Subcortical and cortical brain activity during the feeling of self-generated emotions

Abstract

In a series of [15O]PET experiments aimed at investigating the neural basis of emotion and feeling, 41 normal subjects recalled and re-experienced personal life episodes marked by sadness, happiness, anger or fear. We tested the hypothesis that the process of feeling emotions requires the participation of brain regions, such as the somatosensory cortices and the upper brainstem nuclei, that are involved in the mapping and/or regulation of internal organism states. Such areas were indeed engaged, underscoring the close relationship between emotion and homeostasis. The findings also lend support to the idea that the subjective process of feeling emotions is partly grounded in dynamic neural maps, which represent several aspects of the organism's continuously changing internal state.

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Figure 1: Neural correlates of feeling sadness and happiness.
Figure 2: Neural correlates of feeling anger and fear.
Figure 3: Emotion-related activity in anterior pontine nuclei.

References

  1. 1

    Davidson, R. J. & Irwin, W. The functional neuroanatomy of emotion and affective style. Trends Cogn. Sci. 3, 11–21 (1999).

    CAS  Article  Google Scholar 

  2. 2

    Dolan, R. J. et al. Neural activation during covert processing of positive emotional facial expressions. Neuroimage 4, 194–200 (1996).

    CAS  Article  Google Scholar 

  3. 3

    Breiter, H. C. et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17, 875–887 (1996).

    CAS  Article  Google Scholar 

  4. 4

    Whalen, P. J. et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18, 411–418 (1998).

    CAS  Article  Google Scholar 

  5. 5

    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 

  6. 6

    Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669–672 (1994).

    CAS  Article  Google Scholar 

  7. 7

    Adolphs, R., Damasio, H., Tranel, D. & Damasio, A. R. Cortical systems for the recognition of emotion in facial expressions. J. Neurosci. 16, 7678–7687 (1996).

    CAS  Article  Google Scholar 

  8. 8

    George, M. S. et al. Brain activity during transient sadness and happiness in healthy women. Am. J. Psychiatry 152, 341–351 (1995).

    CAS  Article  Google Scholar 

  9. 9

    Pardo, J. V., Pardo, P. J. & Raichle, M. E. Neural correlates of self-induced dysphoria. Am. J. Psychiatry 150, 713–719 (1993).

    CAS  Article  Google Scholar 

  10. 10

    Reiman, E. M. et al. Neuroanatomical correlates of externally and internally generated human emotion. Am. J. Psychiatry 154, 918–925 (1997).

    CAS  Article  Google Scholar 

  11. 11

    Lane, R. D., Reiman, E. M., Ahern, G. L., Schwartz, G. E. & Davidson, R. J. Neuroanatomical correlates of happiness, sadness, and disgust. Am. J. Psychiatry 154, 926–933 (1997).

    CAS  Article  Google Scholar 

  12. 12

    Mayberg, H. S. et al. Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. Am. J. Psychiatry 156, 675–682 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Drevets, W. C. et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386, 824–827 (1997).

    CAS  Article  Google Scholar 

  14. 14

    Damasio, A. R. The Feeling of What Happens: Body and Emotion in the Making of Consciousness (Harcourt Brace, New York, 1999).

    Google Scholar 

  15. 15

    Bandler, R. & Shipley, M. Columnar organization in the midbrain periaqueductal gray—modules for emotional expression? Trends Neurosci. 17, 379–389 (1994).

    CAS  Article  Google Scholar 

  16. 16

    Behbehani, M. M. Functional-characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 46, 575–605 (1995).

    CAS  Article  Google Scholar 

  17. 17

    Bernard, J. F. & Bandler, R. Parallel circuits for emotional coping behaviour: New pieces in the puzzle. J. Comp. Neurol. 401, 429–436 (1998).

    CAS  Article  Google Scholar 

  18. 18

    Panksepp, J., Nelson, E. & Bekkedal M. Brain systems for the mediation of social separation-distress and social-reward. Evolutionary antecedents and neuropeptide intermediaries. Ann. NY Acad. Sci. 807, 78–100 (1997).

    CAS  Article  Google Scholar 

  19. 19

    Damasio, A. R. Descartes' Error: Emotion, Reason, and the Human Brain (Grosset/Putnam, New York, 1994).

