Letter | Published:

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669–672 (1994)

  2. 2

    Young, A. W. et al. Face processing impairments after amygdalotomy. Brain 118, 15–24 (1995)

  3. 3

    Adolphs, R. et al. Recognition of facial emotion in nine subjects with bilateral amygdala damage. Neuropsychologia 37, 1111–1117 (1999)

  4. 4

    Schmolck, H. & Squire, L. R. Impaired perception of facial emotions following bilateral damage to the anterior temporal lobe. Neuropsychology 15, 30–38 (2001)

  5. 5

    Morris, J. S. et al. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812–815 (1996)

  6. 6

    Adams, R. B., Gordon, H. L., Baird, A. A., Ambady, N. & Kleck, R. E. Effects of gaze on amygdala sensitivity to anger and fear faces. Science 300, 1536 (2003)

  7. 7

    Adolphs, R. & Tranel, D. in The Amygdala. A Functional Analysis (ed. Aggleton, J. P.) 587–630 (Oxford Univ. Press, New York, 2000)

  8. 8

    Bechara, A. et al. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115–1118 (1995)

  9. 9

    Adolphs, R., Tranel, D. & Damasio, A. R. The human amygdala in social judgment. Nature 393, 470–474 (1998)

  10. 10

    Gosselin, F. & Schyns, P. G. Bubbles: a technique to reveal the use of information in recognition. Vision Res. 41, 2261–2271 (2001)

  11. 11

    Schyns, P. G., Bonnar, L. & Gosselin, F. Show me the features! Understanding recognition from the use of visual information. Psychol. Sci. 13, 402–409 (2002)

  12. 12

    Smith, M. L., Cottrell, G. W., Gosselin, F. & Schyns, P. G. Transmitting and decoding facial expressions of emotion. Psychol. Sci. (in the press)

  13. 13

    Ekman, P. & Friesen, W. Pictures of Facial Affect (Consulting Psychologists Press, Palo Alto, California, 1976)

  14. 14

    Lundqvist, D. & Litton, J.-E. The Karolinska Directed Faces (Karolinska Institute, 1998)

  15. 15

    Haith, M. M., Bergman, T. & Moore, M. J. Eye contact and face scanning in early infancy. Science 198, 853–855 (1977)

  16. 16

    Keating, C. & Keating, E. G. Visual scan patterns of rhesus monkeys viewing faces. Perception 11, 211–219 (1982)

  17. 17

    Amaral, D. G. & Price, J. L. Amygdalo-cortical connections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230, 465–496 (1984)

  18. 18

    Anderson, A. K. & Phelps, E. A. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309 (2001)

  19. 19

    Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J. & Dolan, R. J. Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neurosci. 7, 1271–1278 (2004)

  20. 20

    Whalen, P. J. Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Curr. Dir. Psychol. Sci. 7, 177–187 (1999)

  21. 21

    Kapp, B. S., Whalen, P. J., Supple, W. F. & Pascoe, J. P. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J.) 254–269 (Wiley-Liss, New York, 1992)

  22. 22

    Holland, P. C. & Gallagher, M. Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci. 3, 65–73 (1999)

  23. 23

    Kawashima, R. et al. The human amygdala plays an important role in gaze monitoring. Brain 122, 779–783 (1999)

  24. 24

    Morris, J. S., deBonis, M. & Dolan, R. J. Human amygdala responses to fearful eyes. Neuroimage 17, 214–222 (2002)

  25. 25

    Anderson, A. K., Spencer, D. D., Fulbright, R. K. & Phelps, E. A. Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology 14, 526–536 (2000)

  26. 26

    Calder, A. J. et al. Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear. Cogn. Neuropsychol. 13, 699–745 (1996)

  27. 27

    Emery, N. J. The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci. Biobehav. Rev. 24, 581–604 (2000)

  28. 28

    Pelphrey, K. A. et al. Visual scanning of faces in autism. J. Autism Dev. Disord. 32, 249–261 (2002)

  29. 29

    Klin, A., Jones, W., Schultz, R., Volkmar, F. R. & Cohen, D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch. Gen. Psychiatry 59, 809–816 (2002)

  30. 30

    Howard, M. A. et al. Convergent neuroanatomical and behavioral evidence of an amygdala hypothesis of autism. Neuroreport 11, 2931–2935 (2000)

Download references

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.

Author information

Correspondence to Ralph Adolphs.

Ethics declarations

Competing interests

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)

Rights and permissions

Reprints and Permissions

About this article

Further reading

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.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.