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A mechanism for impaired fear recognition after amygdala damage

Abstract

Ten years ago, we reported that SM, a patient with rare bilateral amygdala damage, showed an intriguing impairment in her ability to recognize fear from facial expressions1. Since then, the importance of the amygdala in processing information about facial emotions has been borne out by a number of lesion2,3,4 and functional imaging studies5,6. Yet the mechanism by which amygdala damage compromises fear recognition has not been identified. Returning to patient SM, we now show that her impairment stems from an inability to make normal use of information from the eye region of faces when judging emotions, a defect we trace to a lack of spontaneous fixations on the eyes during free viewing of faces. Although SM fails to look normally at the eye region in all facial expressions, her selective impairment in recognizing fear is explained by the fact that the eyes are the most important feature for identifying this emotion. Notably, SM's recognition of fearful faces became entirely normal when she was instructed explicitly to look at the eyes. This finding provides a mechanism to explain the amygdala's role in fear recognition, and points to new approaches for the possible rehabilitation of patients with defective emotion perception.

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Figure 1: SM fails to make use of visual information from the eyes in faces.
Figure 2: SM fails to fixate on the eyes when viewing facial expressions.
Figure 3: Instructed viewing of the eyes improves impaired fear recognition in SM.

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Acknowledgements

We thank all participants for their time and effort; N. J. Cohen and members of his laboratory, D. Hannula and J. Gibbons, for help with the administration and analysis of eye movement data; H. Damasio and M. Koenigs for comments on the manuscript; B. Lewis and K. Scheer for assistance with testing subjects, and R. Henson for help in scheduling their visits. This work was supported by grants from NINDS and NIMH, and a Twenty-first Century Science grant from the James S. McDonnell Foundation.

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Correspondence to Ralph Adolphs.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure Legends

Legends for the 5 Supplementary Figures (in the five files given below), and the Supplementary Table 1. Also contains additional references. (DOC 33 kb)

Supplementary Figure S1

The design of the bubbles stimuli. (JPG 22 kb)

Supplementary Figure S2

Differences in the effective information used by SM with each of the individual ten normal control subjects. (JPG 30 kb)

Supplementary Figure S3

Differences in the effective information used by each of the individual ten normal control subjects as compared to the other nine. (JPG 18 kb)

Supplementary Figure S4

The effective information used by subjects with unilateral amygdala damage. (JPG 24 kb)

Supplementary Figure S5

Effective information used to discriminate gender (same for all subjects). (JPG 10 kb)

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Adolphs, R., Gosselin, F., Buchanan, T. et al. A mechanism for impaired fear recognition after amygdala damage. Nature 433, 68–72 (2005). https://doi.org/10.1038/nature03086

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