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Neuropsychology of fear and loathing

Key Points

  • Ideas about emotion in neuroscience and psychology have been dominated by a debate on whether emotion can be encompassed within a single unifying model. In neuroscience this approach is epitomised by the limbic system theory, and in psychology by dimensional models of emotion. Comparative research has gradually eroded the limbic model, and some scientists have proposed that certain individual emotions are represented separately in the brain. Evidence from humans consistent with this proposal has been obtained by showing that signals of fear and disgust may be processed by distinct neural substrates. The focus of this article is to review this research and its implications for theories of emotion.

  • The amygdala is involved in processing facial signals of fear and in fear conditioning. This conclusion has emerged from evidence converging from the analysis of animals with amygdala lesions, from patients with bilateral amygdala damage and from functional imaging experiments in healthy individuals. Research also shows that the amygdala is involved in coding fear cues from other sensory modalities, although in the human literature this is currently under debate.

  • Studies on patients and functional imaging research show a link between the recognition of facial expressions of disgust and the insula-basal ganglia regions. Whether these same brain areas underlie the coding of disgust signals from multiple sensory modalities is only beginning to be addressed.

  • The double dissociation between the recognition of fear and disgust shown in the patient studies and functional imaging research is difficult to reconcile with a number of current models of emotion, but in particular models based on just two dimensions. These two-dimensional models were proposed to account for the structure of emotion and they are reasonably successful in describing the measures of self-reported emotion. However, it is unclear that such models can account for specific deficits in processing fear and disgust. In future it may be more useful for emotion research to focus on causal mechanisms rather than descriptive taxonomies.

Abstract

For over 60 years, ideas about emotion in neuroscience and psychology have been dominated by a debate on whether emotion can be encompassed within a single, unifying model. In neuroscience, this approach is epitomized by the limbic system theory and, in psychology, by dimensional models of emotion. Comparative research has gradually eroded the limbic model, and some scientists have proposed that certain individual emotions are represented separately in the brain. Evidence from humans consistent with this approach has recently been obtained by studies indicating that signals of fear and disgust are processed by distinct neural substrates. We review this research and its implications for theories of emotion.

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Figure 1: The human amygdala, basal ganglia and insula.
Figure 2: The Emotion Hexagon test of facial-expression recognition14.
Figure 3: Functional imaging studies of fear recognition.
Figure 4: Functional imaging studies of disgust recognition.

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Acknowledgements

We would like to thank Jill Keane, Brian Cox and Matthew Brett for their assistance in preparing this article, and Professor Paul Ekman for giving us permission to reproduce examples of the Ekman and Friesen (1976) faces.

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ENCYCLOPEDIA OF LIFE SCIENCES

Limbic system

MIT ENCYCLOPEDIA OF COGNITIVE SCIENCE

Emotion and the human brain

Emotion and the animal brain

Amygdala

Limbic system

Basal ganglia

Glossary

AMYGDALA

A small almond-shaped structure, comprising 13 nuclei, buried in the anterior medial section of each temporal lobe.

BASAL GANGLIA

A group of interconnected subcortical nuclei in the forebrain and midbrain that includes the striatum (putamen and caudate nucleus), globus pallidus, subthalamic nucleus, ventral tegmental area and substantia nigra.

FEAR CONDITIONING

A form of Pavlovian (classical) conditioning in which the animal learns that an innocuous stimulus (for example, an auditory tone — the conditioned stimulus or CS), comes to reliably predict the occurrence of a noxious stimulus (for example, foot shock — the unconditioned stimulus or US) following their repeated paired presentation. As a result of this procedure, presentation of the CS alone elicits conditioned fear responses previously associated with the noxious stimulus only.

VOXEL

Volume element. The smallest distinguishable, box-shaped part of a three-dimensional space.

EMOTIONAL STROOP TASK

A task in which participants are asked to name the colour of the font in which neutral and threat words are printed. Results show that colour-naming times for the threat words are slower than for neutral words. The generally accepted interpretation is that emotional words involuntarily capture attention, distracting the participants from naming.

OBSESSIVE-COMPULSIVE DISORDER

A psychological disorder in which the person is burdened by recurrent, persistent thoughts or ideas, and/or feels compelled to carry out a repetitive, ritualized behaviour. Anxiety is increased by attempts to resist the compulsion and is relieved by giving way to it.

TOURETTE'S SYNDROME

A rare genetic disorder, characterized by facial and vocal tics, and less frequently by verbal profanities.

CONDITIONED TASTE AVERSION

A form of memory in which a taste is associated with digestive malaise, leading to avoidance of the taste in subsequent presentations. This form of memory depends on the integrity of the insula.

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Calder, A., Lawrence, A. & Young, A. Neuropsychology of fear and loathing. Nat Rev Neurosci 2, 352–363 (2001). https://doi.org/10.1038/35072584

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