The Human Amygdala: An Evolved System for Relevance Detection

Abstract

SYNOPSISEvidence from pioneering animal research has suggested that the amygdala is involved in the processing of aversive stimuli, particularly fear-related information. Fear is central in the evolution of the mammalian brain: it is automatically and rapidly elicited by potentially dangerous and deadly events. The view that the amygdala shares the main characteristics of modular systems, e.g. domain specificity, automaticity, and cognitive impenetrability, has become popular in neuroscience. Because of its computational properties, it has been proposed to implement a rapid-response 'fear module'. In this article, we review recent patient and neuroimaging data of the human brain and argue that the fundamental criteria for the amygdala to be a modular system are not met. We propose a different computational view and suggest the notion of a specific involvement of the human amygdala in the appraisal of relevant events that include, but are not restricted to, fearrelated stimuli. Considering the amygdala as a 'relevance detector' would integrate the 'fear module' hypothesis with the concept of an evolved neural system devoted to the processing of a broader category of biologically relevant stimuli. In primates, socially relevant events appear to have become, through evolution, the dominant elements of the amygdala's domain of specificity. KEY WORDSsocial cognition, emotion, appraisal, evolutionary psychology, temporal lobe, human brain PURPOSE AND OVERVIEWThe study of the functions of the amygdala has exploded during the so-called 'decade of the brain'. During this period many new anatomical and functional findings about the amygdala have been obtained (see /10,11 /). A marker of this interest is that numerous reviews on the amygdala have been published; these articles include reviews highlighting the amygdala's contributions to emotion /3,27,73/, vigilance-emotion relationships /34,100/, memory /46,63,76/, attention /51/, fear conditioning /26/, reward-based learning /18/ and social cognition /2,4,13/. In the present review, we challenge one of the major features of the current theories of the human amygdala by proposing a different hypothesis about its computational profile and domain of specificity. In order to do so, we adopt a perspective that takes into account data from cognitive neuropsychology and functional brain imaging in humans. After a short presentation of the dual route architecture in which the amygdala is involved, we show that the definition of the amygdala's specific domain of processing is highly controversial and propose a perspective that may help to resolve this debate. A DUAL ROUTE ARCHITECTURE TO THE AMYGDALAPioneering animal studies have provided an important contribution to the understanding of the anatomical and functional structure of the amygdala. The primate amygdala is an almond-shaped VOLUME 14, NO. 4. 2003 303 Brought to you by | University of Arizona Authenticated Download Date | 5/31/15 5:45 AM 304 I). SANDER Ε Γ AL. nuclear complex composed of at least 13 nuclei located'in t...

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