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Neural systems supporting interoceptive awareness

Nature Neuroscience volume 7, pages 189–195 (2004)Cite this article

Abstract

Influential theories of human emotion argue that subjective feeling states involve representation of bodily responses elicited by emotional events. Within this framework, individual differences in intensity of emotional experience reflect variation in sensitivity to internal bodily responses. We measured regional brain activity by functional magnetic resonance imaging (fMRI) during an interoceptive task wherein subjects judged the timing of their own heartbeats. We observed enhanced activity in insula, somatomotor and cingulate cortices. In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task. Furthermore, local gray matter volume in the same region correlated with both interoceptive accuracy and subjective ratings of visceral awareness. Indices of negative emotional experience correlated with interoceptive accuracy across subjects. These findings indicate that right anterior insula supports a representation of visceral responses accessible to awareness, providing a substrate for subjective feeling states.

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Figure 1: Task design.
Figure 2: Activity relating to interoceptive attention (second-level random effects analysis of 17 subjects, P < 0.02 corrected).
Figure 3: Functional neural correlates of interoceptive sensitivity.
Figure 4: Morphometric (gray matter) correlates of interoceptive sensitivity.
Figure 5: Gray matter correlates of measures of self-rated bodily awareness.

References

  1. Cameron, O.G. Interoception: the inside story—a model for psychosomatic processes. Psychosom. Med. 63, 697–710 (2001).

    Article  CAS  Google Scholar 

  2. Melmed, R.N. Mind, Body and Medicine (Oxford Univ. Press, Oxford, UK, 2002).

    Google Scholar 

  3. Jennings, J.R. & van der Molen, M.W. Cardiac timing and the central regulation of action. Psychol. Res. 66, 337–349 (2002).

    Article  Google Scholar 

  4. Jennings, J.R. Is it important that the mind is in a body? Inhibition and the heart. Psychophysiology 29, 369–383 (1992).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  6. Dolan, R.J. Emotion, cognition, and behavior. Science 298, 1191–1194 (2002).

    Article  CAS  Google Scholar 

  7. James, W. Physical basis of emotion. Psychol. Rev. 1, 516–529 (1894). Reprinted in Psychol. Rev. 101, 205–210 (1994).

    Article  Google Scholar 

  8. Lange, C. The Emotions (Williams & Wilkins, Baltimore, Maryland, 1922). Translated by I.A. Haupt; original work published 1885.

    Google Scholar 

  9. Whitehead, W.E., Drescher, V.M., Heiman, P. & Blackwell, B. Relation of heart rate control to heart beat perception. Biofeedback and Self Regulation 2, 371–392 (1977).

    Article  Google Scholar 

  10. Yates, A.J., Jones, K.E., Marie, G.V. & Hogben, J.H. Detection of the heart beat and events in the cardiac cycle. Psychophysiology 22, 561–567 (1985).

    Article  CAS  Google Scholar 

  11. Wiens, S. & Palmer, S.N. Quadratic trend analysis and heart beat detection. Biol. Psychol. 58, 159–175 (2001).

    Article  CAS  Google Scholar 

  12. Jones, G.E. Perception of visceral sensations: a review of recent findings, methodologies and future directions. in Advances in Psychophysiology Vol. 5 (eds. Jennings, J.R. et al.) 55–191 (Jessica Kingsley, London, 1994).

    Google Scholar 

  13. Ferguson, M.L. & Katkin, E.S. Visceral perception, anhedonia, and emotion. Biol. Psychol. 42, 131–145 (1996).

    Article  CAS  Google Scholar 

  14. Wiens, S., Mezzacappa, E. & Katkin, E.S. Heart beat detection and the experience of emotion. Cognit. Emotion 14, 417–427 (2000).

    Article  Google Scholar 

  15. Katkin, E.S., Wiens, S. & Ohman, A. Nonconscious fear conditioning, visceral perception, and the development of gut feelings. Psychol. Sci. 12, 366–370 (2001).

    Article  CAS  Google Scholar 

  16. Mumford, D.B. et al. The Bradford Somatic Inventory. A multi-ethnic inventory of somatic symptoms reported by anxious and depressed patients in Britain and the Indo-Pakistan subcontinent. Br. J. Psychiatry 158, 379–386 (1991).

    Article  CAS  Google Scholar 

  17. Ludwick-Rosenthal, R. & Neufeld, R.W. Heart beat interoception: a study of individual differences. Int. J. Psychophysiol. 3, 57–65 (1985).

    Article  CAS  Google Scholar 

  18. Ehlers, A. & Breuer, P. How good are patients with panic disorder at perceiving their heart beats? Biol. Psychol. 42, 165–182 (1996).

    Article  CAS  Google Scholar 

  19. Zoellner, L.A. & Craske, M.G. Interoceptive accuracy and panic. Behav. Res. Ther. 37, 141–158 (1999).

    Article  Google Scholar 

  20. Stewart, S.H., Buffett-Jerrott, S.E. & Kokaram, R. Heart beat awareness and heart rate reactivity in anxiety sensitivity: a further investigation. J. Anxiety Disord. 15, 535–553 (2001).

    Article  CAS  Google Scholar 

  21. Barsky, A.J. Palpitations, arrhythmias, and awareness of cardiac activity. Ann. Intern. Med. 134, 832–837 (2001).

    Article  CAS  Google Scholar 

  22. Van der Does, A.J.W., Antony, M.M., Ehlers, A. & Barsky, A.J. Heart beat perception in panic disorder: a reanalysis. Behav. Res. Ther. 38, 47–62 (2000).

