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

Iigaya, Kiyohito and Hauser, Tobias U. and Kurth-Nelson, Zeb and O'Doherty, John P. and Dayan, Peter and Dolan, Raymond J. (2020) The value of what’s to come: Neural mechanisms coupling prediction error and the utility of anticipation. Science Advances, 6 (25). Art. No. eaba3828. ISSN 2375-2548. PMCID PMC7304967. https://resolver.caltech.edu/CaltechAUTHORS:20190709-075726647

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1126/sciadv.aba3828DOIArticle
http://advances.sciencemag.org/cgi/content/full/6/25/eaba3828/DC1PublisherSupporting Information
https://neurovault.org/collections/DXZZFYSF/Related ItemData
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7304967PubMed CentralArticle
https://doi.org/10.1101/588699DOIDiscussion Paper
ORCID:
AuthorORCID
Iigaya, Kiyohito0000-0002-4748-8432
Hauser, Tobias U.0000-0002-7997-8137
O'Doherty, John P.0000-0003-0016-3531
Dayan, Peter0000-0003-3476-1839
Dolan, Raymond J.0000-0001-9356-761X
Alternate Title:The value of what’s to come: neural mechanisms coupling prediction error and reward anticipation
Additional Information:© 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. Received for publication November 28, 2019. Accepted for publication May 7, 2020. We thank T. Behrens for his insightful suggestion for the Fourier phase-randomization test. We thank C. Camerer, O. Hikosaka, G. Loewenstein, S. Romani, E. Bromberg-Martin, J. Gotlieb, E. Ludvig, Y. Liu, B. Blain, G. Story, L. Hunt, J. Cockburn, V. Man, T. Aquino, C. Charpentier, B. Fung, W. Pauli, and E. Burkett for the most valuable discussions and helpful suggestions for the manuscript. We also thank radiographers at the UCL for their assistance in running fMRI experiments. This work was funded by the Max Planck Society, the Gatsby Foundation, Wellcome Trust Investigator Award, the Japan Society for the Promotion of Science, the Swartz Foundation, Wellcome Sir Henry Dale Fellowship (211155/Z/18/Z), the Jacobs Foundation (2017-1261-04), the Medical Research Foundation, The Alexander von Humboldt Foundation, and 2018 NARSAD Young Investigator grant (27023) from the Brain and Behavior Research Foundation. Author contributions: K.I., Z.K.-N., P.D., and R.J.D. designed the project. K.I. and Z.K.-N. performed the experiment. K.I., T.U.H., Z.K-N., J.P.O., P.D., and R.J.D. analyzed and discussed the results and wrote the manuscript. The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper is available on NeuroVault [https://neurovault.org/collections/DXZZFYSF/].
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
Max Planck SocietyUNSPECIFIED
Gatsby Charitable FoundationUNSPECIFIED
Wellcome Trust211155/Z/18/Z
Japan Society for the Promotion of Science (JSPS)UNSPECIFIED
Swartz FoundationUNSPECIFIED
Jacobs Foundation2017-1261-04
Medical Research FoundationUNSPECIFIED
Alexander von Humboldt FoundationUNSPECIFIED
Brain and Behavior Research Foundation27023
Issue or Number:25
PubMed Central ID:PMC7304967
Record Number:CaltechAUTHORS:20190709-075726647
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190709-075726647
Official Citation:The value of what’s to come: Neural mechanisms coupling prediction error and the utility of anticipation. BY KIYOHITO IIGAYA, TOBIAS U. HAUSER, ZEB KURTH-NELSON, JOHN P. O’DOHERTY, PETER DAYAN, RAYMOND J. DOLAN Science Advances 19 Jun 2020: Vol. 6, no. 25, eaba3828; DOI: 10.1126/sciadv.aba3828
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:96939
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:09 Jul 2019 20:04
Last Modified:25 Nov 2020 01:07

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