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      Functional heterogeneity within the rodent lateral orbitofrontal cortex dissociates outcome devaluation and reversal learning deficits

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          Abstract

          The orbitofrontal cortex (OFC) is critical for updating reward-directed behaviours flexibly when outcomes are devalued or when task contingencies are reversed. Failure to update behaviour in outcome devaluation and reversal learning procedures are considered canonical deficits following OFC lesions in non-human primates and rodents. We examined the generality of these findings in rodents using lesions of the rodent lateral OFC (LO) in instrumental action-outcome and Pavlovian cue-outcome devaluation procedures. LO lesions disrupted outcome devaluation in Pavlovian but not instrumental procedures. Furthermore, although both anterior and posterior LO lesions disrupted Pavlovian outcome devaluation, only posterior LO lesions were found to disrupt reversal learning. Posterior but not anterior LO lesions were also found to disrupt the attribution of motivational value to Pavlovian cues in sign-tracking. These novel dissociable task- and subregion-specific effects suggest a way to reconcile contradictory findings between rodent and non-human primate OFC research.

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          Most cited references69

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          Orbitofrontal cortex as a cognitive map of task space.

          Orbitofrontal cortex (OFC) has long been known to play an important role in decision making. However, the exact nature of that role has remained elusive. Here, we propose a unifying theory of OFC function. We hypothesize that OFC provides an abstraction of currently available information in the form of a labeling of the current task state, which is used for reinforcement learning (RL) elsewhere in the brain. This function is especially critical when task states include unobservable information, for instance, from working memory. We use this framework to explain classic findings in reversal learning, delayed alternation, extinction, and devaluation as well as more recent findings showing the effect of OFC lesions on the firing of dopaminergic neurons in ventral tegmental area (VTA) in rodents performing an RL task. In addition, we generate a number of testable experimental predictions that can distinguish our theory from other accounts of OFC function. Copyright © 2014 Elsevier Inc. All rights reserved.
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            Actions and Habits: The Development of Behavioural Autonomy

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              The orbitofrontal cortex and reward.

              E Rolls (2000)
              The primate orbitofrontal cortex contains the secondary taste cortex, in which the reward value of taste is represented. It also contains the secondary and tertiary olfactory cortical areas, in which information about the identity and also about the reward value of odors is represented. The orbitofrontal cortex also receives information about the sight of objects and faces from the temporal lobe cortical visual areas, and neurons in it learn and reverse the visual stimulus to which they respond when the association of the visual stimulus with a primary reinforcing stimulus (such as a taste reward) is reversed. However, the orbitofrontal cortex is involved in representing negative reinforcers (punishers) too, such as aversive taste, and in rapid stimulus-reinforcement association learning for both positive and negative primary reinforcers. In complementary neuroimaging studies in humans it is being found that areas of the orbitofrontal cortex (and connected subgenual cingulate cortex) are activated by pleasant touch, by painful touch, by rewarding and aversive taste, and by odor. Damage to the orbitofrontal cortex in humans can impair the learning and reversal of stimulus- reinforcement associations, and thus the correction of behavioral responses when these are no longer appropriate because previous reinforcement contingencies change. This evidence thus shows that the orbitofrontal cortex is involved in decoding and representing some primary reinforcers such as taste and touch; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and in controlling and correcting reward-related and punishment-related behavior, and thus in emotion.

                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                25 July 2018
                2018
                : 7
                : e37357
                Affiliations
                [1 ]deptSchool of Psychology The University of New South Wales KensingtonAustralia
                [2 ]deptDepartment of Experimental Psychology University of Oxford OxfordUnited Kingdom
                National Institute on Drug Abuse, National Institutes of Health United States
                Princeton University United States
                National Institute on Drug Abuse, National Institutes of Health United States
                Author information
                http://orcid.org/0000-0003-2635-5638
                Article
                37357
                10.7554/eLife.37357
                6101941
                30044220
                617ed902-c9bf-490a-bec0-dbba09791e41
                © 2018, Panayi et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 07 April 2018
                : 24 July 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000923, Australian Research Council;
                Award ID: DP0989027
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000923, Australian Research Council;
                Award ID: DP120103564
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                The rodent orbitofrontal cortex makes functionally distinct contributions to flexible behavioural control, even within a single putative orbitofrontal subregion, which has important implications for establishing homology between rodent and primate orbitofrontal cortex.

                Life sciences
                orbitofrontal cortex,outcome devaluation,reversal learning,autoshaping,pavlovian learning,outcome identity,rat

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