The role of the amygdala in human fear: Automatic detection of threat (Fragment)

Arne O¨ hman

Psychology Section, Department of Clinical Neuroscience, Karolinska Institute and Hospital, 171 76 Stockholm, Sweden

Summary

Behavioral data suggest that fear stimuli automatically activate fear and capture attention. This effect is likely to be mediated by a subcortical brain network centered on the amygdala. Consistent with this view, brain imaging studies show that masked facial stimuli activate the amygdala as do masked pictures of threatening animals such as snakes and spiders. When the stimulus conditions allow conscious processing, the amygdala response to feared stimuli is enhanced and a cortical network that includes the anterior cingulate cortex and the anterior insula is activated. However, the initial amygdala response to a fear-relevant but non-feared stimulus (e.g. pictures of spiders for a snake phobic) disappears with conscious processing and the cortical network is not recruited. Instead there is activation of the dorsolateral and orbitofrontal cortices that appears to inhibit the amygdala response. The data suggest that activation of the amygdala is mediated by a subcortical pathway, which passes through the superior colliculi and the pulvinar nucleus of the thalamus before accessing the amygdala, and which operates on low spatial frequency information.

Introduction

The purpose of this article is to review some of the recent literature on the role of the amygdala in fear with particular emphasis on my own work. After specifying what I mean by fear, I shall start out with some behavioral work that implicates the amygdala for human fear responses, and then I proceed to brain imaging studies that help to delineate the role of the amygdala in fear activation and attention capture.

A perspective on fear

Fear is an activated, aversive emotional state that serves to motivate the organism to cope with threatening events (O¨ hman, 2000). The coping attempts are more or less clearly focused on metabolically taxing defensive behaviors such as immobility (freezing), escape, or attack. Even though immobility refers to an apparently passive and quiescent organism, it involves an attentive stance associated with an active physiology, in some respects similar to the one seen in the more active flight and fight defenses (O¨hman and Wiens, 2003). A recurrent theme in the text is that fear is controlled from ancient systems in the brain, primarily the amygdala, that may act relatively independently of the later emerging higher cognitions (e.g. LeDoux, 1996; Rosen and Schulkin, 1998; O¨hman and Mineka, 2001).