Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

Abstract

STUDIES in animals have shown that the amygdala receives highly processed visual input1,2, contains neurons that respond selectively to faces3, and that it participates in emotion4,5 and social behaviour6. Although studies in epileptic patients support its role in emotion7, determination of the amygdala's function in humans has been hampered by the rarity of patients with selective amygdala lesions8. Here, with the help of one such rare patient, we report findings that suggest the human amygdala may be indispensable to: (1) recognize fear in facial expressions; (2) recognize multiple emotions in a single facial expression; but (3) is not required to recognize personal identity from faces. These results suggest that damage restricted to the amygdala causes very specific recognition impairments, and thus constrains the broad notion that the amygdala is involved in emotion.

Access 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

    Herzog, A. G. & Van Hoesen, G. W. Brain Res. 115, 57–69 (1976).

    CAS  Article  Google Scholar 

  2. 2

    Amaral, D. G., Price, J. L., Pitkanen, A. & Carmichael, S. T. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J. P.) 1–66 (Wiley-Liss, New York, 1992).

    Google Scholar 

  3. 3

    Rolls, E. T. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J. P.) 143–167 (Wiley-Liss, New York, 1992).

    Google Scholar 

  4. 4

    Aggleton, J. P. (ed.) The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (Wiley-Liss, New York, 1992).

  5. 5

    LeDoux, J. E. Behavl Brain Res. 58, 69–79 (1993).

    CAS  Article  Google Scholar 

  6. 6

    Kling, A. S. & Brothers, L. A. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J. P.) 353–378 (Wiley-Liss, New York, 1992).

    Google Scholar 

  7. 7

    Halgren, E., Walter, R. D., Cherlow, D. G. & Crandall, P. H. Brain 101, 83–117 (1978).

    CAS  Article  Google Scholar 

  8. 8

    Aggleton, J. P. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J. P.) 485–504 (Wiley-Liss, New York, 1992).

    Google Scholar 

  9. 9

    Nahm, F. K. D., Tranel, D., Damasio, H. & Damasio, A. R. Neuropsychologia 31, 727–744 (1993).

    CAS  Article  Google Scholar 

  10. 10

    Tranel, D. & Hyman, B. T. Archs Neurol. 47, 349–355 (1990).

    CAS  Article  Google Scholar 

  11. 11

    Hofer, P.-A. Acta Derm. Venerol. 53, 5–52 (1973).

    Google Scholar 

  12. 12

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

    Google Scholar 

  13. 13

    Tranel, D., Damasio, A. R. & Damasio, H. Neurology 38, 690–696 (1988).

    CAS  Article  Google Scholar 

  14. 14

    Damasio, A. R., Tranel, D. & Damasio, H. A. Rev. Neurosci. 13, 89–109 (1990).

    CAS  Article  Google Scholar 

  15. 15

    Humphreys, G. W., Donnelly, N. & Riddoch, M. J. Neuropsychologia 31, 173–181 (1993).

    CAS  Article  Google Scholar 

  16. 16

    Hasselmo, M. E., Rolls, E. T. & Baylis, G. C. Behavl Brain Res. 32, 203–218 (1989).

    CAS  Article  Google Scholar 

  17. 17

    Blanchard, D. C. & Blanchard, R. J. J. comp. Physiol. Psychol. 81, 281–290 (1972).

    CAS  Article  Google Scholar 

  18. 18

    Weiskrantz, L. J. comp. Physiol. Psychol. 49, 381–391 (1956).

    CAS  Article  Google Scholar 

  19. 19

    Davis, M. A. Rev. Neurosci. 15, 353–375 (1992).

    CAS  Article  Google Scholar 

  20. 20

    Russell, J. A. & Bullock, M. J. Pers. Soc. Psychol. 48, 1290–1298 (1985).

    Article  Google Scholar 

  21. 21

    Russell, J. A. J. Pers. Soc. Psychol. 39, 1161–1178 (1980).

    Article  Google Scholar 

  22. 22

    Russell, J. A., Lewicka, M. & Niit, T. J. Pers. Soc. Psychol. 57, 848–856 (1989).

    Article  Google Scholar 

  23. 23

    Ekman, P. Darwin and Facial Expression: A Century of Research in Review (Academic, New York, 1973).

    Google Scholar 

  24. 24

    Darwin, C. The Expression of the Emotions in Man and Animals (University of Chicago Press, Chicago, 1872/1965).

    Google Scholar 

  25. 25

    Russell, J. A. Psychol. Bull. 110, 426–450 (1991).

    CAS  Article  Google Scholar 

  26. 26

    Damasio, H. & Frank, R. Archs Neurol. 49, 137–143 (1992).

    CAS  Article  Google Scholar 

  27. 27

    Damasio, H. & Damasio, A. R. Lesion Analysis in Neuropsychology (Oxford University Press, New York, 1989).

    Google Scholar 

  28. 28

    Guttman, L. A. Psychometrika 33, 469–506 (1968).

    Article  Google Scholar 

  29. 29

    Kruskal, J. B. Psychometrika 29, 115–129 (1964).

    MathSciNet  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Adolphs, R., Tranel, D., Damasio, H. et al. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669–672 (1994). https://doi.org/10.1038/372669a0

Download citation

Further reading

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing