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      The anterior insula bidirectionally modulates cost‐benefit decision‐making on a rodent gambling task

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          Abstract

          Deficits in cost‐benefit decision‐making, as assessed in the Iowa Gambling Task ( IGT), are commonly observed in neuropsychiatric disorders such as addiction. There is considerable variation in the maximization of rewards on such tasks, both in the general population and in rodent models, suggesting individual differences in decision‐making may represent a key endophenotype for vulnerability to neuropsychiatric disorders. Increasing evidence suggests that the insular cortex, which is involved in interoception and emotional processes in humans, may be a key neural locus in the control of decision‐making processes. However, the extent to which the insula contributes to individual differences in cost‐benefit decision‐making remains unknown. Using male Sprague Dawley rats, we first assessed individual differences in the performance over the course of a single session on a rodent analogue of the IGT ( rGT). Rats were matched for their ability to maximize reward and received bilateral excitotoxic or sham lesions of the anterior insula cortex ( AIC). Animals were subsequently challenged on a second rGT session with altered contingencies. Finally, animals were also assessed for instrumental conditioning and reversal learning. AIC lesions produced bidirectional alterations on rGT performance; rats that had performed optimally prior to surgery subsequently showed impairments, and animals that had performed poorly showed improvements in comparison with sham‐operated controls. These bidirectional effects were not attributable to alterations in behavioural flexibility or in motivation. These data suggest that the recruitment of the AIC during decision‐making may be state‐dependent and help guide response selection towards subjectively favourable options.

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          Most cited references36

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          Deciding advantageously before knowing the advantageous strategy.

          Deciding advantageously in a complex situation is thought to require overt reasoning on declarative knowledge, namely, on facts pertaining to premises, options for action, and outcomes of actions that embody the pertinent previous experience. An alternative possibility was investigated: that overt reasoning is preceded by a nonconscious biasing step that uses neural systems other than those that support declarative knowledge. Normal participants and patients with prefrontal damage and decision-making defects performed a gambling task in which behavioral, psychophysiological, and self-account measures were obtained in parallel. Normals began to choose advantageously before they realized which strategy worked best, whereas prefrontal patients continued to choose disadvantageously even after they knew the correct strategy. Moreover, normals began to generate anticipatory skin conductance responses (SCRs) whenever they pondered a choice that turned out to be risky, before they knew explicitly that it was a risky choice, whereas patients never developed anticipatory SCRs, although some eventually realized which choices were risky. The results suggest that, in normal individuals, nonconscious biases guide behavior before conscious knowledge does. Without the help of such biases, overt knowledge may be insufficient to ensure advantageous behavior.
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            Circuitry and functional aspects of the insular lobe in primates including humans.

            The progress made in understanding the insula in the decade following an earlier review (Augustine, Neurol. Res., 7 (1985) 2-10) is examined in this review. In these ten years, connections have been described between the insula and the orbital cortex, frontal operculum, lateral premotor cortex, ventral granular cortex, and medial area 6 in the frontal lobe. Insular connections between the second somatosensory area and retroinsular area of the parietal lobe have been documented. The insula was found to connect with the temporal pole and the superior temporal sulcus of the temporal lobe. It has an abundance of local intrainsular connections and projections to subdivisions of the cingulate gyrus. The insula has connections with the lateral, lateral basal, central, cortical and medial amygdaloid nuclei. It also connects with nonamygdaloid areas such as the perirhinal cortex, entorhinal, and periamygdaloid cortex. The thalamic taste area, the parvicellular part of the ventral posteromedial nucleus, projects fibers to the ipsilateral insular-opercular cortex. In the past decade, confirmation has been given to the insula as a visceral sensory area, visceral motor area, motor association area, vestibular area, and language area. Recent studies have expanded the role of the insula as a somatosensory area, emphasizing its multifaceted, sensory role. The idea of the insula as limbic integration cortex has been affirmed and its role in Alzheimer's disease suggested.
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              Insensitivity to future consequences following damage to human prefrontal cortex.

              Following damage to the ventromedial prefrontal cortex, humans develop a defect in real-life decision-making, which contrasts with otherwise normal intellectual functions. Currently, there is no neuropsychological probe to detect in the laboratory, and the cognitive and neural mechanisms responsible for this defect have resisted explanation. Here, using a novel task which simulates real-life decision-making in the way it factors uncertainty of premises and outcomes, as well as reward and punishment, we find that prefrontal patients, unlike controls, are oblivious to the future consequences of their actions, and seem to be guided by immediate prospects only. This finding offers, for the first time, the possibility of detecting these patients' elusive impairment in the laboratory, measuring it, and investigating its possible causes.
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                Author and article information

                Contributors
                pc579@cam.ac.uk
                Journal
                Eur J Neurosci
                Eur. J. Neurosci
                10.1111/(ISSN)1460-9568
                EJN
                The European Journal of Neuroscience
                John Wiley and Sons Inc. (Hoboken )
                0953-816X
                1460-9568
                06 October 2017
                November 2017
                : 46
                : 10 ( doiID: 10.1111/ejn.2017.46.issue-10 )
                : 2620-2628
                Affiliations
                [ 1 ] Department of Psychology University of Cambridge Downing Street Cambridge CB2 3EB UK
                [ 2 ] Service de Psychiatrie et Addictologie CHU de Martinique Fort de France Cedex France
                [ 3 ] Department of Neuroscience and Physiology Neuroscience Institute New York University School of Medicine New York NY USA
                [ 4 ] Service de Neurologie CIC‐INSERM 1402 CHU de Poitiers Poitiers Cedex France
                Author notes
                [*] [* ] Correspondence: Dr Paul Cocker, as above.

                E‐mail: pc579@ 123456cam.ac.uk

                [†]

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-2957-2884
                http://orcid.org/0000-0002-7383-372X
                Article
                EJN13689
                10.1111/ejn.13689
                5725664
                28887899
                72a17c5a-4895-4ebe-a48c-d460af8ae64e
                © 2017 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 July 2017
                : 27 August 2017
                : 29 August 2017
                Page count
                Figures: 4, Tables: 0, Pages: 9, Words: 8039
                Funding
                Funded by: INSERM AVENIR
                Funded by: Fondation pour la Recherche Médicale (FRM)
                Funded by: FRM Young Investigator
                Funded by: Banting Postdoctoral Fellowship
                Funded by: AXA Research fund Fellowship
                Funded by: MRC
                Award ID: RG82507
                Funded by: Leverhulme Trust
                Award ID: RG83473
                Categories
                Behavioural Neuroscience
                Behavioural Neuroscience
                Custom metadata
                2.0
                ejn13689
                November 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.2.8 mode:remove_FC converted:12.12.2017

                Neurosciences
                insular cortex,individual differences,decision‐making,gambling task
                Neurosciences
                insular cortex, individual differences, decision‐making, gambling task

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