Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2004 Jan 1;554(Pt 1):227-35.
doi: 10.1113/jphysiol.2003.056804.

Mechanosensitive duodenal afferents contribute to vagal modulation of inflammation in the rat

Frederick Jia-Pei Miao  1 , Paul G Green, Jon D Levine
Affiliations

Mechanosensitive duodenal afferents contribute to vagal modulation of inflammation in the rat

Frederick Jia-Pei Miao et al. J Physiol. .

Abstract

Noxious stimuli inhibit inflammation by activating neuroendocrine stress axes, an effect that is potently attenuated by ongoing activity in subdiaphragmatic vagal afferents. Because this vagal afferent activity is carried in the coeliac and coeliac accessory branches of the subdiaphragmatic vagus, we tested the hypothesis that the activity arises from vagal afferents that innervate a proximal segment of the gastrointestinal tract. Surgical removal of the duodenum, but not the stomach, produces a marked (six orders of magnitude) leftward shift in the dose-response curve for intraplantar capsaicin-induced inhibition of synovial plasma extravasation induced by the potent inflammatory mediator bradykinin, in the knee joint; this is similar in magnitude to the inhibition produced by subdiaphragmatic or by coeliac plus coeliac accessory branch vagotomy. Fasting, to unload mechanically sensitive polymodal afferents in the proximal gastrointestinal tract, produces a similar leftward shift in the dose-response curve for the inhibitory effect of capsaicin, an effect that is reversed by balloon distension in the duodenum in fasted rats, while balloon distension postvagotomy had no effect. These results suggest that activation of mechanically sensitive vagal afferents in the duodenum contributes vagal afferent activity that modulates neuroendocrine control of the inflammatory response.

PubMed Disclaimer

Figures

Figure 1
Figure 1. Effect of subdiaphragmatic vagotomy on the depression of bradykinin-induced plasma extravasation in the knee joint of the rat by intradermal capsaicin in the plantar skin of the hind paw
Depression of bradykinin-induced plasma extravasation during stimulation of nociceptors in the plantar skin of the hind paw by capsaicin (3, 10 and 30 μg intradermal (i.d.)) in sham-vagotomised rats (○) and in rats in which the subdiaphragmatic vagus nerves were cut, immediately prior to the experiment (•).
Figure 2
Figure 2. Effect of electrical stimulation of the proximal end of the cut subdiaphragmatic vagus nerve on vagotomy-induced enhancement of the depression of bradykinin-induced plasma extravasation by cumulative dosing with intradermal capsaicin
Subselective coeliac plus coeliac accessory branch vagotomy induces a marked enhancement of capsaicin (3, 10 and 30 μg, i.d.) induced inhibition of bradykinin plasma extravasation (half-filled circles) compared to sham vagotomy controls (○ from Fig. 1); the enhancement produced by coeliac plus coeliac accessory subdiaphragmatic vagotomy was similar to that produced by complete subdiaphragmatic vagotomy (• from Fig. 1). Electrical stimulation of the proximal end of the cut subdiaphragmatic vagus (s) completely reversed the effect of subdiaphragmatic vagotomy.
Figure 3
Figure 3. Effect of surgical excision of the stomach or duodenum on the depression of bradykinin-induced plasma extravasation by intradermal capsaicin
Bradykinin-induced plasma extravasation during stimulation of nociceptors in the hind paw with capsaicin (3, 10, 30 and 100 μg i.d.) after gastrectomy (□) or after duodenectomy (▪), compared to sham vagotomy (○ from Fig. 1) and vagotomy (• from Fig. 1). Gastrectomy had no effect on the dose–response curve for capsaicin-induced inhibition of bradykinin plasma extravasation compared to control vagus intact rats, while duodenectomy enhanced capsaicin inhibition of bradykinin plasma extravasation. The magnitude of the enhancement of the effect of capsaicin by duodenectomy was similar to the magnitude of the effect of subdiaphragmatic vagotomy.
Figure 4
Figure 4. Effect of 48 h fasting from solid food on the depression of bradykinin-induced plasma extravasation by intradermal capsaicin in the hind paw
>The depression of bradykinin plasma extravasation by the intraplantar injection of capsaicin (3, 10 and 30 μg i.d.) in rats that were fasted for 48 h (t) was enhanced, compared to fed rats (○ from Fig. 1). The magnitude of enhancement induced by fasting was similar to the magnitude of that induced by subdiaphragmatic vagotomy (•; from Fig. 1).
Figure 5
Figure 5. Effect of duodenal balloon distension, in 48-h fasted rats
Depression of bradykinin plasma extravasation by intraplantar capsaicin (3, 10 and 30 μg I.d.) in 48-h fasted rats (t from Fig. 4) was reversed by distension of a balloon in the duodenum (♦). Selective coeliac and accessory coeliac branch vagotomy (⋄) markedly reduced the effect of balloon distention.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Andrews PL. Vagal afferent innervation of the gastrointestinal tract. Prog Brain Res. 1986;67:65–86. - PubMed
    1. Berthoud HR, Carlson NR, Powley TL. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol. 1991;260:R200–207. - PubMed
    1. Berthoud HR, Kressel M, Neuhuber WL. An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol. 1992;186:431–442. - PubMed
    1. Blackshaw LA, Grundy D. Effects of cholecystokinin (cck-8) on two classes of gastroduodenal vagal afferent fibre. J Auton Nerv Syst. 1990;31:191–201. - PubMed
    1. Bluthe RM, Walter V, Parnet P, Laye S, Lestage J, Verrier D, Poole S, Stenning BE, Kelley KW, Dantzer R. Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C R Acad Sci III. 1994;317:499–503. - PubMed

Publication types

LinkOut - more resources