The Contribution of Orbitofrontal Cortex to Action Selection

Abstract:  A number of recent findings suggest that the orbitofrontal cortex (OFC) influences action selection by providing information about the incentive value of behavioral goals or outcomes. However, much of this evidence has been derived from experiments using Pavlovian conditioning preparations of one form or another, making it difficult to determine whether the OFC is selectively involved in stimulus–outcome learning or whether it plays a more general role in processing reward value. Although many theorists have argued that these are fundamentally similar processes (i.e., that stimulus‐reward learning provides the basis for choosing between actions based on anticipated reward value), several behavioral findings indicate that they are, in fact, dissociable. We have recently investigated the role of the OFC in the control of free operant lever pressing using tests that independently target the effect of stimulus–outcome learning and outcome devaluation on performance. We found that OFC lesions disrupted the tendency of Pavlovian cues to facilitate instrumental performance but left intact the suppressive effects of outcome devaluation. Rather than processing goal value, therefore, we hypothesize that the contribution of the OFC to goal‐directed action is limited to encoding predictive stimulus–outcome relationships that can bias instrumental response selection.

[1]  W. Estes Discriminative conditioning. I. A discriminative property of conditioned anticipation. , 1943 .

[2]  L. S. Kogan Review of Principles of Behavior. , 1943 .

[3]  B. Skinner,et al.  Principles of Behavior , 1944 .

[4]  R. Rescorla,et al.  Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. , 1967, Psychological review.

[5]  R. Bolles Reinforcement, expectancy, and learning. , 1972 .

[6]  C. N. Uhl Response elimination in rats with schedules of omission training, including yoked and response-independent reinforcement comparisons , 1974 .

[7]  É. Asratyan Conditional reflex theory and motivational behavior. , 1974, Acta neurobiologiae experimentalis.

[8]  Asratyan Ea Conditional reflex theory and motivational behavior. , 1974 .

[9]  J. Price,et al.  Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat , 1977, The Journal of comparative neurology.

[10]  P. Holland,et al.  Differential effects of two ways of devaluing the unconditioned stimulus after Pavlovian appetitive conditioning. , 1979, Journal of experimental psychology. Animal behavior processes.

[11]  P. Holland,et al.  Differential effects of omission contingencies on various components of Pavlovian appetitive conditioned responding in rats. , 1979, Journal of experimental psychology. Animal behavior processes.

[12]  J. Ayres,et al.  Stimulus-reinforcer and response-reinforcer relations in the control of conditioned appetitive headpoking (goal tracking) in rats. , 1979 .

[13]  L. J. Hammond The effect of contingency upon the appetitive conditioning of free-operant behavior. , 1980, Journal of the experimental analysis of behavior.

[14]  Christopher D. Adams,et al.  Instrumental Responding following Reinforcer Devaluation , 1981 .

[15]  J. Bruce Overmier,et al.  Pavlovian conditioned stimulus effects upon instrumental choice behavior are reinforcer specific , 1983 .

[16]  R. Rescorla,et al.  Postconditioning devaluation of a reinforcer affects instrumental responding. , 1985 .

[17]  R. Bolles,et al.  Differential outcome effect using a biologically neutral outcome difference. , 1986 .

[18]  R. Rescorla,et al.  Associations between the discriminative stimulus and the reinforcer in instrumental learning. , 1988 .

[19]  Effect of reinforcer devaluation on discriminative control of instrumental behavior. , 1990, Journal of experimental psychology. Animal behavior processes.

[20]  Robert A. Rescorla,et al.  Effect of reinforcer devaluation on discriminative control of instrumental behavior. , 1990, Journal of experimental psychology. Animal behavior processes.

[21]  H. Kita,et al.  Amygdaloid projections to the frontal cortex and the striatum in the rat , 1990, The Journal of comparative neurology.

[22]  A. McDonald,et al.  Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat , 1991, Neuroscience.

[23]  P. Durlach,et al.  The Effect of Intertrial Food Presentations on Anticipatory Goal-Tracking in the Rat , 1993, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[24]  B. Balleine,et al.  Actions and responses: The dual psychology of behaviour. , 1993 .

[25]  R. Rescorla Transfer of instrumental control mediated by a devalued outcome , 1994 .

[26]  R. Colwill,et al.  Encoding of the unconditioned stimulus in Pavlovian conditioning , 1994 .

[27]  A. Delamater Outcome-selective effects of intertrial reinforcement in a Pavlovian appetitive conditioning paradigm with rats , 1995 .

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

[29]  F. Mascagni,et al.  Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat , 1996, Neuroscience.

[30]  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.

[31]  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.

[32]  A. Dickinson,et al.  Omission Learning after Instrumental Pretraining , 1998 .

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

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

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

[36]  H. Eichenbaum,et al.  Crossmodal Associative Memory Representations in Rodent Orbitofrontal Cortex , 1999, Neuron.

[37]  E T Rolls,et al.  Responses to the Sensory Properties of Fat of Neurons in the Primate Orbitofrontal Cortex , 1999, The Journal of Neuroscience.

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

[39]  R. Rescorla Learning about qualitatively different outcomes during a blocking procedure , 1999 .

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

[41]  J. Hollerman,et al.  Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior. , 2000, Progress in brain research.

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

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

[44]  G. Hall,et al.  Lesions of the Basolateral Amygdala Disrupt Selective Aspects of Reinforcer Representation in Rats , 2001, The Journal of Neuroscience.

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

[46]  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.

[47]  B. Balleine,et al.  The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning , 2003, The Journal of Neuroscience.

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

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

[50]  P. Holland Relations between Pavlovian-instrumental transfer and reinforcer devaluation. , 2004, Journal of experimental psychology. Animal behavior processes.

[51]  Alicia Izquierdo,et al.  Combined unilateral lesions of the amygdala and orbital prefrontal cortex impair affective processing in rhesus monkeys. , 2004, Journal of neurophysiology.

[52]  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.

[53]  P. Holland,et al.  Amygdala–frontal interactions and reward expectancy , 2004, Current Opinion in Neurobiology.

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

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

[56]  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.

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

[58]  B. Balleine,et al.  Double Dissociation of Basolateral and Central Amygdala Lesions on the General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer , 2005, The Journal of Neuroscience.

[59]  B. Balleine Neural bases of food-seeking: Affect, arousal and reward in corticostriatolimbic circuits , 2005, Physiology & Behavior.

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

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

[62]  A. Roberts,et al.  Primate orbitofrontal cortex and adaptive behaviour , 2006, Trends in Cognitive Sciences.

[63]  B. Balleine,et al.  Parallel incentive processing: an integrated view of amygdala function , 2006, Trends in Neurosciences.

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

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

[66]  B. Balleine,et al.  Action Selection and Initiation in Instrumental Conditioning , 2007 .