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A differential neural response in the human amygdala to fearful and happy facial expressions

Abstract

THE amygdala is thought to play a crucial role in emotional and social behaviour1. Animal studies implicate the amygdala in both fear conditioning2 and face perception3. In humans, lesions of the amygdala can lead to selective deficits in the recognition of fearful facial expressions4,5 and impaired fear conditioning6,7, and direct electrical stimulation evokes fearful emotional responses8. Here we report direct in vivo evidence of a differential neural response in the human amygdala to facial expressions of fear and happiness. Positron-emission tomography (PET) measures of neural activity were acquired while subjects viewed photographs of fearful or happy faces, varying systematically in emotional intensity. The neuronal response in the left amygdala was significantly greater to fearful as opposed to happy expressions. Furthermore, this response showed a significant interaction with the intensity of emotion (increasing with increasing fearfulness, decreasing with increasing happiness). The findings provide direct evidence that the human amygdala is engaged in processing the emotional salience of faces, with a specificity of response to fearful facial expressions.

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References

  1. Kling, A. S. & Brothers, L. A. in The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction (ed. Aggleton, J. P.) 353–377 (Wiley-Liss, New York, 1992).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  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. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. Nature 372, 669–672 (1994).

    Article  ADS  CAS  Google Scholar 

  5. Calder, A. J. et al. Cogn. Neuropsychol. 13, 699–745 (1996).

    Article  Google Scholar 

  6. Bechara, A. et al. Science 269, 1115–1118 (1995).

    Article  ADS  CAS  Google Scholar 

  7. LaBar, K. S., LeDoux, J. E., Spencer, D. D. & Phelps, E. A. J. Neurosci. 15, 6846–6855 (1995).

    Article  CAS  Google Scholar 

  8. Halgren, E., Babb, T. C., Rausch, R. & Crandall, P. H. Brain 101, 83–117 (1978).

    Article  CAS  Google Scholar 

  9. Darwin, C. The Expression of the Emotions in Man and Animals (Univ. Chicago Press, 1965).

    Google Scholar 

  10. Ekman, P. Emotion in the Human Face (Cambridge Univ. Press, Cambridge, 1982).

    Google Scholar 

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

    Google Scholar 

  12. Perrett, D. I., May, K. A. & Yoshikawa, S. Nature 368, 239–242 (1994).

    Article  ADS  CAS  Google Scholar 

  13. Halgren, E. in The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction (ed. Aggleton, J. P.) 190–228 (Wiley-Liss, New York, 1992).

    Google Scholar 

  14. Ketter, T. A. et al. Arch. Gen. Psychiatry 53, 59–69 (1996).

    Article  CAS  Google Scholar 

  15. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. J. Neurosci. 15, 5879–5891 (1995).

    Article  CAS  Google Scholar 

  16. Hamann, S. B. et al. Nature 379, 497 (1996).

    Article  ADS  CAS  Google Scholar 

  17. George, M. S. et al. J. Neuropsychiatry Clin. Neurosci. 5, 384–394 (1993).

    Article  CAS  Google Scholar 

  18. Sergent, J., Ohta, S., MacDonald, B. & Zuck, E. Vis. Cogn. 1, 349–369 (1994).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  20. Iwai, E. & Yukie, M. J. Comp. Neurol. 261, 362–387 (1987).

    Article  CAS  Google Scholar 

  21. Aggleton, J. P., Burton, M. J. & Passingham, R. E. Brain Res. 190, 347–368 (1980).

    Article  CAS  Google Scholar 

  22. Perrett, D. I. et al. Hum. Neurobiol. 3, 197–208 (1984).

    CAS  PubMed  Google Scholar 

  23. Perrett, D. I. et al. J. Exp. Biol. 146, 87–114 (1989).

    CAS  PubMed  Google Scholar 

  24. Le Doux, J. E., Iwata, J., Cicchetti, P. & Reis, D. J. J. Neurosci. 10, 1062–1069 (1988).

    Article  Google Scholar 

  25. Kluver, H. & Bucy, P. C. Arch. Neurol. Psychiatry 42, 979–1000 (1939).

    Article  Google Scholar 

  26. Weiskrantz, L. J. Comp. Physiol. Psychol. 4, 381–391 (1956).

    Article  Google Scholar 

  27. Kling, A. S., Steklis, H. D. & Deutsch, S. Exp. Neurol. 66, 88–96 (1979).

    Article  CAS  Google Scholar 

  28. Friston, K. J. et al. Hum. Brain Mapp. 2, 189–210 (1995).

    Article  Google Scholar 

  29. Friston, K. J. et al. Hum. Brain Mapp. 3, 165–189 (1995).

    Article  Google Scholar 

  30. Worsley, K. J. et al. Hum. Brain Mapp. (in the press).

Download references

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Morris, J., Frith, C., Perrett, D. et al. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812–815 (1996). https://doi.org/10.1038/383812a0

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