Capturing the temporal evolution of choice across prefrontal cortex

Activity in prefrontal cortex (PFC) has been richly described using economic models of choice. Yet such descriptions fail to capture the dynamics of decision formation. Describing dynamic neural processes has proven challenging due to the problem of indexing the internal state of PFC and its trial-by-trial variation. Using primate neurophysiology and human magnetoencephalography, we here recover a single-trial index of PFC internal states from multiple simultaneously recorded PFC subregions. This index can explain the origins of neural representations of economic variables in PFC. It describes the relationship between neural dynamics and behaviour in both human and monkey PFC, directly bridging between human neuroimaging data and underlying neuronal activity. Moreover, it reveals a functionally dissociable interaction between orbitofrontal cortex, anterior cingulate cortex and dorsolateral PFC in guiding cost-benefit decisions. We cast our observations in terms of a recurrent neural network model of choice, providing formal links to mechanistic dynamical accounts of decision-making. DOI: http://dx.doi.org/10.7554/eLife.11945.001

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

[2]  Bruno Rossion,et al.  Figures and figure supplements , 2014 .

[3]  N. Parga,et al.  Dynamic Control of Response Criterion in Premotor Cortex during Perceptual Detection under Temporal Uncertainty , 2015, Neuron.

[4]  Mark M Churchland,et al.  Vacillation, indecision and hesitation in moment-by-moment decoding of monkey motor cortex , 2015, eLife.

[5]  H. Kennedy,et al.  A Large-Scale Circuit Mechanism for Hierarchical Dynamical Processing in the Primate Cortex , 2015, Neuron.

[6]  Gustavo Deco,et al.  Task-driven intra- and interarea communications in primate cerebral cortex , 2014, Proceedings of the National Academy of Sciences.

[7]  Timothy E. J. Behrens,et al.  Hierarchical competitions subserving multi-attribute choice , 2014, Nature Neuroscience.

[8]  Zachary F Mainen,et al.  Neural antecedents of self-initiated actions in secondary motor cortex , 2014, Nature Neuroscience.

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

[10]  Il Memming Park,et al.  Encoding and decoding in parietal cortex during sensorimotor decision-making , 2014, Nature Neuroscience.

[11]  Christopher J. Cueva,et al.  Dynamics of Neural Population Responses in Prefrontal Cortex Indicate Changes of Mind on Single Trials , 2014, Current Biology.

[12]  Tommy C. Blanchard,et al.  Reward Value Comparison via Mutual Inhibition in Ventromedial Prefrontal Cortex , 2014, Neuron.

[13]  J. O'Doherty,et al.  The problem with value , 2014, Neuroscience & Biobehavioral Reviews.

[14]  Laurence T. Hunt,et al.  What are the neural origins of choice variability? , 2014, Trends in Cognitive Sciences.

[15]  P. Cisek,et al.  Deliberation and Commitment in the Premotor and Primary Motor Cortex during Dynamic Decision Making , 2014, Neuron.

[16]  Tommy C. Blanchard,et al.  Neurons in Dorsal Anterior Cingulate Cortex Signal Postdecisional Variables in a Foraging Task , 2014, The Journal of Neuroscience.

[17]  M. Greicius,et al.  The Will to Persevere Induced by Electrical Stimulation of the Human Cingulate Gyrus , 2013, Neuron.

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

[19]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[20]  Steven W Kennerley,et al.  Single-Neuron Mechanisms Underlying Cost-Benefit Analysis in Frontal Cortex , 2013, The Journal of Neuroscience.

[21]  Aaron C. Koralek,et al.  Temporally Precise Cell-Specific Coherence Develops in Corticostriatal Networks during Learning , 2013, Neuron.

[22]  Mark W. Woolrich,et al.  Trial-Type Dependent Frames of Reference for Value Comparison , 2013, PLoS Comput. Biol..

[23]  Gustavo Deco,et al.  Coherent delta-band oscillations between cortical areas correlate with decision making , 2013, Proceedings of the National Academy of Sciences.

[24]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[25]  P. Dayan,et al.  Effort and Valuation in the Brain: The Effects of Anticipation and Execution , 2013, The Journal of Neuroscience.

