Adaptive coding of action values in the human rostral cingulate zone

Correctly selecting appropriate actions in an uncertain environment requires gathering experience about the available actions by sampling them over several trials. Recent findings suggest that the human rostral cingulate zone (RCZ) is important for the integration of extended action–outcome associations across multiple trials and in coding the subjective value of each action. During functional magnetic resonance imaging, healthy volunteers performed two versions of a probabilistic reversal learning task with high (HP) or low (LP) reward probabilities that required them to integrate action–outcome relations over lower or higher numbers of trials, respectively. In the HP session, subjects needed fewer trials to adjust their behavior in response to a reversal of response–reward contingencies. Similarly, the learning rate derived from a reinforcement learning model was higher in the HP condition. This was accompanied by a stronger response of the RCZ to negative feedback upon reversals in the HP condition. Furthermore, RCZ activity related to negative reward prediction errors varied as a function of the learning rate, which determines to what extent the prediction error is used to update action values. These data show that RCZ responses vary as a function of the information content provided by the environment. The more likely a negative event indicates the need for behavioral adaptations, the more prominent is the response of the RCZ. Thus, both the window of trials over which reinforcement information is integrated and adjustment of action values in the RCZ covary with the stochastics of the environment.

[1]  H. Barbas,et al.  Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey , 1990, The Journal of comparative neurology.

[2]  G. V. Van Hoesen,et al.  Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: Evidence for somatotopy in areas 24c and 23c , 1992, The Journal of comparative neurology.

[3]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[4]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[7]  Thomas G. Dietterich What is machine learning? , 2020, Archives of Disease in Childhood.

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

[9]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[10]  M. Inase,et al.  Organization of inputs from cingulate motor areas to basal ganglia in macaque monkey , 2001, The European journal of neuroscience.

[11]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

[12]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[13]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[14]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

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

[16]  A. Turken,et al.  Dissociation between conflict detection and error monitoring in the human anterior cingulate cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. Robbins,et al.  Defining the Neural Mechanisms of Probabilistic Reversal Learning Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[18]  Morten L Kringelbach,et al.  Neural correlates of rapid reversal learning in a simple model of human social interaction , 2003, NeuroImage.

[19]  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.

[20]  Samuel M. McClure,et al.  Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum , 2003, Neuron.

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

[22]  Naomi Hasegawa,et al.  Thalamocortical and intracortical connections of monkey cingulate motor areas , 2003, The Journal of comparative neurology.

[23]  Peter Dayan,et al.  Q-learning , 1992, Machine Learning.

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

[25]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

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

[27]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[28]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[29]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

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

[31]  R. E. Passingham,et al.  Prediction error for free monetary reward in the human prefrontal cortex , 2004, NeuroImage.

[32]  J. O'Doherty,et al.  Reward representations and reward-related learning in the human brain: insights from neuroimaging , 2004, Current Opinion in Neurobiology.

[33]  D. Yves von Cramon,et al.  Neuroimaging of Performance Monitoring: Error Detection and Beyond , 2004, Cortex.

[34]  Erratum: Human anterior cingulate neurons and the integration of monetary reward with motor responses , 2005, Nature Neuroscience.

[35]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

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

[37]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

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

[39]  R. James R. Blair,et al.  Neural correlates of response reversal: Considering acquisition , 2007, NeuroImage.

[40]  M. Reuter,et al.  Genetically Determined Differences in Learning from Errors , 2007, Science.

[41]  Michael J. Frank,et al.  Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning , 2007, Proceedings of the National Academy of Sciences.

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

[43]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[44]  Michael X. Cohen,et al.  Dopamine gene predicts the brain's response to dopaminergic drug , 2007, The European journal of neuroscience.

[45]  S. Kapur,et al.  Temporal Difference Modeling of the Blood-Oxygen Level Dependent Response During Aversive Conditioning in Humans: Effects of Dopaminergic Modulation , 2007, Biological Psychiatry.

[46]  D. Pine,et al.  The contribution of ventrolateral and dorsolateral prefrontal cortex to response reversal , 2008, Behavioural Brain Research.

[47]  M. Reuter,et al.  Dopamine DRD2 polymorphism alters reversal learning and associated neural activity , 2009, NeuroImage.