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Published March 18, 2015 | Published
Journal Article Open

The ecology of human fear: survival optimization and the nervous system

Abstract

We propose a Survival Optimization System (SOS) to account for the strategies that humans and other animals use to defend against recurring and novel threats. The SOS attempts to merge ecological models that define a repertoire of contextually relevant threat induced survival behaviors with contemporary approaches to human affective science. We first propose that the goal of the nervous system is to reduce surprise and optimize actions by (i) predicting the sensory landscape by simulating possible encounters with threat and selecting the appropriate pre-encounter action and (ii) prevention strategies in which the organism manufactures safe environments. When a potential threat is encountered the (iii) threat orienting system is engaged to determine whether the organism ignores the stimulus or switches into a process of (iv) threat assessment, where the organism monitors the stimulus, weighs the threat value, predicts the actions of the threat, searches for safety, and guides behavioral actions crucial to directed escape. When under imminent attack, (v) defensive systems evoke fast reflexive indirect escape behaviors (i.e., fight or flight). This cascade of responses to threat of increasing magnitude are underwritten by an interconnected neural architecture that extends from cortical and hippocampal circuits, to attention, action and threat systems including the amygdala, striatum, and hard-wired defensive systems in the midbrain. The SOS also includes a modulatory feature consisting of cognitive appraisal systems that flexibly guide perception, risk and action. Moreover, personal and vicarious threat encounters fine-tune avoidance behaviors via model-based learning, with higher organisms bridging data to reduce face-to-face encounters with predators. Our model attempts to unify the divergent field of human affective science, proposing a highly integrated nervous system that has evolved to increase the organism's chances of survival.

Additional Information

© 2015 Mobbs, Hagan, Dalgleish, Silston and Prévost. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Received: 30 September 2014; Accepted: 07 February 2015; Published: 18 March 2015. We thank Michael Ewbank, Peter Dayan, Ralph Adolphs, and Bernhard Staresina for their feedback on an earlier version of the paper. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Edited by: Rogier B. Mars, University of Oxford, UK. Reviewed by: Jean Daunizeau, Brain and Spine Institute (ICM), France Adam Perkins, King's College London, UK.

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August 20, 2023
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October 18, 2023