[26]  Timothy Edward John Behrens,et al.  Ventromedial Prefrontal and Anterior Cingulate Cortex Adopt Choice and Default Reference Frames during Sequential Multi-Alternative Choice , 2013, The Journal of Neuroscience.

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

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

[29]  J. Ditterich,et al.  Neural Dynamics of Choice: Single-Trial Analysis of Decision-Related Activity in Parietal Cortex , 2012, The Journal of Neuroscience.

[30]  Christopher Summerfield,et al.  Building Bridges between Perceptual and Economic Decision-Making: Neural and Computational Mechanisms , 2012, Front. Neurosci..

[31]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[32]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[33]  C. Padoa-Schioppa,et al.  Neuronal Encoding of Subjective Value in Dorsal and Ventral Anterior Cingulate Cortex , 2012, The Journal of Neuroscience.

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

[35]  L. Fellows,et al.  Double Dissociation of Stimulus-Value and Action-Value Learning in Humans with Orbitofrontal or Anterior Cingulate Cortex Damage , 2011, The Journal of Neuroscience.

[36]  Timothy E. J. Behrens,et al.  Double dissociation of value computations in orbitofrontal and anterior cingulate neurons , 2011, Nature Neuroscience.

[37]  Antonio Rangel,et al.  The Decision Value Computations in the vmPFC and Striatum Use a Relative Value Code That is Guided by Visual Attention , 2011, The Journal of Neuroscience.

[38]  I. L. Nieuwenhuis,et al.  The role of the ventromedial prefrontal cortex in memory consolidation , 2011, Behavioural Brain Research.

[39]  Timothy Edward John Behrens,et al.  Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex , 2010, Proceedings of the National Academy of Sciences.

[40]  Mathias Pessiglione,et al.  Separate Valuation Subsystems for Delay and Effort Decision Costs , 2010, The Journal of Neuroscience.

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

[42]  K. Koepsell,et al.  Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies , 2010, Proceedings of the National Academy of Sciences.

[43]  B. Richmond,et al.  Ventromedial and Orbital Prefrontal Neurons Differentially Encode Internally and Externally Driven Motivational Values in Monkeys , 2010, The Journal of Neuroscience.

[44]  Kenway Louie,et al.  Separating Value from Choice: Delay Discounting Activity in the Lateral Intraparietal Area , 2010, The Journal of Neuroscience.

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

[46]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[47]  N. Filippini,et al.  Distinct patterns of brain activity in young carriers of the APOE e4 allele , 2009, NeuroImage.

[48]  Jonathan D. Wallis,et al.  Neurons in the Frontal Lobe Encode the Value of Multiple Decision Variables , 2009, Journal of Cognitive Neuroscience.

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

[50]  P. Matthews,et al.  Distinct patterns of brain activity in young carriers of the APOE e4 allele , 2009, NeuroImage.

[51]  Timothy Edward John Behrens,et al.  Effort-Based Cost–Benefit Valuation and the Human Brain , 2009, The Journal of Neuroscience.

[52]  Timothy E. J. Behrens,et al.  Frontal Cortex Subregions Play Distinct Roles in Choices between Actions and Stimuli , 2008, The Journal of Neuroscience.

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

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

[55]  Byron M. Yu,et al.  Techniques for extracting single-trial activity patterns from large-scale neural recordings , 2007, Current Opinion in Neurobiology.

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

[57]  Paul Cisek,et al.  Preparing for speed. Focus on "Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach". , 2006, Journal of neurophysiology.

[58]  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.

[59]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

[60]  J. O'Doherty,et al.  The Role of the Ventromedial Prefrontal Cortex in Abstract State-Based Inference during Decision Making in Humans , 2006, The Journal of Neuroscience.

[61]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[62]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[63]  Stephen D. Mayhew,et al.  Automated single-trial measurement of amplitude and latency of laser-evoked potentials (LEPs) using multiple linear regression , 2006, Clinical Neurophysiology.

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

[65]  Mark W. Woolrich,et al.  Constrained linear basis sets for HRF modelling using Variational Bayes , 2004, NeuroImage.

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

[67]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[68]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[69]  Jeffrey N. Rouder,et al.  Modeling Response Times for Two-Choice Decisions , 1998 .

[70]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

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

[72]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[73]  Colin Camerer,et al.  Neuroeconomics: decision making and the brain , 2008 .