Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Jan 15;498(Pt 2):473–481. doi: 10.1113/jphysiol.1997.sp021873

Vagal branches involved in inhibition of bradykinin-induced synovial plasma extravasation by intrathecal nicotine and noxious stimulation in the rat.

F J Miao 1, W Jänig 1, J D Levine 1
PMCID: PMC1159216  PMID: 9032694

Abstract

1. Stimulation of cutaneous and spinal visceral nociceptive afferents and intrathecal nicotine reduces bradykinin-induced plasma extravasation (BK-induced PE) in the knee joint of the rat. This depression is mediated by the hypothalamo-pituitary-adrenal (HPA) axis and is potentiated by subdiaphragmatic vagotomy. It is believed that activity in vagal afferents tonically inhibits ascending impulse transmission in the neuraxis projecting to the hypothalamus. Vagotomy, by removing such inhibition, allows greater depression of BK-induced PE. In this study we determined whether the vagal afferents which negatively regulate activities of the HPA axis are present in all branches of the abdominal vagus nerves or only in specific branches. 2. We measured the depression of BK-induced PE elicited by graded stimulation of spinal visceral afferents with intraperitoneal capsaicin and by intrathecal nicotine in vagus-intact rats and in rats in which specific vagal branches were selectively interrupted. (i) Interruption of the coeliac branches mimicked the effect of total subdiaphragmatic vagotomy in potentiating the depression of BK-induced PE generated by intrathecal nicotine and by stimulation of spinal visceral afferents. (ii) Interruption of the gastric and hepatic branches of the abdominal vagus nerves together or individually did not affect the depression of BK-induced PE generated by the two stimuli. 3. These results indicate that afferent activity in coeliac and accessory coeliac vagal branches is involved in the regulation of the nociceptive system-initiated depression of BK-induced PE. The afferent fibres in these vagal branches involved probably monitor physiological events in abdominal visceral organs.

