A new perspective on the role of the orbitofrontal cortex in adaptive behaviour

The orbitofrontal cortex (OFC) is crucial for changing established behaviour in the face of unexpected outcomes. This function has been attributed to the role of the OFC in response inhibition or to the idea that the OFC is a rapidly flexible associative-learning area. However, recent data contradict these accounts, and instead suggest that the OFC is crucial for signalling outcome expectancies. We suggest that this function — signalling of expected outcomes — can also explain the crucial role of the OFC in changing behaviour in the face of unexpected outcomes.

[1]  D. Ferrier.  The Functions of the Brain , 1887, Edinburgh Medical Journal.

[2]  J. R.,et al.  Quantitative analysis , 1892, Nature.

[3]  Charles M. Butter,et al.  Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta , 1969 .

[4]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[5]  J. Fuster.  Prefrontal Cortex , 2018 .

[6]  R. Rescorla.  Pavlovian conditioning. It's not what you think it is. , 1988, The American psychologist.

[7]  R. Rescorla.  Pavlovian conditioning. It's not what you think it is. , 1988 .

[8]  A. Damasio,et al.  The return of Phineas Gage: clues about the brain from the skull of a famous patient. , 1994, Science.

[9]  B. Balleine,et al.  Motivational control of goal-directed action , 1994 .

[10]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[11]  T. Preuss.  Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[12]  H Eichenbaum,et al.  Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. , 1995, Journal of neurophysiology.

[13]  Michael S. Gazzaniga,et al.  On Neural Circuits and Cognition , 1995, Neural Computation.

[14]  E. Rolls,et al.  Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. , 1996, Journal of neurophysiology.

[15]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

[16]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.

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

[18]  E. Rolls,et al.  Orbitofrontal cortex neurons: role in olfactory and visual association learning. , 1996, Journal of neurophysiology.

[19]  E. Murray,et al.  Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys , 1997, The Journal of Neuroscience.

[20]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[21]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[22]  M. Mishkin,et al.  Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys , 1997, Neuropsychologia.

[23]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[24]  J. Hollerman,et al.  Dopamine neurons report an error in the temporal prediction of reward during learning , 1998, Nature Neuroscience.

[25]  G. Schoenbaum,et al.  Orbitofrontal Cortex and Representation of Incentive Value in Associative Learning , 1999, The Journal of Neuroscience.

[26]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[27]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

[28]  E T Rolls,et al.  Sensory‐specific satiety‐related olfactory activation of the human orbitofrontal cortex , 2000, Neuroreport.

[29]  E. Murray,et al.  Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex , 2000, The Journal of Neuroscience.

[30]  B. Knowlton,et al.  Effects of US devaluation on win-stay and win-shift radial maze performance in rats. , 2000, Behavioral neuroscience.

[31]  K. Hikosaka,et al.  Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. , 2000, Cerebral cortex.

[32]  W. Schultz,et al.  Dopamine responses comply with basic assumptions of formal learning theory , 2001, Nature.

[33]  T. Robbins,et al.  Dissociable contributions of the orbitofrontal and lateral prefrontal cortex of the marmoset to performance on a detour reaching task , 2001, The European journal of neuroscience.

[34]  Sham M. Kakade,et al.  Opponent interactions between serotonin and dopamine , 2002, Neural Networks.

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

[36]  Geoffrey Schoenbaum,et al.  Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations , 2002, Neuroreport.

[37]  J. Deakin,et al.  Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement , 2002, Psychopharmacology.

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

[39]  S Kheramin,et al.  Role of the orbital prefrontal cortex in choice between delayed and uncertain reinforcers: a quantitative analysis , 2003, Behavioural Processes.

[40]  G. Schoenbaum,et al.  Encoding Predicted Outcome and Acquired Value in Orbitofrontal Cortex during Cue Sampling Depends upon Input from Basolateral Amygdala , 2003, Neuron.

[41]  Geoffrey Schoenbaum,et al.  Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. , 2003, Learning & memory.

[42]  M. Farah,et al.  Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. , 2003, Brain : a journal of neurology.

[43]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[44]  T. Robbins,et al.  Dissociable Contributions of the Orbitofrontal and Infralimbic Cortex to Pavlovian Autoshaping and Discrimination Reversal Learning: Further Evidence for the Functional Heterogeneity of the Rodent Frontal Cortex , 2003, The Journal of Neuroscience.

[45]  V. Brown,et al.  Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat , 2003, Behavioural Brain Research.

[46]  E. Miller,et al.  Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task , 2003, The European journal of neuroscience.

[47]  B. Balleine,et al.  The role of prelimbic cortex in instrumental conditioning , 2003, Behavioural Brain Research.

[48]  B. Everitt,et al.  Lesions of the Orbitofrontal but not Medial Prefrontal Cortex Disrupt Conditioned Reinforcement in Primates , 2003, The Journal of Neuroscience.

[49]  T. Otto,et al.  Neural substrates of olfactory discrimination learning with auditory secondary reinforcement. I. Contributions of the basolateral amygdaloid complex and orbitofrontal cortex , 2003, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[50]  Geoffrey Schoenbaum,et al.  Different Roles for Orbitofrontal Cortex and Basolateral Amygdala in a Reinforcer Devaluation Task , 2003, The Journal of Neuroscience.

[51]  B. Everitt,et al.  The Effects of Selective Orbitofrontal Cortex Lesions on the Acquisition and Performance of Cue‐Controlled Cocaine Seeking in Rats , 2003, Annals of the New York Academy of Sciences.

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

[53]  Masataka Watanabe,et al.  Long‐ and short‐range reward expectancy in the primate orbitofrontal cortex , 2004, The European journal of neuroscience.

