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      The value of what’s to come: Neural mechanisms coupling prediction error and the utility of anticipation

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          Abstract

          Hippocampal-midbrain circuit boosts the utility of anticipation in the prefrontal cortex and drives information-seeking behavior.

          Abstract

          Having something to look forward to is a keystone of well-being. Anticipation of future reward, such as an upcoming vacation, can often be more gratifying than the experience itself. Theories suggest the utility of anticipation underpins various behaviors, ranging from beneficial information-seeking to harmful addiction. However, how neural systems compute anticipatory utility remains unclear. We analyzed the brain activity of human participants as they performed a task involving choosing whether to receive information predictive of future pleasant outcomes. Using a computational model, we show three brain regions orchestrate anticipatory utility. Specifically, ventromedial prefrontal cortex tracks the value of anticipatory utility, dopaminergic midbrain correlates with information that enhances anticipation, while sustained hippocampal activity mediates a functional coupling between these regions. Our findings suggest a previously unidentified neural underpinning for anticipation’s influence over decision-making and unify a range of phenomena associated with risk and time-delay preference.

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          Most cited references46

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          Testing for nonlinearity in time series: the method of surrogate data

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            A framework for mesencephalic dopamine systems based on predictive Hebbian learning.

            We develop a theoretical framework that shows how mesencephalic dopamine systems could distribute to their targets a signal that represents information about future expectations. In particular, we show how activity in the cerebral cortex can make predictions about future receipt of reward and how fluctuations in the activity levels of neurons in diffuse dopamine systems above and below baseline levels would represent errors in these predictions that are delivered to cortical and subcortical targets. We present a model for how such errors could be constructed in a real brain that is consistent with physiological results for a subset of dopaminergic neurons located in the ventral tegmental area and surrounding dopaminergic neurons. The theory also makes testable predictions about human choice behavior on a simple decision-making task. Furthermore, we show that, through a simple influence on synaptic plasticity, fluctuations in dopamine release can act to change the predictions in an appropriate manner.
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              Patients with hippocampal amnesia cannot imagine new experiences.

              Amnesic patients have a well established deficit in remembering their past experiences. Surprisingly, however, the question as to whether such patients can imagine new experiences has not been formally addressed to our knowledge. We tested whether a group of amnesic patients with primary damage to the hippocampus bilaterally could construct new imagined experiences in response to short verbal cues that outlined a range of simple commonplace scenarios. Our results revealed that patients were markedly impaired relative to matched control subjects at imagining new experiences. Moreover, we identified a possible source for this deficit. The patients' imagined experiences lacked spatial coherence, consisting instead of fragmented images in the absence of a holistic representation of the environmental setting. The hippocampus, therefore, may make a critical contribution to the creation of new experiences by providing the spatial context into which the disparate elements of an experience can be bound. Given how closely imagined experiences match episodic memories, the absence of this function mediated by the hippocampus, may also fundamentally affect the ability to vividly re-experience the past.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                June 2020
                19 June 2020
                : 6
                : 25
                : eaba3828
                Affiliations
                [1 ]Max-Planck UCL Centre for Computational Psychiatry and Ageing Research, 10-12 Russell Square, London WC1B 5EH, UK.
                [2 ]Gatsby Computational Neuroscience Unit, University College London, 25 Howland Street, London W1T 4JG, UK.
                [3 ]Division of Humanities and Social Sciences, California Institute of Technology, 1200 E California Blvd, Pasadena, CA 91125, USA.
                [4 ]Wellcome Centre for Human Neuroimaging, University College London, 12 Queen Square, London WC1N 3BG, UK.
                [5 ]Deepmind, 6 Pancras Square, London N1C 4AG, UK.
                [6 ]Max Planck Institute for Biological Cybernetics, 72076 Tubingen, Germany.
                [7 ]University of Tübingen, 72074 Tübingen, Germany.
                Author notes
                [* ]Corresponding author. Email: kiigaya@ 123456caltech.edu
                [†]

                These authors share senior authorship.

                Author information
                http://orcid.org/0000-0002-4748-8432
                http://orcid.org/0000-0002-7997-8137
                http://orcid.org/0000-0003-3476-1839
                http://orcid.org/0000-0001-9356-761X
                Article
                aba3828
                10.1126/sciadv.aba3828
                7304967
                32596456
                abf689f9-2a8a-4f10-be10-ab010983c856
                Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

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

                History
                : 28 November 2019
                : 07 May 2020
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100000874, Brain and Behavior Research Foundation;
                Funded by: doi http://dx.doi.org/10.13039/501100000324, Gatsby Charitable Foundation;
                Funded by: doi http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Funded by: doi http://dx.doi.org/10.13039/501100003986, Jacobs Foundation;
                Funded by: doi http://dx.doi.org/10.13039/501100009187, Medical Research Foundation;
                Funded by: doi http://dx.doi.org/10.13039/501100013372, Wellcome Trust Centre for Mitochondrial Research;
                Funded by: Max Planck Foundation;
                Funded by: Swartz Foundation;
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Cognitive Neuroscience
                Cognitive Neuroscience
                Custom metadata
                Sef Rio

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