Dynamic Encoding of Responses and Outcomes by Neurons in Medial Prefrontal Cortex

Medial prefrontal cortex (MPFC) and lateral prefrontal cortex (LPFC) both contribute to goal-directed behavior, but their precise role remains unclear. Several lines of evidence suggest that MPFC is more important than LPFC for outcome-guided response selection. To examine this, we trained two subjects to perform a task that required them to monitor the specific outcome associated with a specific response on a trial-by-trial basis. While the subjects performed this task, we recorded the electrical activity of single neurons simultaneously from MPFC and LPFC. There were marked differences in the neuronal properties of these two areas. Neurons encoding the response were present in both areas, but in MPFC, there were also neurons that encoded the outcome. In particular, neurons encoded the subject's intended response and how preferable the received outcome was. Thus, only in MPFC was all the information necessary to solve the task encoded. In addition, largely separate populations of MPFC neurons encoded the response and the outcome. Neurons encoding the outcome were in the anterior parts of MPFC: posterior to the corpus callosum, there was a marked drop in their incidence. Our results suggest differences in the contribution of MPFC and LPFC to action control. MPFC neurons encode the desirability of the outcome produced by a specific response on a trial-by-trial basis. This capability may contribute to several of the functions of MPFC, such as action valuation, error detection, and decision making.

[1]  Dale T. Miller,et al.  Self-serving biases in the attribution of causality: Fact or fiction? , 1975 .

[2]  A. Tversky,et al.  The framing of decisions and the psychology of choice. , 1981, Science.

[3]  M. Petrides Motor conditional associative-learning after selective prefrontal lesions in the monkey , 1982, Behavioural Brain Research.

[4]  R. Passingham,et al.  The role of premotor and parietal cortex in the direction of action , 1982, Brain Research.

[5]  T. Shallice,et al.  Deficits in strategy application following frontal lobe damage in man. , 1991, Brain : a journal of neurology.

[6]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M. Gabriel,et al.  Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Handbook , 1993 .

[8]  P. Strick,et al.  Cingulate Motor Areas , 1993 .

[9]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[10]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[11]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[12]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[13]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[14]  M Petrides,et al.  Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  S. Carmichael,et al.  Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. , 1996, The Journal of comparative neurology.

[16]  Masataka Watanabe Reward expectancy in primate prefrental neurons , 1996, Nature.

[17]  M. Petrides,et al.  Specialized systems for the processing of mnemonic information within the primate frontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  J. Duncan,et al.  Intelligence and the Frontal Lobe: The Organization of Goal-Directed Behavior , 1996, Cognitive Psychology.

[19]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[20]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

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

[22]  B. Balleine,et al.  Goal-directed instrumental action: contingency and incentive learning and their cortical substrates , 1998, Neuropharmacology.

[23]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[24]  P. B. Cipolloni,et al.  Cortical connections of the frontoparietal opercular areas in the Rhesus monkey , 1999, The Journal of comparative neurology.

[25]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[26]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[27]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[28]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[29]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[30]  D. Gaffan,et al.  Interaction of Inferior Temporal Cortex with Frontal Cortex and Basal Forebrain: Double Dissociation in Strategy Implementation and Associative Learning , 2002, The Journal of Neuroscience.

[31]  K. A. Hadland,et al.  The anterior cingulate and reward-guided selection of actions. , 2003, Journal of neurophysiology.

[32]  D. V. von Cramon,et al.  Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[33]  M. Roesch,et al.  Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex. , 2003, Journal of neurophysiology.

[34]  Keiji Tanaka,et al.  Neuronal Correlates of Goal-Based Motor Selection in the Prefrontal Cortex , 2003, Science.

[35]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[36]  E. Miller,et al.  From rule to response: neuronal processes in the premotor and prefrontal cortex. , 2003, Journal of neurophysiology.

[37]  Ziv M. Williams,et al.  Human anterior cingulate neurons and the integration of monetary reward with motor responses , 2004, Nature Neuroscience.

[38]  Clay B. Holroyd,et al.  Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals , 2004, Nature Neuroscience.

[39]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[40]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[41]  D. Barraclough,et al.  Prefrontal cortex and decision making in a mixed-strategy game , 2004, Nature Neuroscience.

[42]  M. Roesch,et al.  Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex , 2004, Science.

[43]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[44]  B. Vogt,et al.  Architecture and neurocytology of monkey cingulate gyrus , 2005, The Journal of comparative neurology.

[45]  J. Tanji,et al.  Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity. , 2005, Journal of neurophysiology.

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

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

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

[49]  E. Procyk,et al.  Reward encoding in the monkey anterior cingulate cortex. , 2006, Cerebral cortex.

[50]  P. Goldman-Rakic,et al.  Modulation of Dorsolateral Prefrontal Delay Activity during Self-Organized Behavior , 2006, The Journal of Neuroscience.

[51]  J. Wallis Orbitofrontal cortex and its contribution to decision-making. , 2007, Annual review of neuroscience.

[52]  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 .

[53]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[54]  Angela J. Yu,et al.  Should I stay or should I go? How the human brain manages the trade-off between exploitation and exploration , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  Keiji Tanaka,et al.  Medial prefrontal cell activity signaling prediction errors of action values , 2007, Nature Neuroscience.

[56]  Robert Desimone,et al.  Top–Down Attentional Deficits in Macaques with Lesions of Lateral Prefrontal Cortex , 2007, The Journal of Neuroscience.

[57]  P. Glimcher,et al.  Action and Outcome Encoding in the Primate Caudate Nucleus , 2007, The Journal of Neuroscience.

[58]  E. Procyk,et al.  Expectations, gains, and losses in the anterior cingulate cortex , 2007, Cognitive, affective & behavioral neuroscience.

[59]  H. Seo,et al.  Dynamic signals related to choices and outcomes in the dorsolateral prefrontal cortex. , 2007, Cerebral cortex.

[60]  David Gaffan,et al.  Dorsolateral prefrontal lesions do not impair tests of scene learning and decision-making that require frontal–temporal interaction , 2008, The European journal of neuroscience.

[61]  L. Fellows,et al.  Dorsal Medial Prefrontal Cortex Plays a Necessary Role in Rapid Error Prediction in Humans , 2008, The Journal of Neuroscience.

[62]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.

[63]  E. Procyk,et al.  Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex , 2008, Neuron.

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

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