Neuronal Remapping and Circuit Persistence in Economic Decisions

The orbitofrontal cortex plays a central role in good-based economic decisions. When subjects make choices, neurons in this region represent the identities and values of offered and chosen goods. Notably, choices in different behavioral contexts may involve a potentially infinite variety of goods. Thus a fundamental question concerns the stability versus flexibility of the decision circuit. Here we show in rhesus monkeys that neurons encoding the identity or the subjective value of particular goods in a given context 'remap' and become associated with different goods when the context changes. At the same time, the overall organization of the decision circuit and the function of individual cells remain stable across contexts. In particular, two neurons supporting the same decision in one context also support the same decision in different contexts. These results demonstrate how the same neural circuit can underlie economic decisions involving a large variety of goods.

[1]  N. Volkow,et al.  Drug addiction: the neurobiology of behaviour gone awry , 2004, Nature Reviews Neuroscience.

[2]  Sara E. Morrison,et al.  Different Time Courses for Learning-Related Changes in Amygdala and Orbitofrontal Cortex , 2011, Neuron.

[3]  W. Schultz,et al.  Adaptation of Reward Sensitivity in Orbitofrontal Neurons , 2010, The Journal of Neuroscience.

[4]  A. Agresti An introduction to categorical data analysis , 1997 .

[5]  T. Robbins,et al.  Decision making and neuropsychiatry , 2001, Trends in Cognitive Sciences.

[6]  J. Kable,et al.  Ventromedial Frontal Lobe Damage Disrupts Value Maximization in Humans , 2011, The Journal of Neuroscience.

[7]  P. Glimcher Foundations of Neuroeconomic Analysis , 2010 .

[8]  S. Thorpe,et al.  The orbitofrontal cortex: Neuronal activity in the behaving monkey , 2004, Experimental Brain Research.

[9]  T. R. Scott,et al.  Satiety-responsive neurons in the medial orbitofrontal cortex of the macaque. , 2008, Behavioral neuroscience.

[10]  Steven W Kennerley,et al.  Encoding of Gustatory Working Memory by Orbitofrontal Neurons , 2009, The Journal of Neuroscience.

[11]  M. Rushworth,et al.  Valuation and decision-making in frontal cortex: one or many serial or parallel systems? , 2012, Current Opinion in Neurobiology.

[12]  C. Padoa-Schioppa Neuronal Origins of Choice Variability in Economic Decisions , 2013, Neuron.

[13]  C. Padoa-Schioppa,et al.  Rational Attention and Adaptive Coding: A Puzzle and a Solution. , 2014, The American economic review.

[14]  J. Tebbs,et al.  An Introduction to Categorical Data Analysis , 2008 .

[15]  Joshua L. Jones,et al.  Orbitofrontal neurons acquire responses to ‘valueless’ Pavlovian cues during unblocking , 2014, eLife.

[16]  E. Rolls,et al.  Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. , 1996, Journal of neurophysiology.

[17]  C. Zelano,et al.  The value of identity: olfactory notes on orbitofrontal cortex function , 2011, Annals of the New York Academy of Sciences.

[18]  P. Tobler,et al.  Identity-specific coding of future rewards in the human orbitofrontal cortex , 2015, Proceedings of the National Academy of Sciences.

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

[20]  J. Verhagen,et al.  The neurocognitive bases of human multimodal food perception: Sensory integration , 2006, Neuroscience & Biobehavioral Reviews.

[21]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. Waltz,et al.  A review of reward processing and motivational impairment in schizophrenia. , 2014, Schizophrenia bulletin.

[23]  Jung Hoon Sul,et al.  Distinct Roles of Rodent Orbitofrontal and Medial Prefrontal Cortex in Decision Making , 2010, Neuron.

[24]  G. Schoenbaum,et al.  Orbitofrontal Cortex and Representation of Incentive Value in Associative Learning , 1999, The Journal of Neuroscience.

[25]  Minmin Luo,et al.  Prospective Coding of Dorsal Raphe Reward Signals by the Orbitofrontal Cortex , 2015, The Journal of Neuroscience.

[26]  P. Cisek Making decisions through a distributed consensus , 2012, Current Opinion in Neurobiology.

[27]  Timothy Edward John Behrens,et al.  Segregated Encoding of Reward–Identity and Stimulus–Reward Associations in Human Orbitofrontal Cortex , 2013, The Journal of Neuroscience.

[28]  C. Padoa-Schioppa,et al.  Integration of Multiple Determinants in the Neuronal Computation of Economic Values , 2014, The Journal of Neuroscience.

[29]  C. Padoa-Schioppa Range-Adapting Representation of Economic Value in the Orbitofrontal Cortex , 2009, The Journal of Neuroscience.

[30]  C. Padoa-Schioppa Neurobiology of economic choice: a good-based model. , 2011, Annual review of neuroscience.

[31]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[32]  C. Padoa-Schioppa,et al.  The representation of economic value in the orbitofrontal cortex is invariant for changes of menu , 2008, Nature Neuroscience.

[33]  R. Saunders,et al.  Prefrontal mechanisms of behavioral flexibility, emotion regulation and value updating , 2013, Nature Neuroscience.

[34]  S. S. Roley,et al.  Sensory Integration , 2013 .

[35]  Xiao-Jing Wang,et al.  Probabilistic Decision Making by Slow Reverberation in Cortical Circuits , 2002, Neuron.

[36]  C. Padoa-Schioppa,et al.  A neuro-computational model of economic decisions. , 2015, Journal of neurophysiology.

[37]  J. Neter,et al.  Applied linear statistical models : regression, analysis of variance, and experimental designs , 1974 .

[38]  R. K. Simpson Nature Neuroscience , 2022 .

[39]  D. Small Flavor is in the brain , 2012, Physiology & Behavior.

[40]  W. Schultz Neuronal Reward and Decision Signals: From Theories to Data. , 2015, Physiological reviews.

[41]  C. Salzman,et al.  Abstract Context Representations in Primate Amygdala and Prefrontal Cortex , 2015, Neuron.

[42]  C. Padoa-Schioppa,et al.  Contributions of Orbitofrontal and Lateral Prefrontal Cortices to Economic Choice and the Good-to-Action Transformation , 2014, Neuron.

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

[44]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[45]  Antonio Rangel,et al.  Neural computations associated with goal-directed choice , 2010, Current Opinion in Neurobiology.

[46]  Neil Burgess,et al.  Attractor Dynamics in the Hippocampal Representation of the Local Environment , 2005, Science.