feeding in the Nucleus Accumbens Shell: Rostrocaudal Segregation of GABA-Elicited Defensive Behavior Versus Eating Behavior , 2001, The Journal of Neuroscience.

[22]  Sham M. Kakade,et al.  Opponent interactions between serotonin and dopamine , 2002, Neural Networks.

[23]  Kenji Doya,et al.  Metalearning and neuromodulation , 2002, Neural Networks.

[24]  P. Montague,et al.  Activity in human ventral striatum locked to errors of reward prediction , 2002, Nature Neuroscience.

[25]  Moshe Levy,et al.  Prospect Theory: Much Ado About Nothing? , 2002, Manag. Sci..

[26]  K. Berridge,et al.  Positive and Negative Motivation in Nucleus Accumbens Shell: Bivalent Rostrocaudal Gradients for GABA-Elicited Eating, Taste “Liking”/“Disliking” Reactions, Place Preference/Avoidance, and Fear , 2002, The Journal of Neuroscience.

[27]  S. Kapur,et al.  Direct Activation of the Ventral Striatum in Anticipation of Aversive Stimuli , 2003, Neuron.

[28]  K. Berridge,et al.  Glutamate motivational ensembles in nucleus accumbens: rostrocaudal shell gradients of fear and feeding , 2003, The European journal of neuroscience.

[29]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

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

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

[32]  G. Schoenbaum,et al.  Lesions of Nucleus Accumbens Disrupt Learning about Aversive Outcomes , 2003, The Journal of Neuroscience.

[33]  G. Schoenbaum,et al.  Neural Encoding in Ventral Striatum during Olfactory Discrimination Learning , 2003, Neuron.

[34]  G. Pagnoni,et al.  Human Striatal Response to Salient Nonrewarding Stimuli , 2003, The Journal of Neuroscience.

[35]  R. Wise Dopamine, learning and motivation , 2004, Nature Reviews Neuroscience.

[36]  Saori C. Tanaka,et al.  Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops , 2004, Nature Neuroscience.

[37]  Jonathan D. Cohen,et al.  Computational roles for dopamine in behavioural control , 2004, Nature.

[38]  C. Bradshaw,et al.  The fear-inhibited light reflex: importance of the anticipation of an aversive event. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  M. Ungless Dopamine: the salient issue , 2004, Trends in Neurosciences.

[40]  K. Doya,et al.  A Neural Correlate of Reward-Based Behavioral Learning in Caudate Nucleus: A Functional Magnetic Resonance Imaging Study of a Stochastic Decision Task , 2004, The Journal of Neuroscience.

[41]  Peter Dayan,et al.  Temporal difference models describe higher-order learning in humans , 2004, Nature.

[42]  Karl J. Friston,et al.  Opponent appetitive-aversive neural processes underlie predictive learning of pain relief , 2005, Nature Neuroscience.

[43]  Dirk J. Heslenfeld,et al.  Activity in human reward-sensitive brain areas is strongly context dependent , 2005, NeuroImage.

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

[45]  P. Dayan,et al.  Dopamine, uncertainty and TD learning , 2005, Behavioral and Brain Functions.

[46]  E. Bowman,et al.  Rat nucleus accumbens neurons predominantly respond to the outcome-related properties of conditioned stimuli rather than their behavioral-switching properties. , 2005, Journal of neurophysiology.

[47]  M. Roitman,et al.  Nucleus Accumbens Neurons Are Innately Tuned for Rewarding and Aversive Taste Stimuli, Encode Their Predictors, and Are Linked to Motor Output , 2005, Neuron.

[48]  R. Dolan,et al.  Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans , 2006, Nature.

[49]  Kenji Doya,et al.  Brain mechanism of reward prediction under predictable and unpredictable environmental dynamics , 2006, Neural Networks.

[50]  E. Vaadia,et al.  Midbrain dopamine neurons encode decisions for future action , 2006, Nature Neuroscience.

[51]  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.

[52]  R. Poldrack Can cognitive processes be inferred from neuroimaging data? , 2006, Trends in Cognitive Sciences.

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

[54]  Sabrina M. Tom,et al.  The Neural Basis of Loss Aversion in Decision-Making Under Risk , 2007, Science.