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Neuroanatomical basis for first- and second-order representations of bodily states
Open accessAbstract
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 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
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Metadata
- 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.
- Venue
- Nature Neuroscience
- Published
- 2001-02
- Volume
- 4
- Issue
- 2
- Pages
- 207-212
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- 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
- bronze
- doi.org
- 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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