What Can Ethobehavioral Studies Tell Us about the Brain's Fear System?

The expression of fear is shaped by an organism's evolutionary history and ecology, and fear has pervasive effects on neural systems and behavior, altering cost–benefit decision-making, spatial navigation, and even biological clocks, among others. While the amygdala seems necessary for many forms of defensive behavior, emerging evidence suggests fear networks that include the hypothalamus, PAG, and mPFC, among others, are distributed throughout the brain and some may support fear responses without the amygdala. Fear and reward-based decision-making are not mutually exclusive systems, and ethological experiments can examine how they interact to produce behavioral decisions that balance perceived costs and benefits. Foraging-associated predation risk is a natural problem all prey must face. Fear evolved due to its protective functions, guiding and shaping behaviors that help animals adapt to various ecological challenges. Despite the breadth of risky situations in nature that demand diversity in fear behaviors, contemporary neurobiological models of fear stem largely from Pavlovian fear conditioning studies that focus on how a particular cue becomes capable of eliciting learned fear responses, thus oversimplifying the brain's fear system. Here we review fear from functional, mechanistic, and phylogenetic perspectives where environmental threats cause animals to alter their foraging strategies in terms of spatial and temporal navigation, and discuss whether the inferences we draw from fear conditioning studies operate in the natural world. Foraging-associated predation risk is a natural problem all prey must face. Fear evolved due to its protective functions, guiding and shaping behaviors that help animals adapt to various ecological challenges. Despite the breadth of risky situations in nature that demand diversity in fear behaviors, contemporary neurobiological models of fear stem largely from Pavlovian fear conditioning studies that focus on how a particular cue becomes capable of eliciting learned fear responses, thus oversimplifying the brain's fear system. Here we review fear from functional, mechanistic, and phylogenetic perspectives where environmental threats cause animals to alter their foraging strategies in terms of spatial and temporal navigation, and discuss whether the inferences we draw from fear conditioning studies operate in the natural world. rhythmic patterns of activity restricted to specific times of the daily cycle, such as the daytime (diurnal), night-time (nocturnal), or dawn-and-dusk times (crepuscular), which are generated by endogenous molecular clocks with approximately 24-h periods and 'entrained' to external cues (zeitgebers), such as sunlight, to remain environmentally relevant. any environmental factors (e.g., predation) that decrease members of a species' reproductive fitness given their current physiological and behavioral traits. a method of using viruses to tag neurons that express a particular gene (e.g., induced by neural activation) and to selectively induce cell death in those neurons. neurons that fire burst spikes preferentially when the animal visits a specific location in a familiarized environment; collectively, these cells are hypothesized to provide a neural representation of the spatial environment. a gene that is expressed during or shortly following the onset of cellular activity (e.g., when a neuron fires an action potential). a sustained enhancement of synaptic transmission following high-frequency stimulation of afferent fibers that has been demonstrated in several brain structures, such as the hippocampus and amygdala, and exhibits properties desirable for information storage (rapidly induced, strengthened by repetition, input specificity, and associativity). a method of precisely controlling the activity of neurons achieved by virus-driven expression of light-sensitive receptors that can be activated or deactivated by a laser focused through optic fibers implanted in the brain. the simplest form of associative learning where an initially neutral stimulus (conditioned stimulus, CS) – via contingent pairing with a biologically significant stimulus (unconditioned stimulus, US) that elicits an unlearned, reflexive behavior (unconditioned response, UR) – acquires a learned behavior (conditioned response, CR) that generally resembles the UR (but not always), precedes the US in time, and reaches a maximum at about the time of US onset. an influential learning algorithm, ΔVn = κ(λ – ΣVi), based on 'US processing' that describes many conditioning phenomenon: κ is a learning constant, λ is the maximum associative strength obtainable with a given US, ΣVi is the sum associative strengths between all CS elements present and the US, and ΔVn is the change in the associative strength of a particular CS on trial n.