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Cited by 312Psychosomatic Disorders and Their TreatmentsHeart Rate Variability and Autonomic ControlNeural and Behavioral Psychology Studies

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

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Critchley, H. D., Mathias, C. J., Dolan, R. J.·2001·Nature Neuroscience
DOI 10.1038/84048
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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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  • A functioning peripheral nervous system is not required for a person to experience a core affective state, provided they have prior experiences that give them central nervous system representations of bodily states.

    “A functioning peripheral nervous system is not necessary for a person to experience a core affective state (e.g., Critchley et al. 2001) as long as they have some prior experiences to provide them with central nervous system representations of bodily states.”

    From The brain basis of emotion: a meta-analytic review (2012) · cites this paper as Critchley et al. 2001

    The Discussion (page unavailable) says that people with acquired peripheral autonomic failure may avoid major emotional deficits partly because established representations can reduce dependence on direct peripheral feedback. But the study concerns autonomic failure, not loss of a functioning peripheral nervous system altogether; it also identifies intact non-autonomic sensory pathways and other bodily responses as reasons emotional deficits may be limited. Prior experience alone is therefore not established as sufficient. (LLM, conf=0.87)

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1 of the 43 references couldn’t be matched to a known paper.

Research works printed but not linked: 3

  1. Mathias C. J. & Bannister, R.) 169-195 (Oxford Univ. Press, Oxford, 1999).
  2. Mathias C. J. & Bannister, R.) 169-195 (Oxford Univ. Press, Oxford, 1999).
  3. Mathias C. J. & Bannister, R.) 45-55 (Oxford Univ. Press, Oxford 1999).

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Authors
Critchley, H. D., Mathias, C. J., & Dolan, R. J.
Affiliations
  • UCL Queen Square Institute of Neurology (GB)
  • St Mary's Hospital (GB)
Corresponding author
Dolan, R. J.
ORCID
Venue
Nature Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2001-02
Volume
4
Issue
2
Pages
207-212
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
DOI
10.1038/84048
OpenAlex
W1510737382
Cited by
312
References
43
Citations by year
2026: 1 · 2025: 3 · 2024: 9 · 2023: 10 · 2022: 8 · 2021: 14 · 2020: 20 · 2019: 14 · 2018: 10 · 2017: 9 · 2016: 8 · 2015: 12 · 2014: 8 · 2013: 13 · 2012: 14
FWCI
10.88
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • Max Planck Digital Library (submittedVersion, other-oa)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
  • Wellcome Trust
  • Brain Research Trust
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Psychosomatic Disorders and Their Treatments
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
bodily states, autonomic nervous system, autonomic failure, dorsal pons, cingulate cortex, medial parietal cortex, emotional experience, afferent feedback, hierarchical representation, pure autonomic failure
MeSH terms
Aged, Autonomic Nervous System Diseases, Brain, Emotions, Female, Gyrus Cinguli, Humans, Male, Mathematics, Middle Aged, Models, Neurological, Parietal Lobe, Pons, Reference Values, Stress, Physiological, Hand Strength

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