The role of vagal visceral afferents in the control of nociception
Abstract
We have shown that activity in subdiaphragmatic vagal afferents modulates mechanical hyperalgesic behavior in the rat. Subdiaphragmatic vagotomy decreases paw-withdrawal threshold to mechanical stimulation (baseline and after intradermal injection of bradykinin), thus enhancing mechanical hyperalgesic behavior. Most of this decrease is generated by an endocrine signal released by the adrenal medullae because denervation or removal of the adrenal medullae prevents or reverses these changes. This novel mechanism may imply that: (a) the brain is able to regulate sensitivity of nociceptors all over the body by a neuroendocrine mechanisms, (b) sensitivity of nociceptors can be influenced by changes in parts of the body which are remote from the location of the sensitized nociceptors and (c) circulating catecholamines can influence nociceptors in a way which is different from those reported so far (see Jänig and McLachlan, 1994; Jänig, 1996a; Jänig et al., 1996).
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The celiac branch of the vagus nerve innervates the small intestine.
“The celiac branch of the vagus nerve innervates the small intestine, and a prominent role of afferents of this branch in the modulation of experimental knee-joint inflammation and pain sensitivity has been reported.74”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [74]
A prominent role of afferents of the celiac branch of the vagus nerve in the modulation of experimental knee-joint inflammation and pain sensitivity has been reported.
“The celiac branch of the vagus nerve innervates the small intestine, and a prominent role of afferents of this branch in the modulation of experimental knee-joint inflammation and pain sensitivity has been reported.74”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [74]
Cites
The american college of rheumatology 1990 criteria for the classification of fibromyalgia
Wolfe, F., Smythe, H. A., Yunus, M. B., Bennett, R. M., Bombardier, C., Goldenberg, D. L., Tugwell, P., Campbell, S. M., Abeles, M., Clark, P., et al. (1990) · Arthritis & Rheumatism · doi:10.1002/art.1780330203 · Cited by 9,563 · see citing works
Physiology of the Gastrointestinal Tract
Johnson, L. R. (2006) · Elsevier eBooks · doi:10.1016/b978-0-12-088394-3.x5000-4 · Cited by 4,611 · see citing works
Central regulation of autonomic functions
(1991) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(91)90107-h · Cited by 1,115 · see citing works
Peripheral and central mechanisms of cutaneous hyperalgesia
Treede, R., Meyer, R. A., Raja, S. N., & Campbell, J. N. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90027-c · Cited by 917 · see citing works
Ericsson, A. B., Kovacs, K., & Sawchenko, P. E. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00897.1994 · Cited by 684 · see citing works
Watkins, L. R., Maier, S. F., & Goehler, L. E. (1995) · Pain · doi:10.1016/0304-3959(95)00186-7 · Cited by 659 · see citing works
Cytokine-to-brain communication: A review & analysis of alternative mechanisms
Watkins, L. R., Maier, S. F., & Goehler, L. E. (1995) · Life Sciences · doi:10.1016/0024-3205(95)02047-m · Cited by 597 · see citing works
Watkins, L. R., Goehler, L. E., Relton, J. K., Tartaglia, N., Silbert, L., Martin, D., & Maier, S. F. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(94)11105-r · Cited by 516 · see citing works
Characterization of cytokine-induced hyperalgesia
Watkins, L. R., Wiertelak, E. P., Goehler, L. E., Smith, K. P., Martin, D., & Maier, S. F. (1994) · Brain Research · doi:10.1016/0006-8993(94)91566-0 · Cited by 502 · see citing works
Topography of efferent vagal innervation of the rat gastrointestinal tract
Berthoud, H., Carlson, N. R., & Powley, T. L. (1991) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1991.260.1.r200 · Cited by 363 · see citing works
Neural and biochemical mediators of endotoxin and stress-induced c-fos expression in the rat brain
Wan, W., Wetmore, L., Sorensen, C. M., Greenberg, A. H., & Nance, D. M. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90179-1 · Cited by 325 · see citing works
Layé, S., Bluthé, R.-M., Kent, S., Combe, C., Medina, C. F., Parnet, P., Kelley, K., & Dantzer, R. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.268.5.r1327 · Cited by 303 · see citing works
The fiber composition of the abdominal vagus of the rat
Prechtl, J. C., & Powley, T. L. (1990) · Anatomy and Embryology · doi:10.1007/bf00198950 · Cited by 299 · see citing works
Vagal afferent modulation of nociception
Randich, A., & Gebhart, G. F. (1992) · Brain Research Reviews · doi:10.1016/0165-0173(92)90009-b · Cited by 298 · see citing works
Neurocircuitry of illness-induced hyperalgesia
Watkins, L. R., Wiertelak, E. P., Goehler, L. E., Mooney-Heiberger, K., Martinez, J., Furness, L. E., Smith, K. P., & Maier, S. F. (1994) · Brain Research · doi:10.1016/0006-8993(94)91742-6 · Cited by 284 · see citing works
Kress, M., Koltzenburg, M., Reeh, P. W., et al. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.2.581 · Cited by 261 · see citing works
Niijima, A. (1996) · Journal of the Autonomic Nervous System · doi:10.1016/s0165-1838(96)00098-7 · Cited by 261 · see citing works