    Article  Google Scholar 

  23. Craig, A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655–666 (2002).

    Article  CAS  Google Scholar 

  24. Critchley, H.D., Corfield, D.R., Chandler, M., Mathias, C.J. & Dolan, R.J. Cerebral correlates of peripheral cardiovascular arousal: a functional neuroimaging study. J. Physiol. 523, 259–270 (2000).

    Article  CAS  Google Scholar 

  25. Critchley, H.D., Mathias, C.J. & Dolan, R.J. Neural correlates of first and second-order representation of bodily states. Nat. Neurosci. 4, 207–212 (2001).

    Article  CAS  Google Scholar 

  26. Critchley, H.D., Mathias, C.J. & Dolan, R.J. Fear-conditioning in humans: the influence of awareness and arousal on functional neuroanatomy. Neuron 33, 653–663 (2002).

    Article  CAS  Google Scholar 

  27. Critchley, H.D. et al. Human cingulate cortex and autonomic cardiovascular control: converging neuroimaging and clinical evidence. Brain 216, 2139–2152 (2003).

    Article  Google Scholar 

  28. Cameron, O.G. & Minoshima, S. Regional brain activation due to pharmacologically induced adrenergic interoceptive stimulation in humans. Psychosom. Med. 64, 851–861 (2002).

    PubMed  Google Scholar 

  29. Harper, R.M., Bandler, R., Spriggs, D. & Alger, J.R. Lateralized and widespread brain activation during transient blood pressure elevation revealed by magnetic resonance imaging. J. Comp. Neurol. 417, 195–204 (2000).

    Article  CAS  Google Scholar 

  30. Aziz, Q., Schnitzler, A. & Enck, P. Functional neuroimaging of visceral sensation. J. Clin. Neurophysiol. 17, 604–612 (2000).

    Article  CAS  Google Scholar 

  31. Peyron, R. et al. Role of operculoinsular cortices in human pain processing: converging evidence from PET, fMRI, dipole modeling, and intracerebral recordings of evoked potentials. NeuroImage 17, 1336–1346 (2002).

    Article  CAS  Google Scholar 

  32. Craig, A.D., Chen, K., Bandy, D. & Reiman, E.M. Thermosensory activation of insular cortex. Nat. Neurosci. 3, 184–190 (2000).

    Article  CAS  Google Scholar 

  33. Phillips, M.L. et al. Neural responses to facial and vocal expressions of fear and disgust. Proc. R. Soc. Lond. B Biol. Sci. 265, 1809–1817 (1998).

    Article  CAS  Google Scholar 

  34. Buchel, 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  CAS  Google Scholar 

  35. Good, C.D., et al. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14, 21–36 (2001).

    Article  CAS  Google Scholar 

  36. Ashburner, J. & Friston, K.J. Voxel-based morphometry—the methods. Neuroimage 11, 805–821 (2000).

    Article  CAS  Google Scholar 

  37. Ashburner, J. & Friston, K.J. Why voxel-based morphometry should be used. Neuroimage 14, 1238–1243 (2001).

    Article  CAS  Google Scholar 

  38. Hamilton, M.C. Hamilton anxiety scale [HAMA]. in Sourcebook of Adult Assessment: Applied Clinical Psychology (eds. Schutte, N.S. & Malouff, J.M.) 154–157 (Plenum Press, New York, 1995).

    Google Scholar 

  39. Beck, A.T. & Steer, R.A. Manual for the Beck Depression Inventory (The Psychological Corporation, San Antonio, Texas, USA 1993).

    Google Scholar 

  40. Watson, D. Intra-individual and inter-individual analyses of positive and negative affect: their relation to health complaints, perceived stress, and daily activities. J. Personality Soc. Psychol. 54, 1020–1030 (1988).

    Article  CAS  Google Scholar 

  41. Porges, S. Body Perception Questionnaire (Laboratory of Developmental Assessment, University of Maryland, 1993).

    Google Scholar 

  42. Damasio, A.R. Descartes' Error (Putnam, New York, 1994).

    Google Scholar 

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

    Google Scholar 

  44. Friston, K. et al. Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapp. 2, 189–210 (1995).

    Article  Google Scholar 

  45. Friston, K. et al. Spatial registration and normalization of images. Human Brain Mapp. 2, 165–189 (1995).

    Article  Google Scholar 

  46. Ashburner, J., Neelin, P., Collins, D.L., Evans, A. & Friston, K. Incorporating prior knowledge into image registration. Neuroimage 6, 344–352 (1997).

    Article  CAS  Google Scholar 

  47. Genovese, C.R., Lazar N.A. & Nichols, T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870–878 (2002).

    Article  Google Scholar 

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Acknowledgements

This work was supported by a Wellcome Clinician Scientist Fellowship to H.D.C. and a Programme Grant to R.J.D.

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Authors and Affiliations

  1. Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, 12 Queen Square, London, WC1N 3BG, UK

    Hugo D Critchley, Pia Rotshtein & Raymond J Dolan

  2. Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London, WC1N 3AR, UK

    Hugo D Critchley

  3. Autonomic Unit, National Hospital for Neurology and Neurosurgery, University College London Hospitals, Queen Square, London, WC1N 3BG, UK

    Hugo D Critchley

  4. Department of Clinical Neuroscience, Psychology Section, Karolinska Hospital, Stockholm, SE-171 76, Sweden

    Stefan Wiens & Arne Öhman

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  1. Hugo D Critchley
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Correspondence to Hugo D Critchley.

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Critchley, H., Wiens, S., Rotshtein, P. et al. Neural systems supporting interoceptive awareness. Nat Neurosci 7, 189–195 (2004). https://doi.org/10.1038/nn1176

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