Multivariate Neural Representations of Value during Reward Anticipation and Consummation in the Human Orbitofrontal Cortex

The role of the orbitofrontal cortex (OFC) in value processing is a focus of research. Conventional imaging analysis, where smoothing and averaging are employed, may not be sufficiently sensitive in studying the OFC, which has heterogeneous anatomical structures and functions. In this study, we employed representational similarity analysis (RSA) to reveal the multi-voxel fMRI patterns in the OFC associated with value processing during the anticipatory and the consummatory phases. We found that multi-voxel activation patterns in the OFC encoded magnitude and partial valence information (win vs. loss) but not outcome (favourable vs. unfavourable) during reward consummation. Furthermore, the lateral OFC rather than the medial OFC encoded loss information. Also, we found that OFC encoded values in a similar way to the ventral striatum (VS) or the anterior insula (AI) during reward anticipation regardless of motivated response and to the medial prefrontal cortex (MPFC) and the VS in reward consummation. In contrast, univariate analysis did not show changes of activation in the OFC. These findings suggest an important role of the OFC in value processing during reward anticipation and consummation.

[1]  M. Kringelbach.  The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[2]  A. Rangel,et al.  Dissociating valuation and saliency signals during decision-making. , 2011, Cerebral cortex.

[3]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Soyoung Q. Park,et al.  The neural code of reward anticipation in human orbitofrontal cortex , 2010, Proceedings of the National Academy of Sciences.

[5]  Li Su,et al.  A Toolbox for Representational Similarity Analysis , 2014, PLoS Comput. Biol..

[6]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[7]  Timothy E. J. Behrens,et al.  Review Frontal Cortex and Reward-guided Learning and Decision-making Figure 1. Frontal Brain Regions in the Macaque Involved in Reward-guided Learning and Decision-making Finer Grained Anatomical Divisions with Frontal Cortical Systems for Reward-guided Behavior , 2022 .

[8]  M. Baulac,et al.  Functional anatomy of the insula: new insights from imaging , 2003, Surgical and Radiologic Anatomy.

[9]  E. Rolls,et al.  Different representations of pleasant and unpleasant odours in the human brain , 2003, The European journal of neuroscience.

[10]  E. Rolls.  The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[11]  J. Dreher,et al.  The Architecture of Reward Value Coding in the Human Orbitofrontal Cortex , 2010, The Journal of Neuroscience.

[12]  Michael G. Hardin,et al.  The influence of context valence in the neural coding of monetary outcomes , 2009, NeuroImage.

[13]  P. Falkai,et al.  The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude – An activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing , 2012, Neuropsychologia.

[14]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[15]  E. Rolls.  The functions of the orbitofrontal cortex , 1999, Brain and Cognition.

[16]  J. Dreher,et al.  The medial orbitofrontal cortex encodes a general unsigned value signal during anticipation of both appetitive and aversive events , 2015, Cortex.

[17]  Cyriel M A Pennartz,et al.  Neural coding of reward magnitude in the orbitofrontal cortex of the rat during a five-odor olfactory discrimination task. , 2007, Learning & memory.

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

[19]  Brian Knutson,et al.  Valence and salience contribute to nucleus accumbens activation , 2008, NeuroImage.

[20]  J. Haynes,et al.  Neural Responses to Unattended Products Predict Later Consumer Choices , 2010, The Journal of Neuroscience.

[21]  Luke J. Chang,et al.  Connectivity-Based Parcellation of the Human Orbitofrontal Cortex , 2012, The Journal of Neuroscience.

[22]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[23]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[24]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[25]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[26]  John-Dylan Haynes,et al.  Disentangling neural representations of value and salience in the human brain , 2014, Proceedings of the National Academy of Sciences.

[27]  Brian Knutson,et al.  Anticipatory affect: neural correlates and consequences for choice , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  B. Hayden,et al.  Distinct Value Signals in Anterior and Posterior Ventromedial Prefrontal Cortex , 2010, The Journal of Neuroscience.

[29]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[30]  Radoslaw Martin Cichy,et al.  Resolving human object recognition in space and time , 2014, Nature Neuroscience.

[31]  Johan D. Carlin,et al.  A Head View-Invariant Representation of Gaze Direction in Anterior Superior Temporal Sulcus , 2011, Current Biology.

[32]  Jin Fan,et al.  Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies , 2011, Neuroscience & Biobehavioral Reviews.

[33]  H. Critchley,et al.  Neural correlates of processing valence and arousal in affective words. , 2006, Cerebral cortex.

[34]  R. Elliott,et al.  Hedonic and informational functions of the human orbitofrontal cortex. , 2010, Cerebral cortex.

[35]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[36]  C. Pennartz,et al.  Population Coding of Reward Magnitude in the Orbitofrontal Cortex of the Rat , 2008, The Journal of Neuroscience.

[37]  Vivian V. Valentin,et al.  Determining the Neural Substrates of Goal-Directed Learning in the Human Brain , 2007, The Journal of Neuroscience.

[38]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[39]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[40]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

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

[42]  S. Krach,et al.  Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. , 2009, Social cognitive and affective neuroscience.

[43]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[44]  Monique Ernst,et al.  Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents , 2013, NeuroImage.

[45]  C. Pennartz,et al.  Single-Cell and Population Coding of Expected Reward Probability in the Orbitofrontal Cortex of the Rat , 2009, The Journal of Neuroscience.