Lesions of the human amygdala impair enhanced perception of emotionally salient events

Article metrics


Commensurate with the importance of rapidly and efficiently evaluating motivationally significant stimuli, humans are probably endowed with distinct faculties1,2 and maintain specialized neural structures to enhance their detection. Here we consider that a critical function of the human amygdala3,4 is to enhance the perception of stimuli that have emotional significance. Under conditions of limited attention for normal perceptual awareness—that is, the attentional blink5,6—we show that healthy observers demonstrate robust benefits for the perception of verbal stimuli of aversive content compared with stimuli of neutral content. In contrast, a patient with bilateral amygdala damage has no enhanced perception for such aversive stimulus events. Examination of patients with either left or right amygdala resections shows that the enhanced perception of aversive words depends specifically on the left amygdala. All patients comprehend normally the affective meaning of the stimulus events, despite the lack of evidence for enhanced perceptual encoding of these events in patients with left amygdala lesions. Our results reveal a neural substrate for affective influences on perception, indicating that similar neural mechanisms may underlie the affective modulation of both recollective7,8,9 and perceptual experience.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Diagram of the dual-target rapid serial visual presentation (RSVP) task.
Figure 2: Proportion of T2 items correctly identified at early and late T1–T2 temporal lags.
Figure 3: Proportion of T2 correctly identified for negative (circles) and neutral (triangles) items at early and late T1–T2 temporal lags for RTL and LTL patients.


  1. 1

    Bruner, J. S. & Postman, L. Emotional selectivity in perception and reaction. J. Pers. 16, 69–77 (1947).

  2. 2

    Niedenthal, P. M. & Kitayama, S. (eds) The Heart's Eye: Emotional Influences in Perception and Attention (Academic, San Diego, 1994).

  3. 3

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

  4. 4

    LeDoux, J. E. The Emotional Brain (Simon & Schuster, New York, 1992).

  5. 5

    Raymond, J. E., Shapiro, K. L. & Arnell, K. M. Temporary suppression of visual processing in an RSVP task: An attentional blink? J. Exp. Psychol. Hum. Percept. Perform. 18, 849–860 (1992).

  6. 6

    Chun, M. M. & Potter, M. C. A two-stage model for multiple target detection in rapid serial visual presentation. J. Exp. Psychol. Hum. Percept. Perform. 21, 109–127 (1995).

  7. 7

    Cahill, L., Babinsky, R., Markowitsch, H. J. & McGaugh, J. L. The amygdala and emotional memory. Nature 377, 295–296 (1995).

  8. 8

    LaBar, K. S. & Phelps, E. A. Arousal mediated memory consolidation: Role of the medial temporal lobe in humans. Psychol. Sci. 9, 490–493 (1998).

  9. 9

    Phelps, E. A. et al. Specifying the contributions of the human amygdala to emotional memory: a case study. Neurocase 4, 527–540 (1998).

  10. 10

    Amaral, D. G., Price, J. L., Pitkanen, A. & Charmichael, S. T. in The Amygdala (ed. Aggleton, J. P.) 1–66 (Wiley-Liss, New York, 1992).

  11. 11

    Nishijo, H., Ono, T. & Nishino, H. Single neuron responses in amygdala of alert monkeys during complex sensory stimulation with affective significance. J. Neurosci. 8, 3570–3583 (1988).

  12. 12

    Cahill, L. et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. Natl Acad. Sci. USA 93, 8016–8021 (1996).

  13. 13

    Hamann, S. B., Ely, T. D., Grafton, S. T. & Kilts, C. D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neurosci. 2, 289–294 (1999).

  14. 14

    Canli, T., Zuo, Z., Brewer, J., Gabrieli, J. D. & Cahill, L. Event-related activation in the human amygdala associates with later memory for individual emotional experience. J. Neurosci. 20, RC99, 1–5 (2000).

  15. 15

    Vogel, E. K., Luck, S. J. & Shapiro, K. L. Electrophysiological evidence for a postperceptual locus of suppression during the attentional blink. J. Exp. Psychol. Hum. Percept. Perform. 24, 1656–1674 (1998).

  16. 16

    Anderson, A. K. Affective influences on attentional dynamics during perceptual encoding: Investigations with the attentional blink. J. Exp. Psychol. Gen. (submitted).

  17. 17

    Anderson, A. K. & Phelps, E. A. Expression without recognition: Contributions of the human amygdala to emotional communication. Psychol. Sci. 11, 106–111 (2000).

  18. 18

    Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. R. Fear and the human amygdala. J. Neurosci. 15, 5879–5891 (1995).

  19. 19

    Strange, B. A., Henson, R. N. A., Friston, K. J. & Dolan, R. J. Brain mechanisms for detecting perceptual, semantic, and emotional deviance. NeuroImage 12, 425–433 (2000).

  20. 20

    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).

  21. 21

    Adolphs, R., Damasio, H., Tranel, D., Cooper, G. & Damasio, A. R. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J. Neurosci. 20, 2683–2690 (2000).

  22. 22

    Funayama, E. S., Grillon, C. G., Davis, M. & Phelps, E. A. A double dissociation in the affective modulation of startle in humans: Effects of unilateral temporal lobectomy. J. Cogn. Neurosci. (in the press).

  23. 23

    Kapp, B. S., Wilson, A., Pascoe, J. P., Supple, W. & Whalen, P. J. in Neurocomputation and Learning: Foundations of Adaptive Networks (eds Gabriel, M. & Moore, J.) 53–90 (MIT Press, Cambridge, Massachusetts, 1990).

  24. 24

    Whalen, P. J. Fear, vigilance, and ambiguity: Initial neuroimaging studies of the human amygdala. Curr. Dir. Psychol. Sci. 7, 177–188 (1998).

  25. 25

    Morris, J. S. et al. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121, 47–57 (1998).

  26. 26

    Morris, J. S., Friston, K. J. & Dolan, R. J. Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proc. R. Soc. Lond. B 265, 649–657 (1998).

  27. 27

    Isenberg, N. et al. Linguistic threat activates the human amygdala. Proc. Natl Acad. Sci. USA 96, 10456–10459 (1999).

  28. 28

    Weinberger, N. M. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 1071–1089 (MIT Press, Cambridge, Massachusetts, 1995).

  29. 29

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

  30. 30

    Spencer, D. D., Spencer, S. S., Mattson, R. H., Williamson, P. D. & Novelly, R. A. Access to the posterior medial temporal lobe structure in the surgical treatment of temporal lobe epilepsy. Neurosurgery 15, 667–671 (1984).

Download references


We thank M. Chun, E. De Rosa, K. O'Connor, K. Ochsner, I. Olson, M. Packard and N. Sobel for comments during the preparation of this manuscript, and D. Spencer for access to the patient samples. This work was supported by the James S. McDonnell Foundation (E.A.P.).

Author information

Correspondence to Adam K. Anderson.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Anderson, A., Phelps, E. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309 (2001) doi:10.1038/35077083

Download citation

Further reading


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.