Abstract

Classical Pavlovian fear conditioning to painful stimuli has provided the generally accepted view of a core system centered in the central amygdala to organize fear responses. Ethologically based models using other sources of threat likely to be expected in a natural environment, such as predators or aggressive dominant conspecifics, have challenged this concept of a unitary core circuit for fear processing. We discuss here what the ethologically based models have told us about the neural systems organizing fear responses. We explored the concept that parallel paths process different classes of threats, and that these different paths influence distinct regions in the periaqueductal gray - a critical element for the organization of all kinds of fear responses. Despite this parallel processing of different kinds of threats, we have discussed an interesting emerging view that common cortical-hippocampal-amygdalar paths seem to be engaged in fear conditioning to painful stimuli, to predators and, perhaps, to aggressive dominant conspecifics as well. Overall, the aim of this review is to bring into focus a more global and comprehensive view of the systems organizing fear responses.

Highlights

  • The prevailing view of central fear system organization emerged from studies using classical Pavlovian fear conditioning, indicating the amygdala as a major player in learning, storage, and expression of fear responses [1]

  • We reviewed how different threats are processed by these parallel circuits, likely to be preserved across species, and how they target the periaqueductal gray (PAG), a critical brain site for the organization of fear responses

  • The medial zone of the hypothalamus has been shown to have a critical role in processing threatening stimuli, like predator exposure and social threats from dominant conspecifics, which, under natural circumstances, are the events more likely to evoke the sensation of fear and the accompanying defensive responses [6,7]

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Summary

Introduction

The prevailing view of central fear system organization emerged from studies using classical Pavlovian fear conditioning, indicating the amygdala as a major player in learning, storage, and expression of fear responses [1]. The view of a unitary central fear system has been challenged by several experimental lines of evidence, and lesions of the central nucleus have been found to have no effect on either unconditioned or conditioned defensive responses to a live predator or its odor [4,5]. We reviewed how different threats are processed by these parallel circuits, likely to be preserved across species, and how they target the periaqueductal gray (PAG), a critical brain site for the organization of fear responses. The aim of this article is to bring into focus a more global and comprehensive view of the systems organizing fear responses, challenging the concept of a unitary core circuit for fear processing, and yet providing the communalities among the fear memory circuits

Different classes of threats mobilize distinct neural systems
The PAG and its role in the expression of fear responses

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