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Model-based aversive learning in humans is supported by preferential task state reactivation

Wise, Toby and Liu, Yunzhe and Chowdhury, Fatima and Dolan, Raymond J. (2021) Model-based aversive learning in humans is supported by preferential task state reactivation. Science Advances, 7 (31). Art. No. eabf9616. ISSN 2375-2548. PMCID PMC8318377. doi:10.1126/sciadv.abf9616.

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Harm avoidance is critical for survival, yet little is known regarding the neural mechanisms supporting avoidance in the absence of trial-and-error experience. Flexible avoidance may be supported by a mental model (i.e., model-based), a process for which neural reactivation and sequential replay have emerged as candidate mechanisms. During an aversive learning task, combined with magnetoencephalography, we show prospective and retrospective reactivation during planning and learning, respectively, coupled to evidence for sequential replay. Specifically, when individuals plan in an aversive context, we find preferential reactivation of subsequently chosen goal states. Stronger reactivation is associated with greater hippocampal theta power. At outcome receipt, unchosen goal states are reactivated regardless of outcome valence. Replay of paths leading to goal states was modulated by outcome valence, with aversive outcomes associated with stronger reverse replay than safe outcomes. Our findings are suggestive of avoidance involving simulation of unexperienced states through hippocampally mediated reactivation and replay.

Item Type:Article
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URLURL TypeDescription Materials ItemData ItemCode CentralArticle
Wise, Toby0000-0002-9021-3282
Liu, Yunzhe0000-0003-0836-9403
Chowdhury, Fatima0000-0002-2013-5370
Dolan, Raymond J.0000-0001-9356-761X
Additional Information:© 2021 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). Submitted 1 December 2020; Accepted 10 June 2021; Published 28 July 2021. We thank H. Schmidt and D. Bates for assistance with piloting and data collection. T.W. is supported by a Wellcome Trust Sir Henry Wellcome Fellowship (206460/Z/17/Z). R.J.D. holds a Wellcome Trust Investigator Award (098362/Z/12/Z). Y.L. is supported by the Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning. The Max Planck UCL Centre is a joint initiative supported by UCL and the Max Planck Society. The Wellcome Centre for Human Neuroimaging is supported by core funding from the Wellcome Trust (203147/Z/16/Z). Author contributions: Design: T.W., Y.L., F.C., and R.J.D. Data collection: T.W., F.C., and Y.L. Analysis: T.W. and Y.L. Writing: T.W., Y.L., F.C., and R.J.D. 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 or are freely available online. MEG and behavioral data are available at, and analysis code is available at
Funding AgencyGrant Number
Wellcome Trust206460/Z/17/Z
Wellcome Trust098362/Z/12/Z
State Key Laboratory of Cognitive Neuroscience and LearningUNSPECIFIED
University College LondonUNSPECIFIED
Max Planck SocietyUNSPECIFIED
Wellcome Trust203147/Z/16/Z
Issue or Number:31
PubMed Central ID:PMC8318377
Record Number:CaltechAUTHORS:20210803-140911946
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Official Citation:Model-based aversive learning in humans is supported by preferential task state reactivation. Toby Wise, Yunzhe Liu, Fatima Chowdhury and Raymond J. Dolan. Sci Adv 7 (31), eabf9616; DOI: 10.1126/sciadv.abf9616
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110122
Deposited By: Tony Diaz
Deposited On:04 Aug 2021 18:43
Last Modified:21 Sep 2021 23:50

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