    Google Scholar 

  20. 20

    Panksepp, J. Affective Neuroscience: The Foundations of Human and Emotions (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  21. 21

    Rauch, S. L., Savage, C. R., Alpert, N. M., Fischman, A. J. & Jenike, M. A. The functional neuroanatomy of anxiety: A study of three disorders using positron emission tomography and symptom provocation. Biol. Psychiatry 42, 446–452 (1997).

    CAS  Article  Google Scholar 

  22. 22

    Bejjani, B. P. et al. Transient acute depression induced by high-frequency deep-brain stimulation. N. Engl. J. Med. 340, 1476–1480 (1999).

    CAS  Article  Google Scholar 

  23. 23

    Schmahmann, J. D. & Sherman, J. C. The cerebellar cognitive affective syndrome. Brain 121, 561–579 (1998).

    Article  Google Scholar 

  24. 24

    Dolan, R. J. A cognitive affective role for the cerebellum. Brain 121, 545–546 (1998).

    Article  Google Scholar 

  25. 25

    Damasio, A. R. Towards a neuropathology of emotion and mood. Nature 386, 769–770 (1997).

    CAS  Article  Google Scholar 

  26. 26

    Gemar, M. C., Kapur, S., Segal, Z. V., Brown, G. M. & Houle, S. Effects of self-generated sad mood on regional cerebral activity: a PET study in normal subjects. Depression 4, 81–88 (1996).

    CAS  Article  Google Scholar 

  27. 27

    Dougherty, D. D. et al. Anger in healthy men: A PET study using script-driven imagery. Biol. Psychiatry 46, 466–472 (1999).

    CAS  Article  Google Scholar 

  28. 28

    Kimbrell, T. A. et al. Regional brain activity during transient self-induced anxiety and anger in healthy adults. Biol. Psychiatry 46, 454–465 (1999).

    CAS  Article  Google Scholar 

  29. 29

    LeDoux, J. The Emotional Brain: The Mysterious Underpinnings of Emotional Life (Simon and Schuster, New York, 1996).

    Google Scholar 

  30. 30

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

    Article  Google Scholar 

  31. 31

    Buechel, C., Morris, J., Dolan, R. J. & Friston, K. J. Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20, 947–957 (1998).

    Article  Google Scholar 

  32. 32

    LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E. & Phelps, E. A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937–945 (1998).

    CAS  Article  Google Scholar 

  33. 33

    Hichwa, R. D., Ponto, L. B. & Watkins, G. L. in Chemists' Views of Imaging Centers (ed. Emran, A.) 401–417 (Plenum, New York, 1995).

    Google Scholar 

  34. 34

    Woods, R. P., Mazziotta, J. C. & Cherry, S. R. MRI-PET registration with automated algorithm. J. Comput. Assist. Tomogr. 17, 536–546 (1993).

    CAS  Article  Google Scholar 

  35. 35

    Woods, R. P., Dapretto, M., Sicotte, N. L., Toga, A. W. & Mazziotta, J. C. Creation and use of a Talairach-compatible atlas for accurate, automated, nonlinear intersubject registration, and analysis of functional imaging data. Hum. Brain Mapp. 8, 73–79 (1999).

    CAS  Article  Google Scholar 

  36. 36

    Friston, K. J., Poline, J. B., Holmes, A. P., Frith, C. D. & Frackowiak, R. J. A multivariate analysis of PET activation studies. Hum. Brain Mapp. 4, 140–151 (1996).

    CAS  Article  Google Scholar 

  37. 37

    Grabowski, T. J. et al. Reliability of PET activation across statistical methods, subject groups, and sample sizes. Hum. Brain Mapp. 4, 23–46 (1996).

    CAS  Article  Google Scholar 

  38. 38

    Worsley, K. J. Local maxima and the expected Euler characteristic of excursion sets of Chi(2), F and T Fields. Adv. Appl. Prob. 26, 13–42 (1994).

    Article  Google Scholar 

  39. 39

    Frank, R., Damasio, H. & Grabowski, T. J. Brainvox: An interactive multimodal visualization and analysis system for neuroanatomical imaging. Neuroimage 5, 13–30 (1997).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Supported in part by grants from the Mathers Foundation and NIH Grant 1 P50 DC 03189-01A1.

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Correspondence to Antonio R. Damasio.

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Damasio, A., Grabowski, T., Bechara, A. et al. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 3, 1049–1056 (2000). https://doi.org/10.1038/79871

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