Conscious and unconscious emotional learning in the human amygdala (original) (raw)

Nature volume 393, pages 467–470 (1998)Cite this article

Abstract

If subjects are shown an angry face as a target visual stimulus for less than forty milliseconds and are then immediately shown an expressionless mask, these subjects report seeing the mask but not the target. However, an aversively conditioned masked target can elicit an emotional response from subjects without being consciously perceived1,2. Here we study the mechanism of this unconsciously mediated emotional learning. We measured neural activity in volunteer subjects who were presented with two angry faces, one of which, through previous classical conditioning, was associated with a burst of white noise. In half of the trials, the subjects' awareness of the angry faces was prevented by backward masking with a neutral face. A significant neural response was elicited in the right, but not left, amygdala to masked presentations of the conditioned angry face. Unmasked presentations of the same face produced enhanced neural activity in the left, but not right, amygdala. Our results indicate that, first, the human amygdala can discriminate between stimuli solely on the basis of their acquired behavioural significance, and second, this response is lateralized according to the subjects' level of awareness of the stimuli.

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References

  1. Esteves, F., Dimberg, U. & Öhman, A. Automatically elicited fear: conditioned skin conductance responses to masked facial expressions. Cogn. Emotion 9, 99–108 (1994).
    Google Scholar
  2. Ohman, A. & Soares, J. J. F. “Unconscious anxiety”: phobic responses to masked stimuli. J. Abnorm. Psychol. 103, 231–240 (1994).
    Article CAS Google Scholar
  3. Weiskrantz, L. Behavioural changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 49, 381–391 (1956).
    Article CAS Google Scholar
  4. Kapp, B. S., Pascoe, J. P. & Bixler, M. A. in Neuropyschology of Memory(eds Butters, N. & Squire, L. R.) 473–488 (Guilford, New York, 1984).
    Google Scholar
  5. Davis, M. in The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction(ed. Aggleton, J. P.) 255–306 (Wiley-Liss, New York, 1992).
    Google Scholar
  6. LeDoux, J. E. The Emotional Brain(Simon and Schuster, New York, 1996).
    Google Scholar
  7. Bechara, A. et al. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115–1118 (1995).
    Article ADS CAS Google Scholar
  8. LaBar, K. S., LeDoux, J. E., Spencer, D. D. & Phelps, E. A. Impaired fear conditioning following unilateral temporal lobectomy. J. Neurosci. 15, 6846–6855 (1995).
    Article CAS Google Scholar
  9. Babinsky, R. et al. The possible contribution of the amygdala to memory. Behav. Neurol. 6, 167–170 (1993).
    Article CAS Google Scholar
  10. Adolphs, R., Cahill, L., Scull, R. & Babinsky, R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learning Memory 4, 291–300 (1997).
    Article CAS Google Scholar
  11. Fried, I., Macdonald, K. A. & Wilson, C. L. Single neuron activity in hippocampus and amygdala during recognition of faces and objects. Neuron 18, 875–887 (1997).
    Article Google Scholar
  12. Whalen, P. J. et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18, 411–418 (1998).
    Article CAS Google Scholar
  13. Leonard, C. M., Rolls, E. T., Wilson, F. A. & Baylis, G. C. Neurons int he amygdala of the monkey with responses selective for faces. Behav. Brain Res. 15, 159–176 (1985).
    Article CAS Google Scholar
  14. 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
  15. DeKosky, S. T., Heilman, K. M., Bowers, D. & Valenstein, E. Recognition and discrimination of emotional faces and pictures. Brain Lang. 9, 206–214 (1980).
    Article CAS Google Scholar
  16. Gazzaniga, M. S. & Smylie, C. S. Facial recognition and brain asymmetries: clues to underlying mechanisms. Ann. Neurol. 13, 536–540 (1983).
    Article CAS Google Scholar
  17. Gur, R. C., Skolnick, B. E. & Gurr, R. E. Effects of emotional discrimination tasks on cerebral blood flow: regional activation and its relation to performance. Brain Cogn. 25, 271–286 (1994).
    Article CAS Google Scholar
  18. Ladavas, E., Cimatti, D., Del Pesce, M. & Tuozzi, G. Emotional evaluation with and without conscious stimulus identification: evidence from a split-brain patient. Cogn. Emotion 7, 95–114 (1993).
    Article Google Scholar
  19. Klinger, M. R. & Greenwald, A. G. Unconscious priming of association judgements. J. Exp. Psych. Learn. Mem. Cogn. 21, 569–581 (1995).
    Article CAS Google Scholar
  20. Hugdahl, K. et al. Brain mechanisms in human classical conditioning: a PET blood flow study. Neuroreport 6, 1723–1728 (1995).
    Article CAS Google Scholar
  21. Morris, J. S., Friston, K. J. & Dolan, R. J. Neural responses to salient visual stimuli. Proc. R. Soc. Lond. B 264, 769–775 (1997).
    Article ADS CAS Google Scholar
  22. Young, A. W., Newcombe, F., de Haan, E. H. F., Small, M. & Hay, D. C. Face perception after brain injury. Selective impairments affecting identity and expression. Brain 116, 941–959 (1993).
    Article Google Scholar
  23. Stone, V. S., Nisenson, L., Eliassen, J. C. & Gazzaniga, M. S. Left hemisphere representations of emotional facial expressions. Neuropsychol. 34, 23–29 (1995).
    Article Google Scholar
  24. Morris, J. S. et al. Adifferential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812–815 (1996).
    Article ADS CAS Google Scholar
  25. Breiter, H. C. et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17, 875–887 (1996).
    Article CAS Google Scholar
  26. Gazzaniga, M. S. in The Cognitive Neurosiciences(ed. Gazzaniga, M. S.) 1049–1061 (MIT Press, Cambridge, MA, 1995).
    Google Scholar
  27. Friston, K. J. et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189–210 (1995).
    Article Google Scholar
  28. Friston, K. J. et al. Spatial registration and normalization of images. Hum. Brain Mapp. 3, 165–189 (1995).
    Article Google Scholar
  29. Worsley, K. J., Marrett, P., Neelin, A. C., Friston, K. J. & Evans, A. C. Aunified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 4, 58–73 (1996).
    Article CAS Google Scholar
  30. Ekman, P. & Friesen, W. V. Pictures of Facial Affect(Consulting Psychologists Press, Palo Alto, 1976).
    Google Scholar

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Authors and Affiliations

  1. Wellcome Department of Cognitive Neurology, Queen Square, WC1N 3BG, London, UK
    J. S. Morris & R. J. Dolan
  2. Department of Clinical Neuroscience, Section of Psychiatry and Psychology, Karolinska Hospital, S-17176, Stockholm, Sweden
    A. Öhman
  3. Royal Free and University College Hospitals School of Medicine, Rowland Hill Street, NW3 2DF, London, UK
    R. J. Dolan

Authors

  1. J. S. Morris
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  2. A. Öhman
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  3. R. J. Dolan
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Morris, J., Öhman, A. & Dolan, R. Conscious and unconscious emotional learning in the human amygdala.Nature 393, 467–470 (1998). https://doi.org/10.1038/30976

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