Neurons in Anterior Cingulate Cortex Multiplex Information about Reward and Action

The dorsal anterior cingulate cortex (dACC) is thought to play a critical role in forming associations between rewards and actions. Currently available physiological data, however, remain inconclusive regarding the question of whether dACC neurons carry information linking particular actions to reward or, instead, encode abstract reward information independent of specific actions. Here we show that firing rates of a majority of dACC neurons in a population studied in an eight-option variably rewarded choice task were sensitive to both saccade direction and reward value. Furthermore, the influences of reward and saccade direction on neuronal activity were approximately equal in magnitude over the range of rewards tested and were statistically independent. Our results indicate that dACC neurons multiplex information about both reward and action, endorsing the idea that this area links motivational outcomes to behavior and undermining the notion that its neurons solely contribute to reward processing in the abstract.

[1]  Theodore H. Poister,et al.  Performance monitoring , 1996 .

[2]  R. Oades,et al.  Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity , 1987, Brain Research Reviews.

[3]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[4]  M. Inase,et al.  Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements. , 1991, Journal of neurophysiology.

[5]  J. Schall,et al.  Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. , 1991, Journal of neurophysiology.

[6]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[7]  Jeffrey D. Schall,et al.  Neural basis of saccade target selection in frontal eye field during visual search , 1993, Nature.

[8]  C. Asanuma,et al.  Neurobiology of Cingulate Cortex and Limbic Thalamus edited by B. A. Vogt and M. Gabriel, Birkha¨user, 1993. $199.00 (639 pages) ISBN 0 8176 3568 8 , 1994, Trends in Neurosciences.

[9]  P. Gaspar,et al.  D1 and D2 Receptor Gene Expression in the Rat Frontal Cortex: Cellular Localization in Different Classes of Efferent Neurons , 1995, The European journal of neuroscience.

[10]  M. Goldberg,et al.  Single neurons in posterior cingulate cortex of behaving macaque: eye movement signals. , 1996, Journal of neurophysiology.

[11]  Alan C. Evans,et al.  Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. , 1996, Cerebral cortex.

[12]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

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

[14]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[15]  J. Hollerman,et al.  Reward prediction in primate basal ganglia and frontal cortex , 1998, Neuropharmacology.

[16]  Paul W. Glimcher,et al.  Response fields of intraparietal neurons quantified with multiple saccadic targets , 1998, Experimental Brain Research.

[17]  A. Turken,et al.  Response selection in the human anterior cingulate cortex , 1999, Nature Neuroscience.

[18]  J. Schall,et al.  Performance monitoring by the supplementary eye ® eld , 2000 .

[19]  E. Procyk,et al.  Anterior cingulate activity during routine and non-routine sequential behaviors in macaques , 2000, Nature Neuroscience.

[20]  T. Paus.  Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[21]  O. Hikosaka,et al.  A neural correlate of response bias in monkey caudate nucleus , 2002, Nature.

[22]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[23]  J. Gold,et al.  Banburismus and the Brain Decoding the Relationship between Sensory Stimuli, Decisions, and Reward , 2002, Neuron.

[24]  B. Richmond,et al.  Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy , 2002, Science.

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

[26]  Frans W Cornelissen,et al.  The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[27]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

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

[29]  Matthew F S Rushworth,et al.  Functional Specialization within Medial Frontal Cortex of the Anterior Cingulate for Evaluating Effort-Related Decisions , 2003, The Journal of Neuroscience.

[30]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

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

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

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

[34]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

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

[36]  Shintaro Funahashi,et al.  Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. I. Cue-, delay-, and response-period activity. , 2004, Journal of neurophysiology.

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

[38]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[39]  Michael L Platt,et al.  Visual and saccade-related activity in macaque posterior cingulate cortex. , 2004, Journal of neurophysiology.

[40]  E. Procyk,et al.  Anterior cingulate error‐related activity is modulated by predicted reward , 2005, The European journal of neuroscience.

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

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

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

[44]  M. Roesch,et al.  Encoding of Time-Discounted Rewards in Orbitofrontal Cortex Is Independent of Value Representation , 2006, Neuron.

[45]  M. Walton,et al.  A Role for the Macaque Anterior Cingulate Gyrus in Social Valuation , 2006, Science.

[46]  Michael L Platt,et al.  Allocentric Spatial Referencing of Neuronal Activity in Macaque Posterior Cingulate Cortex , 2006, The Journal of Neuroscience.

[47]  W. Schultz.  Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

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

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

[50]  H. Seo,et al.  Temporal Filtering of Reward Signals in the Dorsal Anterior Cingulate Cortex during a Mixed-Strategy Game , 2007, The Journal of Neuroscience.

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

[52]  Daeyeol Lee,et al.  Functional Specialization of the Primate Frontal Cortex during Decision Making , 2007, The Journal of Neuroscience.

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

[54]  C. Padoa-Schioppa,et al.  The representation of economic value in the orbitofrontal cortex is invariant for changes of menu , 2008, Nature Neuroscience.

[55]  Benjamin Y. Hayden,et al.  Posterior Cingulate Cortex Mediates Outcome-Contingent Allocation of Behavior , 2008, Neuron.

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

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

[58]  John M. Pearson,et al.  Fictive Reward Signals in the Anterior Cingulate Cortex , 2009, Science.

[59]  S. Kennerley,et al.  Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables , 2009, The European journal of neuroscience.

[60]  Aldo Genovesio,et al.  Monkey Orbitofrontal Cortex Encodes Response Choices Near Feedback Time , 2009, The Journal of Neuroscience.

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

[62]  S. Kennerley,et al.  Encoding of reward and space during a working memory task in the orbitofrontal cortex and anterior cingulate sulcus. , 2009, Journal of neurophysiology.

[63]  J. Wallis,et al.  Dynamic Encoding of Responses and Outcomes by Neurons in Medial Prefrontal Cortex , 2009, The Journal of Neuroscience.