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.

Keywords: amygdala; anxiety; appraisal; defensive distance; fear; periaqueductal gray; survival optimization system.

Figure 1

Lima and Dill's predator-prey model. Flow chart displaying possible outcomes of a predator-prey encounter. The symbols signify the conditional probabilities of each step of the pathway. a, avoid; e, escape; I, ignore; p, probability that the prey detects the predator first; q, probability that the predator detects the prey first (adapted from Lima and Dill, 1990).

Figure 2

The Medial PFC network. (A) Based on non-human primate research, the major connections of the medial PFC, include the amygdala, PAG, hypothalamus, ventromedial striatum, pallidum and mediodorsal (MD) thalamus. (B) The medial PFC occupies the medial surface of the PFC, encompassing Brodmann's areas 32, 2, 14, 10, and 24 (adapted from Carmichael and Price, 1994). McNaughton and Corr's (2004) parallel neurocircuits of (C) defensive avoidance and (D) defensive approach.

Figure 3

The Survival Optimization System (SOS). (A) Fanselow and Lester's “Threat Imminence Continuum” (B) The SOS proposes that five strategy systems that are associated with predatory imminence and processed in a serial or non-serial manner. Each stage is modulated by several interacting systems including a cognitive system that selectively controls and regulates survival strategies along an abstract to concrete threat continuum. Internal probabilistic models subconsciously learn about, and facilitate responses to, threat. As one moves from predictive to defensive systems, innate and fixed systems are increasingly engaged. PE, prediction error; FFF, Flight/Fight and Freeze.