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How cognitive and reactive fear circuits optimize escape decisions in humans

Qi, Song and Hassabis, Demis and Sun, Jiayin and Guo, Fangjian and Daw, Nathaniel and Mobbs, Dean (2018) How cognitive and reactive fear circuits optimize escape decisions in humans. Proceedings of the National Academy of Sciences of the United States of America, 115 (12). pp. 3186-3191. ISSN 0027-8424. PMCID PMC5866541. http://resolver.caltech.edu/CaltechAUTHORS:20180306-081009894

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Abstract

Flight initiation distance (FID), the distance at which an organism flees from an approaching threat, is an ecological metric of cost–benefit functions of escape decisions. We adapted the FID paradigm to investigate how fast- or slow-attacking “virtual predators” constrain escape decisions. We show that rapid escape decisions rely on “reactive fear” circuits in the periaqueductal gray and midcingulate cortex (MCC), while protracted escape decisions, defined by larger buffer zones, were associated with “cognitive fear” circuits, which include posterior cingulate cortex, hippocampus, and the ventromedial prefrontal cortex, circuits implicated in more complex information processing, cognitive avoidance strategies, and behavioral flexibility. Using a Bayesian decision-making model, we further show that optimization of escape decisions under rapid flight were localized to the MCC, a region involved in adaptive motor control, while the hippocampus is implicated in optimizing decisions that update and control slower escape initiation. These results demonstrate an unexplored link between defensive survival circuits and their role in adaptive escape decisions.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1712314115DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5866541/PubMed CentralArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1712314115/-/DCSupplementalPublisherSupporting Information
https://doi.org/10.1101/207936DOIDiscussion Paper
https://www.biorxiv.org/content/early/2017/10/23/207936OrganizationDiscussion Paper
ORCID:
AuthorORCID
Mobbs, Dean0000-0003-1175-3772
Additional Information:© 2018 National Academy of Sciences. Published under the PNAS license. Edited by Michael S. Gazzaniga, University of California, Santa Barbara, CA, and approved February 8, 2018 (received for review September 6, 2017). Published ahead of print March 5, 2018. We thank John O’Doherty, Peter Dayan, Alex Shackman, James Curley, and Joe LeDoux for their advice and Nir Jacoby for his work on an earlier version of the paradigm. This study was supported by a grant from National Alliance for Research on Schizophrenia and Depression (to D.M.). Author contributions: S.Q., D.H., J.S., N.D., and D.M. designed research; S.Q. performed research; S.Q., F.G., N.D., and D.M. analyzed data; and S.Q., D.H., F.G., N.D., and D.M. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1712314115/-/DCSupplemental.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
National Alliance for Research on Schizophrenia and DepressionUNSPECIFIED
Subject Keywords:fear; anxiety; escape; ecology; decision making
PubMed Central ID:PMC5866541
Record Number:CaltechAUTHORS:20180306-081009894
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180306-081009894
Official Citation:How cognitive and reactive fear circuits optimize escape decisions in humans Song Qi, Demis Hassabis, Jiayin Sun, Fangjian Guo, Nathaniel Daw, Dean Mobbs Proceedings of the National Academy of Sciences Mar 2018, 115 (12) 3186-3191; DOI: 10.1073/pnas.1712314115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:85123
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:06 Mar 2018 17:16
Last Modified:26 Oct 2018 21:29

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