Cognitive Regulation during Decision Making Shifts Behavioral Control between Ventromedial and Dorsolateral Prefrontal Value Systems

Cognitive regulation is often used to influence behavioral outcomes. However, the computational and neurobiological mechanisms by which it affects behavior remain unknown. We studied this issue using an fMRI task in which human participants used cognitive regulation to upregulate and downregulate their cravings for foods at the time of choice. We found that activity in both ventromedial prefrontal cortex (vmPFC) and dorsolateral prefrontal cortex (dlPFC) correlated with value. We also found evidence that two distinct regulatory mechanisms were at work: value modulation, which operates by changing the values assigned to foods in vmPFC and dlPFC at the time of choice, and behavioral control modulation, which operates by changing the relative influence of the vmPFC and dlPFC value signals on the action selection process used to make choices. In particular, during downregulation, activation decreased in the value-sensitive region of dlPFC (indicating value modulation) but not in vmPFC, and the relative contribution of the two value signals to behavior shifted toward the dlPFC (indicating behavioral control modulation). The opposite pattern was observed during upregulation: activation increased in vmPFC but not dlPFC, and the relative contribution to behavior shifted toward the vmPFC. Finally, ventrolateral PFC and posterior parietal cortex were more active during both upregulation and downregulation, and were functionally connected with vmPFC and dlPFC during cognitive regulation, which suggests that they help to implement the changes to the decision-making circuitry generated by cognitive regulation.

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

[2]  J. Townsend,et al.  Decision field theory: a dynamic-cognitive approach to decision making in an uncertain environment. , 1993, Psychological review.

[3]  R. Frances,et al.  Cognitive therapy of substance abuse , 1994 .

[4]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[5]  J. Gross Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. , 1998, Journal of personality and social psychology.

[6]  P. Montague,et al.  Neural Economics and the Biological Substrates of Valuation , 2002, Neuron.

[7]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[8]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

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

[10]  W. Newsome,et al.  Choosing the greater of two goods: neural currencies for valuation and decision making , 2005, Nature Reviews Neuroscience.

[11]  David Badre,et al.  Frontal lobe mechanisms that resolve proactive interference. , 2005, Cerebral cortex.

[12]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[13]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[14]  Jonathan D. Cohen,et al.  The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. , 2006, Psychological review.

[15]  Sang Hee Kim,et al.  Neural Correlates of Positive and Negative Emotion Regulation , 2007, Journal of Cognitive Neuroscience.

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

[17]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

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

[20]  Roger Ratcliff,et al.  The Diffusion Decision Model: Theory and Data for Two-Choice Decision Tasks , 2008, Neural Computation.

[21]  Colin Camerer,et al.  Dissociating the Role of the Orbitofrontal Cortex and the Striatum in the Computation of Goal Values and Prediction Errors , 2008, The Journal of Neuroscience.

[22]  Daeyeol Lee,et al.  Prefrontal Coding of Temporally Discounted Values during Intertemporal Choice , 2008, Neuron.

[23]  Brent L. Hughes,et al.  Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008, Neuron.

[24]  M. Delgado,et al.  Regulating the expectation of reward via cognitive strategies , 2008, Nature Neuroscience.

[25]  V. Michel,et al.  An Automatic Valuation System in the Human Brain: Evidence from Functional Neuroimaging , 2009, Neuron.

[26]  D. Wolpert,et al.  Changing your mind: a computational mechanism of vacillation , 2009, Nature.

[27]  J. O'Doherty,et al.  Evidence for a Common Representation of Decision Values for Dissimilar Goods in Human Ventromedial Prefrontal Cortex , 2009, The Journal of Neuroscience.

[28]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[29]  P. Glimcher,et al.  The Neurobiology of Decision: Consensus and Controversy , 2009, Neuron.

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

[31]  M. Rushworth,et al.  General Mechanisms for Making Decisions? This Review Comes from a Themed Issue on Cognitive Neuroscience Edited the Representation of Value and Reward Expectations in Frontal Cortex Reward Prediction Errors and Learning Rates Other Types of Prediction Error , 2022 .

[32]  Ian Krajbich,et al.  Visual fixations and the computation and comparison of value in simple choice , 2010, Nature Neuroscience.

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

[34]  J. O'Doherty,et al.  Appetitive and Aversive goal values are encoded in the medial orbitofrontal cortex at the time of decision-making , 2009, NeuroImage.

[35]  Christof Koch,et al.  The Drift Diffusion Model Can Account for the Accuracy and Reaction Time of Value-Based Choices Under High and Low Time Pressure , 2010, Judgment and Decision Making.

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

[37]  F. Christian How the Brain Integrates Costs and Benefits During Decision Making , 2010 .

[38]  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.

[39]  A. Rangel,et al.  Dissociating valuation and saliency signals during decision-making. , 2011, Cerebral cortex.

[40]  Colin Camerer,et al.  Transformation of stimulus value signals into motor commands during simple choice , 2011, Proceedings of the National Academy of Sciences.

[41]  M. Woolrich,et al.  Mechanisms underlying cortical activity during value-guided choice , 2011, Nature Neuroscience.

[42]  Antonio Rangel,et al.  Decision value computation in DLPFC and VMPFC adjusts to the available decision time , 2012, The European journal of neuroscience.