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      Dissociable roles for lateral orbitofrontal cortex and lateral prefrontal cortex during preference driven reversal learning

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          Abstract

          One of the archetypal task manipulations known to depend on frontal-lobe function is reversal learning, where a dominant response must be overridden due to changes in the contingencies relating stimuli, responses, and environmental feedback. Previous studies have indicated that the lateral prefrontal cortex (LPFC), the lateral orbitofrontal cortex (LOFC), the anterior cingulate cortex (ACC), and the caudate nucleus (CN) all contribute to reversal learning. However, the exact contributions that they make during this cognitively complex task remain poorly defined. Here, using functional magnetic resonance imaging, we examine which of the cognitive processes that contribute to the performance of a reversal best predicts the pattern of activation within distinct sub-regions of the frontal lobes. We demonstrate that during reversal learning the LOFC is particularly sensitive to the implementation of the reversal, whereas the LPFC is recruited more generally during attentional control. By contrast, the ACC and CN respond when new searches are initiated regardless of whether the previous response is available, whilst medial orbitofrontal cortex (MOFC) activity is correlated with the positive affect of feedback. These results accord well with the hypothesis that distinct components of adaptable behaviour are supported by anatomically distinct components of the executive system.

          Highlights

          ► We model fMRI data at distinct stages of a reward driven reversal learning task. ► Lateral orbitofrontal cortex responds particularly strongly at the point of reversal. ► Lateral prefrontal cortex shows a similar response during other switches. ► Medial orbitofrontal cortex activity correlates with the rewarding value of feedback. ► Anterior cingulate cortex and caudate respond whenever new searches are initiated.

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          Most cited references45

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          Cognitive and emotional influences in anterior cingulate cortex.

          Bush, Luu, Posner (2000)
          Anterior cingulate cortex (ACC) is a part of the brain's limbic system. Classically, this region has been related to affect, on the basis of lesion studies in humans and in animals. In the late 1980s, neuroimaging research indicated that ACC was active in many studies of cognition. The findings from EEG studies of a focal area of negativity in scalp electrodes following an error response led to the idea that ACC might be the brain's error detection and correction device. In this article, these various findings are reviewed in relation to the idea that ACC is a part of a circuit involved in a form of attention that serves to regulate both cognitive and emotional processing. Neuroimaging studies showing that separate areas of ACC are involved in cognition and emotion are discussed and related to results showing that the error negativity is influenced by affect and motivation. In addition, the development of the emotional and cognitive roles of ACC are discussed, and how the success of this regulation in controlling responses might be correlated with cingulate size. Finally, some theories are considered about how the different subdivisions of ACC might interact with other cortical structures as a part of the circuits involved in the regulation of mental and emotional activity.
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            Abstract reward and punishment representations in the human orbitofrontal cortex.

            The orbitofrontal cortex (OFC) is implicated in emotion and emotion-related learning. Using event-related functional magnetic resonance imaging (fMRI), we measured brain activation in human subjects doing an emotion-related visual reversal-learning task in which choice of the correct stimulus led to a probabilistically determined 'monetary' reward and choice of the incorrect stimulus led to a monetary loss. Distinct areas of the OFC were activated by monetary rewards and punishments. Moreover, in these areas, we found a correlation between the magnitude of the brain activation and the magnitude of the rewards and punishments received. These findings indicate that one emotional involvement of the human orbitofrontal cortex is its representation of the magnitudes of abstract rewards and punishments, such as receiving or losing money.
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              Dissociation in prefrontal cortex of affective and attentional shifts.

              The prefrontal cortex is implicated in such human characteristics as volition, planning, abstract reasoning and affect. Frontal-lobe damage can cause disinhibition such that the behaviour of a subject is guided by previously acquired responses that are inappropriate to the current situation. Here we demonstrate that disinhibition, or a loss of inhibitory control, can be selective for particular cognitive functions and that different regions of the prefrontal cortex provide inhibitory control in different aspects of cognitive processing. Thus, whereas damage to the lateral prefrontal cortex (Brodmann's area 9) in monkeys causes a loss of inhibitory control in attentional selection, damage to the orbito-frontal cortex in monkeys causes a loss of inhibitory control in 'affective' processing, thereby impairing the ability to alter behaviour in response to fluctuations in the emotional significance of stimuli. These findings not only support the view that the prefrontal cortex has multiple functions, but also provide evidence for the distribution of different cognitive functions within specific regions of prefrontal cortex.
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                Author and article information

                Journal
                Neuroimage
                Neuroimage
                Neuroimage
                Academic Press
                1053-8119
                1095-9572
                15 February 2012
                15 February 2012
                : 59-20
                : 4
                : 4102-4112
                Affiliations
                [a ]Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3DY, UK
                [b ]Medical Research Council Cognition and Brain Sciences Unit, Chaucer Road, Cambridge, UK
                [c ]Behavioural and Clinical Neuroscience Institute, Downing Street, University of Cambridge, CB2 3EB, UK
                [d ]Centre for Brain and Mind, University of Western Ontario, London, Ontario, Canada
                Author notes
                [* ]Corresponding author at: Centre for Brain and Mind, University of Western Ontario, London, Ontario, Canada. ahampshi@ 123456uwo.ca
                [1]

                AMC and AH contributed equally to this work.

                Article
                YNIMG8851
                10.1016/j.neuroimage.2011.10.072
                3391678
                22075266
                f41aa65b-a740-4545-9264-54ba75fb48ce
                © 2012 Elsevier Inc.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 8 August 2011
                : 5 October 2011
                : 17 October 2011
                Categories
                Article

                Neurosciences
                reversal learning,frontal lobe,fmri,attention,executive function
                Neurosciences
                reversal learning, frontal lobe, fmri, attention, executive function

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