[54]  E. Murray,et al.  Bilateral Orbital Prefrontal Cortex Lesions in Rhesus Monkeys Disrupt Choices Guided by Both Reward Value and Reward Contingency , 2004, The Journal of Neuroscience.

[55]  B. Balleine,et al.  Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning , 2004, The European journal of neuroscience.

[56]  E. Rolls,et al.  Reward-related Reversal Learning after Surgical Excisions in Orbito-frontal or Dorsolateral Prefrontal Cortex in Humans , 2004, Journal of Cognitive Neuroscience.

[57]  S. Thorpe,et al.  The orbitofrontal cortex: Neuronal activity in the behaving monkey , 2004, Experimental Brain Research.

[58]  A. Sirigu,et al.  The Involvement of the Orbitofrontal Cortex in the Experience of Regret , 2004, Science.

[59]  T. Robbins,et al.  Contrasting Roles of Basolateral Amygdala and Orbitofrontal Cortex in Impulsive Choice , 2004, The Journal of Neuroscience.

[60]  B. Richmond,et al.  Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules , 2005, The Journal of Neuroscience.

[61]  W. Pan,et al.  Dopamine Cells Respond to Predicted Events during Classical Conditioning: Evidence for Eligibility Traces in the Reward-Learning Network , 2005, The Journal of Neuroscience.

[62]  Geoffrey Schoenbaum,et al.  Rapid Associative Encoding in Basolateral Amygdala Depends on Connections with Orbitofrontal Cortex , 2005, Neuron.

[63]  Michela Gallagher,et al.  Lesions of Orbitofrontal Cortex Impair Rats' Differential Outcome Expectancy Learning But Not Conditioned Stimulus-Potentiated Feeding , 2005, The Journal of Neuroscience.

[64]  M. Roesch,et al.  Orbitofrontal Cortex, Associative Learning, and Expectancies , 2005, Neuron.

[65]  Karen Gale,et al.  GABAA-Mediated Inhibition of Basolateral Amygdala Blocks Reward Devaluation in Macaques , 2005, The Journal of Neuroscience.

[66]  P. Glimcher,et al.  Midbrain Dopamine Neurons Encode a Quantitative Reward Prediction Error Signal , 2005, Neuron.

[67]  P. Holland,et al.  Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task. , 2005, Behavioral neuroscience.

[68]  A A M Wilde,et al.  It's Not What You Think , 2017 .

[69]  B. Balleine,et al.  Blockade of NMDA receptors in the dorsomedial striatum prevents action–outcome learning in instrumental conditioning , 2005, The European journal of neuroscience.

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

[71]  M. Roesch,et al.  Abnormal associative encoding in orbitofrontal neurons in cocaine‐experienced rats during decision‐making , 2006, The European journal of neuroscience.

[72]  M. Quirk,et al.  Representation of Spatial Goals in Rat Orbitofrontal Cortex , 2006, Neuron.

[73]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[74]  Sidney A. Simon,et al.  Neural Ensemble Coding of Satiety States , 2006, Neuron.

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

[76]  Elisabeth A. Murray,et al.  Behavioral/systems/cognitive Selective Bilateral Amygdala Lesions in Rhesus Monkeys Fail to Disrupt Object Reversal Learning , 2022 .

[77]  O. Hikosaka,et al.  Lateral habenula as a source of negative reward signals in dopamine neurons , 2007, Nature.

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

[79]  Joseph J. Paton,et al.  Expectation Modulates Neural Responses to Pleasant and Aversive Stimuli in Primate Amygdala , 2007, Neuron.

[80]  B. Balleine,et al.  Orbitofrontal Cortex Mediates Outcome Encoding in Pavlovian But Not Instrumental Conditioning , 2007, The Journal of Neuroscience.

[81]  M. Roesch,et al.  Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards , 2007, Nature Neuroscience.

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

[83]  J. Kralik,et al.  Rhesus monkeys with orbital prefrontal cortex lesions can learn to inhibit prepotent responses in the reversed reward contingency task. , 2006, Cerebral cortex.

[84]  Philip G. F. Browning,et al.  Neurotoxic Lesions of the Medial Mediodorsal Nucleus of the Thalamus Disrupt Reinforcer Devaluation Effects in Rhesus Monkeys , 2007, The Journal of Neuroscience.

[85]  J. Bachevalier,et al.  The effects of selective amygdala, orbital frontal cortex or hippocampal formation lesions on reward assessment in nonhuman primates , 2007, The European journal of neuroscience.

[86]  G. Schoenbaum,et al.  Basolateral Amygdala Lesions Abolish Orbitofrontal-Dependent Reversal Impairments , 2007, Neuron.

[87]  Geoffrey Schoenbaum,et al.  Double Dissociation of the Effects of Medial and Orbital Prefrontal Cortical Lesions on Attentional and Affective Shifts in Mice , 2008, The Journal of Neuroscience.

[88]  Geoffrey Schoenbaum,et al.  The role of the orbitofrontal cortex in the pursuit of happiness and more specific rewards , 2008, Nature.

[89]  Y. Niv,et al.  Dialogues on prediction errors , 2008, Trends in Cognitive Sciences.

[90]  T. Robbins,et al.  Stop-signal reaction-time task performance: role of prefrontal cortex and subthalamic nucleus. , 2008, Cerebral cortex.

[91]  J. Bachevalier,et al.  Behavioral/systems/cognitive Selective Aspiration or Neurotoxic Lesions of Orbital Frontal Areas 11 and 13 Spared Monkeys' Performance on the Object Discrimination Reversal Task , 2022 .

[92]  M. Roesch,et al.  The Orbitofrontal Cortex and Ventral Tegmental Area Are Necessary for Learning from Unexpected Outcomes , 2009, Neuron.