Elsevier

Psychoneuroendocrinology

Volume 30, Issue 10, November 2005, Pages 953-958
Psychoneuroendocrinology

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

https://doi.org/10.1016/j.psyneuen.2005.03.019Get rights and content

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.

Section snippets

A perspective on fear

Fear is an activated, aversive emotional state that serves to motivate the organism to cope with threatening events (Öhman, 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

Amygdala activation to masked and non-masked fear stimuli

Morris et al. (1998) examined regional cerebral blood flow responses assessed by positron emission tomography to masked facial stimuli whose emotional impact had been enhanced by Pavlovian conditioning. They reported specific activation of the right amygdala to masked conditioned angry faces as compared to masked non-conditioned angry faces.

To further elucidate the dynamics of fear activation in the human brain Carlsson et al. (2004) recruited participants that either were fearful of snakes or

Conclusions

Research on the neural basis of fear has made important headways during the last few decades. We have gained important knowledge about the factors that activate fear, including the role of non-conscious processes and the role of fear in guiding attention. Furthermore, we are beginning to come to grips with the neural mechanisms behind these behavioral effects. Fear stimuli engage a subcortical network of structures that is centered on the amygdala and that can activate fear responses via an

Acknowledgements

The author's research that is reviewed in this paper was supported by grants from the Swedish Research Council and the Bank of Sweden Tercentennial Foundation. He wishes to express his gratitude to his co-workers Katrina Carlsson, Ray Dolan, Francisco Esteves, Anders Flykt, Martin Ingvar, Pernilla Juth, Andreas Karlsson, Daniel Lundqvist, John Morris, and Karl-Magnus Petersson.

References (34)

  • P. Vuilleumier et al.

    Effects of attention and emotion on faces processing in the human brain: an event-related fMRI study

    Neuron

    (2001)
  • A.K. Anderson et al.

    Neural correlates of the automatic processing of threat facial signals

    J. Neurosci.

    (2003)
  • J.L. Armony et al.

    How danger is encoded: toward a systems, cellular, and computational understanding of cognitive-emotional interactions in fear

  • S.J. Bishop et al.

    Prefrontal cortical function and anxiety: controlling attention to threat related stimuli

    Nat. Neurosci.

    (2004)
  • S.J. Bishop et al.

    State anxiety modulation of the amygdala response to unattended threat-related stimuli

    J. Neurosci.

    (2004)
  • K. Carlsson et al.

    Fear and the amygdala: manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but non-feared) stimuli

    Emotion

    (2004)
  • W.A. Cunningham et al.

    Separable components in the processing of black and white faces

    Psychol. Sci.

    (2004)
  • R.J. Davidson et al.

    Dysfunction in the neural circuitry of emotion regulation—a possible prelude to violence

    Science

    (2000)
  • U. Dimberg et al.

    Behold the wrath: psychophysiological responses to facial stimuli

    Motiv Emotion

    (1996)
  • J. Globisch et al.

    Fear appears fast: temporal course of startle reflex potentiation in animal fearful subjects

    Psychophysiology

    (1999)
  • J.E. LeDoux

    Information flow from sensation to emotion: plasticity in the neural computation of stimulus value

  • J.E. LeDoux

    The Emotional Brain

    (1996)
  • J.E. LeDoux

    Emotion circuits in the brain

    Ann. Rev. Neurosci.

    (2000)
  • W.H.R. Miltner et al.

    Eye movements and behavioral responses to threatening and nonthreatening stimuli during visual search in phobic and nonphobic subjects

    Emotion

    (2004)
  • J.S. Morris et al.

    Conscious and unconscious emotional learning in the human amygdala

    Nature

    (1998)
  • J.S. Morris et al.

    A subcortical pathway to the right amygdala mediating ‘unseen’ fear

    Proc. Natl Acad. Sci. USA

    (1999)
  • J.S. Morris et al.

    Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field

    Brain

    (2001)
  • Cited by (509)

    • Civilian Moral Injury and Amygdala Functional Connectivity During Attention to Threat

      2024, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
    View all citing articles on Scopus
    View full text