Characteristics of function-specific pathways in the sympathetic nervous system
Jänig, W., & McLachlan, E. M. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90092-m · Cited by 261 · see citing works
Self-citationJänig, W., Levine, J. D., & Michaelis, M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61087-0 · Cited by 260 · see citing works
Self-citationStreltzer, J. (2001) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v62n0814c · Cited by 260 · see citing works
Kwiat, G. C., & Basbaum, A. I. (1992) · Somatosensory & Motor Research · doi:10.3109/08990229209144768 · Cited by 235 · see citing works
Jänig, W. (1985) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/bfb0034086 · Cited by 235 · see citing works
Self-citationMeller, S. T., & Gebhart, G. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90398-l · Cited by 234 · see citing works
Mechanisms of tumor necrosis factor-α (TNF-α) hyperalgesia
Watkins, L. R., Goehler, L. E., Relton, J. K., Brewer, M. T., & Maier, S. F. (1995) · Brain Research · doi:10.1016/0006-8993(95)00715-3 · Cited by 226 · see citing works
Bret-Dibat, J. L., Bluthé, R.-M., Kent, S., KELLEY, K. W., & Dantzer, R. (1995) · Brain Behavior and Immunity · doi:10.1006/brbi.1995.1023 · Cited by 224 · see citing works
Berthoud, H., Kressel, M., Raybould, H., & Neuhuber, W. (1995) · Anatomy and Embryology · doi:10.1007/bf00187819 · Cited by 216 · see citing works
Neurobiology of visceral afferent neurons: neuroanatomy, functions, organ regulations and sensations
Jänig, W. (1996) · Biological Psychology · doi:10.1016/0301-0511(95)05145-7 · Cited by 198 · see citing works
Self-citationSensory afferents from the gastrointestinal tract
Grundy, D., & Scratcherd, T. (1989) · Comprehensive physiology · doi:10.1002/cphy.cp060116 · Cited by 190 · see citing works
Blockade of lipopolysaccharide-induced fever by subdiaphragmatic vagotomy in guinea pigs
SEHIC, E., & Blatteis, C. M. (1996) · Brain Research · doi:10.1016/0006-8993(96)00326-5 · Cited by 186 · see citing works
Mense, S., & Meyer, H. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017028 · Cited by 160 · see citing works
Fever: How May Circulating Pyrogens Signal the Brain?
Cm, B., & SEHIC, E. (1997) · Physiology · doi:10.1152/physiologyonline.1997.12.1.1 · Cited by 147 · see citing works
Doe, W. F. (1989) · Gut · doi:10.1136/gut.30.12.1679 · Cited by 121 · see citing works
Richards, W., Hillsley, K., Eastwood, C., & Grundy, D. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021781 · Cited by 117 · see citing works
Sensitization of articular afferents to mechanical stimuli by bradykinin
Neugebauer, V., Schaible, H., & Schmidt, R. F. (1989) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00370884 · Cited by 116 · see citing works
Yeomans, D. C., Clark, F. M., Paice, J. A., & Proudfit, H. K. (1992) · Pain · doi:10.1016/0304-3959(92)90098-v · Cited by 115 · see citing works
Berthoud, H., Patterson, L. M., Willing, A. E., Mueller, K., & Neuhuber, W. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01222-x · Cited by 111 · see citing works
Taiwo, Y. O., & Levine, J. D. (1988) · Brain Research · doi:10.1016/0006-8993(88)90487-8 · Cited by 107 · see citing works
Self-citationSILENT AFFERENTS: A SEPARATE CLASS OF PRIMARY AFFERENTS?
Michaelis, M., Häbler, H., & Jänig, W. (1996) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1996.tb02579.x · Cited by 103 · see citing works
Self-citationVagotomy-Induced Enhancement of Mechanical Hyperalgesia in the Rat Is Sympathoadrenal-Mediated
Khasar, S. G., Miao, F. J., Jänig, W., et al. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-08-03043.1998 · Cited by 102 · see citing works
Self-citationSub-diaphragmatic vagal afferent integration of meal-related gastrointestinal signals
Schwartz, G. J., & Moran, T. H. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00039-h · Cited by 102 · see citing works
Production of Hyperalgesic Prostaglandins by Sympathetic Postganglionic Neurons
Gonzales, R., Goldyne, M. E., Taiwo, Y. O., & Levine, J. D. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb08557.x · Cited by 89 · see citing works
Self-citationSuppression of meal size by intestinal nutrients is eliminated by celiac vagal deafferentation
Walls, E. K., Phillips, R. J., Wang, F., Holst, M., & Powley, T. L. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.269.6.r1410 · Cited by 84 · see citing works
Khasar, S. G., Miao, F. J., Jänig, W., et al. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00030.x · Cited by 76 · see citing works
Self-citationRole of sympathetic postganglionic neurons in synovial plasma extravasation induced by bradykinin
Miao, F. J., Jänig, W., & Levine, J. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.2.715 · Cited by 57 · see citing works
Self-citationNeural: Mediation of food aversions and anorexia induced by tumor necrosis factor and tumors
Bernstein, I. L. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00046-h · Cited by 57 · see citing works
Khasar, S. G., Miao, F. J., & Levine, J. D. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00280-v · Cited by 54 · see citing works
Self-citationThe ultrastructure and permeability of tracheobronchial blood vessels in health and disease.
