Electrophysiological evidence for distinct vagal pathways mediating CCK‐evoked motor effects in the proximal versus distal stomach
Open accessAbstract
Intravenous cholecystokinin octapeptide (CCK-8) elicits vago-vagal reflexes that inhibit phasic gastric contractions and reduce gastric tone in urethane-anaesthetized rats. A discrete proximal subdivision of the ventral gastric vagus nerve (pVGV) innervates the proximal stomach, but the fibre populations within it have not been characterized previously.We hypothesized that I.V. CCK-8 injection would excite inhibitory efferent outflow in the pVGV, in contrast to its inhibitory effect on excitatory efferent outflow in the distal subdivision (dVGV), which supplies the distal stomach. In each VGV subdivision, a dual-recording technique was used to record afferent and efferent activity simultaneously, while also monitoring intragastric pressure (IGP). CCK-8 dose dependently (100-1000 pmol kg(-1), I.V.) reduced gastric tone, gastric contractile activity and multi-unit dVGV efferent discharge, but increased pVGV efferent firing. Single-unit analysis revealed a minority of efferent fibres in each branch whose response differed in direction from the bulk response. Unexpectedly, efferent excitation in the pVGV was significantly shorter lived and had a significantly shorter decay half-time than did efferent inhibition in the dVGV, indicating that distinct pathways drive CCK-evoked outflow to the proximal vs. the distal stomach. Efferent inhibition in the dVGV began several seconds before, and persisted significantly longer than, simultaneously recorded dVGV afferent excitation.Thus, dVGV afferent excitation could not account for the pattern of dVGV efferent inhibition. However, the time course of dVGV afferent excitation paralleled that of pVGV efferent excitation. Similarly, the duration of CCK-8-evoked afferent responses recorded in the accessory celiac branch of the vagus (ACV) matched the duration of dVGV efferent responses. The observed temporal relationships suggest that postprandial effects on gastric complicance of CCK released from intestinal endocrine cells may require circulating concentrations to rise to levels capable of exciting distal gastric afferent fibres, in contrast to more immediate effects on distal gastric contractile activity mediated via vago-vagal reflexes initiated by paracrine excitation of intestinal afferents.
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Gut peptides in the systemic circulation can bind cognate receptors on immune cells and vagus nerve terminals, thereby enabling indirect gut-brain communication.
“Gut peptides in the systemic circulation can bind cognate receptors on immune cells and vagus nerve terminals thereby enabling indirect gut-brain communication.”
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Niijima, A., Hatanaka, S., & Furuhama, K. (1996) · Journal of Autonomic Pharmacology · doi:10.1111/j.1474-8673.1996.tb00356.x · Cited by 11 · see citing works
Sources of anterior gastric vagal efferent discharge in rats: an electrophysiological study
Wei, J. Y., Tache, Y., & Kruger, L. (1992) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(92)90142-4 · Cited by 8 · see citing works
Adelson, D. W., Kosoyan, H. P., Wang, Y., et al. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01143.2006 · Cited by 7 · see citing works
Self-citationThe Anatomic Basis for the Variable Adequacy of Incomplete Vagotomy
Legros, G., & Griffith, C. A. (1968) · Annals of Surgery · doi:10.1097/00000658-196812000-00014 · Cited by 7 · see citing works
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Anxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · see citing works
Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells
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El Aidy, S., Dinan, T. G., & Cryan, J. F. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.03.002 · Cited by 215 · see citing works
Potential gut–brain mechanisms behind adverse mental health outcomes of bariatric surgery
Brown, R. M., Guerrero-Hreins, E., Brown, W. A., le Roux, C. W., & Sumithran, P. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00520-2 · Cited by 49 · see citing works
- Authors
- Okano‐Matsumoto, S., McRoberts, J. A., Taché, Y., & Adelson, D. W.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Adelson, David W.
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2011-01-14
- Volume
- 589
- Issue
- 2
- Pages
- 371-393
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC3043539
- OpenAlex
- W1517423134
- Cited by
- 30
- References
- 104
- Citations by year
- 2026: 1 · 2025: 1 · 2022: 1 · 2021: 5 · 2020: 2 · 2019: 4 · 2018: 1 · 2017: 1 · 2016: 3 · 2015: 3 · 2014: 1 · 2013: 3 · 2012: 1
- FWCI
- 2.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 41301, R21DK074736, P30DK041301)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- CCK-8, vago-vagal reflex, gastric motility, gastric tone, gastric contractility, efferent inhibition, intragastric pressure
- MeSH terms
- Analysis of Variance, Animals, Dose-Response Relationship, Drug, Electrophysiology, Male, Neurons, Efferent, Sincalide, Stomach, Vagus Nerve, Rats, Sprague-Dawley, Rats
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 ›
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