Behavioral / Cognitive Interactions between Dorsolateral and Ventromedial Prefrontal Cortex Underlie Context-Dependent Stimulus Valuation in Goal-Directed Choice

External circumstances and internal bodily states often change and require organisms to flexibly adapt valuation processes to select the optimal action in a given context. Here, we investigate the neurobiology of context-dependent valuation in 22 human subjects using functional magnetic resonance imaging. Subjects made binary choices between visual stimuli with three attributes (shape, color, and pattern) that were associated with monetary values. Context changes required subjects to deviate from the default shape valuation and to integrate a second attribute to comply with the goal to maximize rewards. Critically, this binary choice task did not involve any conflict between opposing monetary, temporal, or social preferences. We tested the hypothesis that interactions between regions of dorsolateral prefrontal cortex (dlPFC) and ventromedial prefrontal cortex (vmPFC) implicated in self-control choices would also underlie the more general function of context-dependent valuation. Consistent with this idea, we found that the degree to which stimulus attributes were reflected in vmPFC activity varied as a function of context. In addition, activity in dlPFC increased when context changes required a reweighting of stimulus attribute values. Moreover, the strength of the functional connectivity between dlPFC and vmPFC was associated with the degree of context-specific attribute valuation in vmPFC at the time of choice. Our findings suggest that functional interactions between dlPFC and vmPFC are a key aspect of context-dependent valuation and that the role of this network during choices that require self-control to adjudicate between competing outcome preferences is a specific application of this more general neural mechanism.

[1]  A. Rangel,et al.  Informatic parcellation of the network involved in the computation of subjective value. , 2014, Social cognitive and affective neuroscience.

[2]  A. Rangel,et al.  Activity in dlPFC and its effective connectivity to vmPFC are associated with temporal discounting , 2014, Front. Neurosci..

[3]  Thomas H. B. FitzGerald,et al.  Reward-Related Activity in Ventral Striatum Is Action Contingent and Modulated by Behavioral Relevance , 2014, The Journal of Neuroscience.

[4]  A. Harris,et al.  Temporally Dissociable Mechanisms of Self-Control: Early Attentional Filtering Versus Late Value Modulation , 2013, The Journal of Neuroscience.

[5]  Joseph W. Kable,et al.  The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value , 2013, NeuroImage.

[6]  Michael L. Platt,et al.  Social Signals in Primate Orbitofrontal Cortex , 2012, Current Biology.

[7]  Robert C. Wilson,et al.  Inferring Relevance in a Changing World , 2012, Front. Hum. Neurosci..

[8]  George Ainslie,et al.  Moderators of the association between brain activation and farsighted choice , 2012, NeuroImage.

[9]  E. Fehr,et al.  Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice , 2011, Nature Neuroscience.

[10]  J. Malmaud,et al.  Focusing Attention on the Health Aspects of Foods Changes Value Signals in vmPFC and Improves Dietary Choice , 2011, The Journal of Neuroscience.

[11]  Jan Peters,et al.  The neural mechanisms of inter-temporal decision-making: understanding variability , 2011, Trends in Cognitive Sciences.

[12]  John M. Pearson,et al.  Posterior cingulate cortex: adapting behavior to a changing world , 2011, Trends in Cognitive Sciences.

[13]  J. Weber,et al.  Prefrontal–striatal pathway underlies cognitive regulation of craving , 2010, Proceedings of the National Academy of Sciences.

[14]  Eric J. Johnson,et al.  Lateral prefrontal cortex and self-control in intertemporal choice , 2010, Nature Neuroscience.

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

[16]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[17]  Colin Camerer,et al.  Self-control in decision-making involves modulation of the vmPFC valuation system , 2009, NeuroImage.

[18]  Peter Fransson,et al.  The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis , 2008, NeuroImage.

[19]  Á. Pascual-Leone,et al.  Studying the neurobiology of social interaction with transcranial direct current stimulation--the example of punishing unfairness. , 2008, Cerebral cortex.

[20]  Jim M. Monti,et al.  Neural Integration of Top-Down Spatial and Feature-Based Information in Visual Search , 2008, The Journal of Neuroscience.

[21]  U. Fischbacher,et al.  The Neural Signature of Social Norm Compliance , 2007, Neuron.

[22]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[23]  Á. Pascual-Leone,et al.  Diminishing Reciprocal Fairness by Disrupting the Right Prefrontal Cortex , 2006, Science.

[24]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

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

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

[27]  Jonathan D. Cohen,et al.  The Neural Basis of Economic Decision-Making in the Ultimatum Game , 2003, Science.

[28]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[29]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[30]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[31]  Jack L. Lancaster,et al.  The Talairach Daemon a database server for talairach atlas labels , 1997 .

[32]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[33]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.