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

Abstract

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.

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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.

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References

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  ADS  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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. 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).

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

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Acknowledgements

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.).

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Correspondence to Adam K. Anderson.

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Figure 1.

Magnetic resonance images of lesion extent in the patient samples. Coronal T1-weighted (a) and fluid-attenuated inversion recovery (FLAIR) T2-weighted images (b.) at the level of the amygdala in patient SP. There is abnormal signal intensity in the left amygdala secondary to gliosis (curved arrows). The absence of the right amygdala as a result of surgical removal (straight arrows) is also portrayed. Coronal T2-weighted images and axial T2-weighted magnetic resonance images of two patients, one with a right temporal lobectomy (c., d.) and another with a left temporal lobectomy (e., f.). By imaging convention, the patient's right side is on the left side of images.

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

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