How the brain integrates costs and bene fi ts during decision making

When we make decisions, the benefits of an option often need to be weighed against accompanying costs. Little is known, however, about the neural systems underlying such cost–benefit computations. Using functional magnetic resonance imaging and choice modeling, we show that decision making based on cost–benefit comparison can be explained as a stochastic accumulation of cost–benefit difference. Model-driven functional MRI shows that ventromedial and left dorsolateral prefrontal cortex compare costs and benefits by computing the difference between neural signatures of anticipated benefits and costs from the ventral striatum and amygdala, respectively. Moreover, changes in blood oxygen level dependent (BOLD) signal in the bilateral middle intraparietal sulcus reflect the accumulation of the difference signal from ventromedial prefrontal cortex. In sum, we show that a neurophysiological mechanism previously established for perceptual decision making, that is, the difference-based accumulation of evidence, is fundamental also in value-based decisions. The brain, thus, weighs costs against benefits by combining neural benefit and cost signals into a single, difference-based neural representation of net value, which is accumulated over time until the individual decides to accept or reject an option.

[1]  M. Farah,et al.  Cerebral Cortex doi:10.1093/cercor/bhl176 The Role of Ventromedial Prefrontal Cortex in Decision Making: Judgment under Uncertainty or Judgment Per Se? , 2007 .

[2]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[3]  M. Shadlen,et al.  The effect of stimulus strength on the speed and accuracy of a perceptual decision. , 2005, Journal of vision.

[4]  M. D’Esposito,et al.  The functional anatomy of a perceptual decision in the human brain. , 2010, Journal of neurophysiology.

[5]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[6]  H. Damasio,et al.  Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. , 2000, Brain : a journal of neurology.

[7]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[8]  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.

[9]  R. Ratcliff,et al.  Neural Representation of Task Difficulty and Decision Making during Perceptual Categorization: A Timing Diagram , 2006, The Journal of Neuroscience.

[10]  J. Gold,et al.  Neural computations that underlie decisions about sensory stimuli , 2001, Trends in Cognitive Sciences.

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

[12]  J. O'Doherty,et al.  Model‐Based fMRI and Its Application to Reward Learning and Decision Making , 2007, Annals of the New York Academy of Sciences.

[13]  L. Fellows Deciding how to decide: ventromedial frontal lobe damage affects information acquisition in multi-attribute decision making. , 2006, Brain : a journal of neurology.

[14]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[15]  Xiao-Jing Wang,et al.  Cortico–basal ganglia circuit mechanism for a decision threshold in reaction time tasks , 2006, Nature Neuroscience.

[16]  Colin Camerer,et al.  Amygdala damage eliminates monetary loss aversion , 2010, Proceedings of the National Academy of Sciences.

[17]  Marios G Philiastides,et al.  A mechanistic account of value computation in the human brain , 2010, Proceedings of the National Academy of Sciences.

[18]  Leslie G. Ungerleider,et al.  A general mechanism for perceptual decision-making in the human brain , 2004, Nature.

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

[20]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[21]  Roger Ratcliff,et al.  A Theory of Memory Retrieval. , 1978 .

[22]  Jonathan D. Cohen,et al.  Dissociating working memory from task difficulty in human prefrontal cortex , 1997, Neuropsychologia.

[23]  Philip L. Smith,et al.  Psychology and neurobiology of simple decisions , 2004, Trends in Neurosciences.

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

[25]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[26]  Jonathan D. Cohen,et al.  Functional Imaging of Decision Conflict , 2008, The Journal of Neuroscience.

[27]  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.

[28]  James L. McClelland,et al.  The time course of perceptual choice: the leaky, competing accumulator model. , 2001, Psychological review.

[29]  H. Damasio,et al.  Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex , 1998, The Journal of Neuroscience.

[30]  M. Shadlen,et al.  A role for neural integrators in perceptual decision making. , 2003, Cerebral cortex.

[31]  T. Paus,et al.  Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex: a review of 107 PET activation studies , 1998, Neuroreport.

[32]  Jeffrey C. Cooper,et al.  Functional magnetic resonance imaging of reward prediction , 2005, Current opinion in neurology.

[33]  J. Gläscher,et al.  Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. , 2009, Cerebral cortex.