McDonald, D. M. (1990) · PubMed · Cited by 52 · see citing works
Green, P. G., Jänig, W., & Levine, J. D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-09-03234.1997 · Cited by 51 · see citing works
Self-citationForeman, R. D. (1989) · Progress in sensory physiology · doi:10.1007/978-3-642-74058-9_1 · Cited by 50 · see citing works
Vagal modulation of nociception
Gebhart, G. F., & Randich, A. (1992) · APS Journal · doi:10.1016/s1058-9139(06)80007-0 · Cited by 47 · see citing works
Selective vagal rhizotomies: a new dorsal surgical approach used for intestinal deafferentations
Walls, E. K., Wang, F. B., Holst, M., Phillips, R. J., Voreis, J. S., Perkins, A. R., Pollard, L., & Powley, T. L. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.269.5.r1279 · Cited by 47 · see citing works
Jarry, H., Düker, E., & Wuttke, W. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90589-0 · Cited by 44 · see citing works
Neurobiology of the autonomic nervous system
Jänig, W., & McLachlan, E. M. (2013) · Oxford University Press eBooks · doi:10.1093/med/9780198566342.003.0003 · Cited by 44 · see citing works
Self-citationComparison of intradermal and subcutaneous hyperalgesic effects of inflammatory mediators in the rat
Khasar, S. G., Green, P. G., & Levine, J. D. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90325-f · Cited by 42 · see citing works
Self-citationMiao, F. J., Jänig, W., & Levine, J. D. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp021873 · Cited by 42 · see citing works
Self-citationPain arising from the urogenital tract
Jänig, W., & Koltzenburg, M. (1992) · UCL Discovery (University College London) · Cited by 39 · see citing works
Self-citationChapter 4 Spinal cord reflex organization of sympathetic systems
Jänig, W. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61858-0 · Cited by 38 · see citing works
Self-citationSympathetic-dependence in bradykinin-induced synovial plasma extravasation is dose-related
Miao, F. J., Green, P. G., Coderre, T. J., et al. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12403-4 · Cited by 37 · see citing works
Self-citationMiao, F. J., Jänig, W., Green, P. G., & Levine, J. D. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.3.1285 · Cited by 29 · see citing works
Self-citationTaché, Y., Wingate, D. L., & Burks, T. F. (1993) · Cited by 18 · see citing works
Sympathetic control of adrenal secretion of enkephalins after hemorrhage in awake dogs
Engeland, W. C., Bereiter, D. A., & Gann, D. S. (1986) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1986.251.2.r341 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · see citing works
Browning, K. N., & Travagli, R. A. (2014) · Comprehensive Physiology · doi:10.1002/cphy.c130055 · Cited by 541 · see citing works
Giamberardino, M. A., Berkley, K. J., Affaitati, G., Lerza, R., Centurione, L., Lapenna, D., & Vecchiet, L. (2002) · Pain · doi:10.1016/s0304-3959(01)00405-5 · Cited by 114 · see citing works
- Authors
- Jänig, W., Khasar, S. G., Miao, F. J.-P., & Levine, J. D.
- Affiliations
- Christian-Albrechts-Universität zu Kiel (DE)
- National Institutes of Health (US)
- Corresponding author
- Jänig, W.
- Venue
- Progress in Brain Research
- Publisher
- Elsevier
- Published
- 2000
- Volume
- 122
- Pages
- 273-287
- ISSN
- 0079-6123 (ISSN-L)
- OpenAlex
- W2908175543
- Cited by
- 70
- References
- 61
- Citations by year
- 2024: 4 · 2022: 2 · 2021: 2 · 2020: 2 · 2018: 1 · 2016: 2 · 2015: 1 · 2014: 5 · 2013: 2
- FWCI
- 17.65
- Type
- book chapter
- Language
- en
- Open access
- closed
- Locations
- Progress in brain research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR32634)
- Topics
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- nociception, mechanical hyperalgesia, subdiaphragmatic vagotomy, bradykinin, adrenal medulla, catecholamines, neuroendocrine regulation, brain-gut interaction
- MeSH terms
- Animals, Brain, Neural Pathways, Pain, Vagus Nerve, Visceral Afferents
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review