Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Impaired auditory recognition of fear and anger following bilateral amygdala lesions

Abstract

The amygdalar complex is a medial temporal lobe structure in the brain which is widely considered to be involved in the neural substrates of emotion. Selective bilateral damage to the human amygdala is rare, offering a unique insight into its functions. There is impairment of social perception after amygdala damage, with defective recognition of facial expressions of emotion1–4. Among the basic emotions, the processing of fear and anger has been shown to be disrupted by amygdala damage1,2,5. Although it remains puzzling why this not found in all cases6, the importance of the amygdala in negative emotion, and especially fear, has been confirmed by conditioning7, memory8 and positron emission tomography (PET) experiments9,10. Central to our understanding of these findings is the question of whether the amygdala is involved specifically in the perception of visual signals of emotion emanating from the face, or more widely in the perception of emotion in all sensory modalities11. We report here a further investigation of one of these rare cases, a woman (D.R.) who has impaired perception of the intonation patterns that are essential to the perception of vocal affect, despite normal hearing. As is the case for recognition of facial expressions, it is recognition of fear and anger that is most severely affected in the auditory domain. This shows that the amygdala's role in the recognition of certain emotions is not confined to vision, which is consistent with its being involved in the appraisal of danger and the emotion of fear12,13.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

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

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Young, A. W. et al. Brain 118, 15–24 (1995).

    Article  Google Scholar 

  4. Young, A. W., Hellawell, D. J., van de Wal, C. & Johnson, M. Neuropsychologia 34, 31–39 (1996).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Cahill, L., Babinsky, R., Markowitsch, H. J. & McGaugh, J. L. Nature 377, 295–296 (1995).

    Article  ADS  CAS  Google Scholar 

  9. Cahill, L. et al. Proc. Natl Acad. Sci. USA 93, 8016–8021 (1996).

    Article  ADS  CAS  Google Scholar 

  10. Morris, J. S. et al. Nature 383, 812–815 (1996).

    Article  ADS  CAS  Google Scholar 

  11. Allman, J. & Brothers, L. Nature 372, 613–614 (1994).

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. LeDoux, J. E. Annu. Rev. Psychol. 46, 209–235 (1995).

    Article  CAS  Google Scholar 

  14. Kay, J., Lesser, R. & Coltheart, M. Psycholinguistic Assessments of Language Processing in Aphasia (PALPA) (Erlbaum, Hove, East Sussex, 1992).

    Google Scholar 

  15. Reid, I., Young, A. W. & Hellawell, D. J. Behav. Neurol. 6, 225–228 (1993).

    Article  CAS  Google Scholar 

  16. Frick, R. W. Psychol. Bull. 97, 412–429 (1985).

    Article  Google Scholar 

  17. Van Lancker, D., Kreiman, J. & Wickens, T. D. J. Phonet. 13, 39–52 (1985).

    Google Scholar 

  18. Nolan, F. The Phonetic Bases of Speaker Recognition (Cambridge University Press, Cambridge, 1983).

    Google Scholar 

  19. Murray, I. R. & Arnott, J. L. J. Acous. Soc. Am. 93, 1097–1108 (1993).

    Article  ADS  CAS  Google Scholar 

  20. Leonard, C. M., Rolls, E. T., Wilson, F. A. W. & Baylis, C. G. Behav. Brain Res. 15, 159–176 (1985).

    Article  CAS  Google Scholar 

  21. Rolls, E. T. Hum. Neurobiol. 3, 209–222 (1984).

    CAS  PubMed  Google Scholar 

  22. Nakamura, K., Mikami, A. & Kubota, K. J. Neurophysiol. 67, 1447–1463 (1992).

    Article  CAS  Google Scholar 

  23. Seeck, M. et al. Ann. Neurol. 34, 369–372 (1993).

    Article  CAS  Google Scholar 

  24. Aggleton, J. P. The Amygdala (Wiley-Liss, New York and Chichester, 1992).

    Google Scholar 

  25. Brothers, L. Am. J. Psychiat. 146, 10–19 (1989).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  27. Cohen, J. D., MacWhinney, B., Flatt, M. & Provost, J. Behav. Res. Meth. 25, 257–271 (1993).

    Article  Google Scholar 

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

    Google Scholar 

  29. Ekman, P. in Nebraska Symposium on Motivation, 1971 (ed. Cole, J. K.) 207–283 (University of Nebraska Press, Lincoln, Nebraska, 1972).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scott, S., Young, A., Calder, A. et al. Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature 385, 254–257 (1997). https://doi.org/10.1038/385254a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/385254a0

This article is cited by

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