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      Valuation of knowledge and ignorance in mesolimbic reward circuitry

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          Significance

          Humans desire to know what the future holds. Yet, at times they decide to remain ignorant (e.g., reject medical screenings). These decisions have important societal implications in domains ranging from health to finance. We show how the opportunity to gain information is valued and explain why knowledge is not always preferred. Specifically, the mesolimbic reward circuitry selectively treats the opportunity to gain knowledge about favorable, but not unfavorable, outcomes as a reward to be approached. This coding predicts biased information seeking: Participants choose knowledge about future desirable outcomes more than about undesirable ones, vice versa for ignorance, and are willing to pay for both. This work demonstrates a role for valence in how the human brain values knowledge.

          Abstract

          The pursuit of knowledge is a basic feature of human nature. However, in domains ranging from health to finance people sometimes choose to remain ignorant. Here, we show that valence is central to the process by which the human brain evaluates the opportunity to gain information, explaining why knowledge may not always be preferred. We reveal that the mesolimbic reward circuitry selectively treats the opportunity to gain knowledge about future favorable outcomes, but not unfavorable outcomes, as if it has positive utility. This neural coding predicts participants’ tendency to choose knowledge about future desirable outcomes more often than undesirable ones, and to choose ignorance about future undesirable outcomes more often than desirable ones. Strikingly, participants are willing to pay both for knowledge and ignorance as a function of the expected valence of knowledge. The orbitofrontal cortex (OFC), however, responds to the opportunity to receive knowledge over ignorance regardless of the valence of the information. Connectivity between the OFC and mesolimbic circuitry could contribute to a general preference for knowledge that is also modulated by valence. Our findings characterize the importance of valence in information seeking and its underlying neural computation. This mechanism could lead to suboptimal behavior, such as when people reject medical screenings or monitor investments more during bull than bear markets.

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          Measuring utility by a single-response sequential method.

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            Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum.

            Clinical manifestations in diseases affecting the dopamine system include deficits in emotional, cognitive, and motor function. Although the parallel organization of specific corticostriatal pathways is well documented, mechanisms by which dopamine might integrate information across different cortical/basal ganglia circuits are less well understood. We analyzed a collection of retrograde and anterograde tracing studies to understand how the striatonigrostriatal (SNS) subcircuit directs information flow between ventromedial (limbic), central (associative), and dorsolateral (motor) striatal regions. When viewed as a whole, the ventromedial striatum projects to a wide range of the dopamine cells and receives a relatively small dopamine input. In contrast, the dorsolateral striatum (DLS) receives input from a broad expanse of dopamine cells and has a confined input to the substantia nigra (SN). The central striatum (CS) receives input from and projects to a relatively wide range of the SN. The SNS projection from each striatal region contains three substantia nigra components: a dorsal group of nigrostriatal projecting cells, a central region containing both nigrostriatal projecting cells and its reciprocal striatonigral terminal fields, and a ventral region that receives a specific striatonigral projection but does not contain its reciprocal nigrostriatal projection. Examination of results from multiple tracing experiments simultaneously demonstrates an interface between different striatal regions via the midbrain dopamine cells that forms an ascending spiral between regions. The shell influences the core, the core influences the central striatum, and the central striatum influences the dorsolateral striatum. This anatomical arrangement creates a hierarchy of information flow and provides an anatomical basis for the limbic/cognitive/motor interface via the ventral midbrain.
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              Can parametric statistical methods be trusted for fMRI based group studies?

              The most widely used task fMRI analyses use parametric methods that depend on a variety of assumptions. While individual aspects of these fMRI models have been evaluated, they have not been evaluated in a comprehensive manner with empirical data. In this work, a total of 2 million random task fMRI group analyses have been performed using resting state fMRI data, to compute empirical familywise error rates for the software packages SPM, FSL and AFNI, as well as a standard non-parametric permutation method. While there is some variation, for a nominal familywise error rate of 5% the parametric statistical methods are shown to be conservative for voxel-wise inference and invalid for cluster-wise inference; in particular, cluster size inference with a cluster defining threshold of p = 0.01 generates familywise error rates up to 60%. We conduct a number of follow up analyses and investigations that suggest the cause of the invalid cluster inferences is spatial auto correlation functions that do not follow the assumed Gaussian shape. By comparison, the non-parametric permutation test, which is based on a small number of assumptions, is found to produce valid results for voxel as well as cluster wise inference. Using real task data, we compare the results between one parametric method and the permutation test, and find stark differences in the conclusions drawn between the two using cluster inference. These findings speak to the need of validating the statistical methods being used in the neuroimaging field.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                31 July 2018
                28 June 2018
                28 June 2018
                : 115
                : 31
                : E7255-E7264
                Affiliations
                [1] aAffective Brain Lab, Department of Experimental Psychology, University College London , WC1H 0AP London, United Kingdom;
                [2] bDivision of Humanities and Social Sciences, California Institute of Technology , Pasadena, CA 91125;
                [3] cDepartment of Neuroscience, Columbia University , New York, NY 10032;
                [4] dKavli Institute for Brain Science, Columbia University , New York, NY 10032;
                [5] eDepartment of Neuroscience, Washington University in St. Louis , St. Louis, MO 63110
                Author notes
                1To whom correspondence may be addressed. Email: ccharpen@ 123456caltech.edu or t.sharot@ 123456ucl.ac.uk .

                Edited by Valerie F. Reyna, Cornell University, Ithaca, NY, and accepted by Editorial Board Member Michael S. Gazzaniga May 30, 2018 (received for review January 10, 2018)

                Author contributions: C.J.C., E.S.B.-M., and T.S. designed research; C.J.C. performed research; C.J.C. and T.S. analyzed data; and C.J.C., E.S.B.-M., and T.S. wrote the paper.

                Article
                201800547
                10.1073/pnas.1800547115
                6077743
                29954865
                e16bb5c7-3f5d-43a2-a4f0-d85c7386c88c
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: Wellcome Trust
                Award ID: 093807/Z/10/Z
                Award Recipient : Tali Sharot
                Categories
                PNAS Plus
                Social Sciences
                Psychological and Cognitive Sciences
                Biological Sciences
                Neuroscience
                From the Cover
                PNAS Plus

                information seeking,decision making,valence,knowledge,ignorance

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