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Neuroanatomical basis for first- and second-order representations of bodily states

Nature Neuroscience volume 4, pages 207–212 (2001)Cite this article

Abstract

Changes in bodily states, particularly those mediated by the autonomic nervous system, are crucial to ongoing emotional experience. A theoretical model proposes a first-order autoregulatory representation of bodily state at the level of dorsal pons, and a second-order experience-dependent re-mapping of changes in bodily state within structures such as cingulate and medial parietal cortices. We tested these anatomical predictions using positron emission tomography and a human neurological model (pure autonomic failure), in which peripheral autonomic denervation prevents the emergence of autonomic responses. Compared to controls, we observed task-independent differences in activity of dorsal pons and context-induced differences in cingulate and medial parietal activity in PAF patients. An absence of afferent feedback concerning autonomically generated bodily states was associated with subtle impairments of emotional responses in PAF patients. Our findings provide empirical support for a theory proposing a hierarchical representation of bodily states.

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Figure 1: Physiological changes during task performance.
Figure 2: Increased activity in pons in PAF subjects.
Figure 3: Between-group differences in activity: interaction with effort.

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Acknowledgements

This work was supported by a Programme Grant to R.J.D. from the Wellcome Trust. H.D.C. is supported by a Clinical Research Fellowship from the Brain Research Trust.

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Authors and Affiliations

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

    H. D. Critchley & R. J. Dolan

  2. Autonomic Unit, National Hospital for Neurology & Neurosurgery and Institute of Neurology, University College London, Queen Square, London, WC1N 3BG, UK

    H. D. Critchley & C. J. Mathias

  3. Neurovascular Medicine Unit, Saint Mary's Hospital, ICSM, Praed Street, London, W2 1NY, UK

    C. J. Mathias

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  1. H. D. Critchley
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Correspondence to R. J. Dolan.

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Critchley, H., Mathias, C. & Dolan, R. Neuroanatomical basis for first- and second-order representations of bodily states. Nat Neurosci 4, 207–212 (2001). https://doi.org/10.1038/84048

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