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Published March 20, 2018 | Supplemental Material + Submitted + Published
Journal Article Open

How cognitive and reactive fear circuits optimize escape decisions in humans

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.

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.

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Published - 3186.full.pdf

Submitted - 207936.full.pdf

Supplemental Material - pnas.1712314115.sapp.pdf

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Additional details

Created:
August 21, 2023
Modified:
October 23, 2023