Full text

PDF
473

Images in this article

479Figure 4
on p.479

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bahns E., Ernsberger U., Jänig W., Nelke A. Discharge properties of mechanosensitive afferents supplying the retroperitoneal space. Pflugers Arch. 1986 Nov;407(5):519–525. doi: 10.1007/BF00657510. [DOI] [PubMed] [Google Scholar]
  2. Bahns E., Ernsberger U., Jänig W., Nelke A. Functional characteristics of lumbar visceral afferent fibres from the urinary bladder and the urethra in the cat. Pflugers Arch. 1986 Nov;407(5):510–518. doi: 10.1007/BF00657509. [DOI] [PubMed] [Google Scholar]
  3. Berthoud H. R., Carlson N. R., Powley T. L. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol. 1991 Jan;260(1 Pt 2):R200–R207. doi: 10.1152/ajpregu.1991.260.1.R200. [DOI] [PubMed] [Google Scholar]
  4. Berthoud H. R., Kressel M., Raybould H. E., Neuhuber W. L. Vagal sensors in the rat duodenal mucosa: distribution and structure as revealed by in vivo DiI-tracing. Anat Embryol (Berl) 1995 Mar;191(3):203–212. doi: 10.1007/BF00187819. [DOI] [PubMed] [Google Scholar]
  5. Bessou P., Perl E. R. Amovement receptor of the small intestine. J Physiol. 1966 Jan;182(2):404–426. doi: 10.1113/jphysiol.1966.sp007829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blumberg H., Haupt P., Jänig W., Kohler W. Encoding of visceral noxious stimuli in the discharge patterns of visceral afferent fibres from the colon. Pflugers Arch. 1983 Jun;398(1):33–40. doi: 10.1007/BF00584710. [DOI] [PubMed] [Google Scholar]
  7. Bueno L., Gue M., Fargeas M. J., Alvinerie M., Junien J. L., Fioramonti J. Vagally mediated inhibition of acoustic stress-induced cortisol release by orally administered kappa-opioid substances in dogs. Endocrinology. 1989 Apr;124(4):1788–1793. doi: 10.1210/endo-124-4-1788. [DOI] [PubMed] [Google Scholar]
  8. CARR J., WILHELM D. L. THE EVALUATION OF INCREASED VASCULAR PERMEABILITY IN THE SKIN OF GUINEA-PIGS. Aust J Exp Biol Med Sci. 1964 Aug;42:511–522. doi: 10.1038/icb.1964.48. [DOI] [PubMed] [Google Scholar]
  9. Coderre T. J., Basbaum A. I., Levine J. D. Neural control of vascular permeability: interactions between primary afferents, mast cells, and sympathetic efferents. J Neurophysiol. 1989 Jul;62(1):48–58. doi: 10.1152/jn.1989.62.1.48. [DOI] [PubMed] [Google Scholar]
  10. Coupland R. E., Parker T. L., Kesse W. K., Mohamed A. A. The innervation of the adrenal gland. III. Vagal innervation. J Anat. 1989 Apr;163:173–181. [PMC free article] [PubMed] [Google Scholar]
  11. Fleming W. W., Westfall D. P., De la Lande I. S., Jellett L. B. Log-normal distribution of equiefective doses of norepinephrine and acetylcholine in several tissues. J Pharmacol Exp Ther. 1972 May;181(2):339–345. [PubMed] [Google Scholar]
  12. González-Fernández I., Gonzalo-Sanz L. M. Vagal influence on the adrenocortical function of the rat. Rev Esp Fisiol. 1987 Jun;43(2):203–207. [PubMed] [Google Scholar]
  13. Green P. G., Miao F. J., Jänig W., Levine J. D. Negative feedback neuroendocrine control of the inflammatory response in rats. J Neurosci. 1995 Jun;15(6):4678–4686. doi: 10.1523/JNEUROSCI.15-06-04678.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Haupt P., Jänig W., Kohler W. Response pattern of visceral afferent fibres, supplying the colon, upon chemical and mechanical stimuli. Pflugers Arch. 1983 Jun;398(1):41–47. doi: 10.1007/BF00584711. [DOI] [PubMed] [Google Scholar]
  15. Mense S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain. 1993 Sep;54(3):241–289. doi: 10.1016/0304-3959(93)90027-M. [DOI] [PubMed] [Google Scholar]
  16. Miao F. J., Green P. G., Coderre T. J., Jänig W., Levine J. D. Sympathetic-dependence in bradykinin-induced synovial plasma extravasation is dose-related. Neurosci Lett. 1996 Mar 1;205(3):165–168. doi: 10.1016/0304-3940(96)12403-4. [DOI] [PubMed] [Google Scholar]
  17. Miao F. J., Jänig W., Dallman M. F., Benowitz N. L., Heller P. H., Basbaum A. I., Levine J. D. Role of vagal afferents and spinal pathways modulating inhibition of bradykinin-induced plasma extravasation by intrathecal nicotine. J Neurophysiol. 1994 Sep;72(3):1199–1207. doi: 10.1152/jn.1994.72.3.1199. [DOI] [PubMed] [Google Scholar]
  18. Miao F. J., Jänig W., Green P. G., Levine J. D. Inhibition of bradykinin-induced synovial plasma extravasation produced by intrathecal nicotine is mediated by the hypothalamopituitary adrenal axis. J Neurophysiol. 1996 Nov;76(5):2813–2821. doi: 10.1152/jn.1996.76.5.2813. [DOI] [PubMed] [Google Scholar]
  19. Miao F. J., Jänig W., Levine J. d. Role of sympathetic postganglionic neurons in synovial plasma extravasation induced by bradykinin. J Neurophysiol. 1996 Feb;75(2):715–724. doi: 10.1152/jn.1996.75.2.715. [DOI] [PubMed] [Google Scholar]
  20. Miao F. J., Lee T. J. Effects of bilirubin on cerebral arterial tone in vitro. J Cereb Blood Flow Metab. 1989 Oct;9(5):666–674. doi: 10.1038/jcbfm.1989.94. [DOI] [PubMed] [Google Scholar]
  21. Norgren R., Smith G. P. Central distribution of subdiaphragmatic vagal branches in the rat. J Comp Neurol. 1988 Jul 8;273(2):207–223. doi: 10.1002/cne.902730206. [DOI] [PubMed] [Google Scholar]
  22. Prechtl J. C., Powley T. L. Organization and distribution of the rat subdiaphragmatic vagus and associated paraganglia. J Comp Neurol. 1985 May 8;235(2):182–195. doi: 10.1002/cne.902350204. [DOI] [PubMed] [Google Scholar]
  23. Prechtl J. C., Powley T. L. The fiber composition of the abdominal vagus of the rat. Anat Embryol (Berl) 1990;181(2):101–115. doi: 10.1007/BF00198950. [DOI] [PubMed] [Google Scholar]
  24. Ritter S., Dinh T. T. Capsaicin-induced neuronal degeneration: silver impregnation of cell bodies, axons, and terminals in the central nervous system of the adult rat. J Comp Neurol. 1988 May 1;271(1):79–90. doi: 10.1002/cne.902710109. [DOI] [PubMed] [Google Scholar]
  25. Schaible H. G., Grubb B. D. Afferent and spinal mechanisms of joint pain. Pain. 1993 Oct;55(1):5–54. doi: 10.1016/0304-3959(93)90183-P. [DOI] [PubMed] [Google Scholar]
  26. Schwartz G. J., Moran T. H. CCK elicits and modulates vagal afferent activity arising from gastric and duodenal sites. Ann N Y Acad Sci. 1994 Mar 23;713:121–128. doi: 10.1111/j.1749-6632.1994.tb44058.x. [DOI] [PubMed] [Google Scholar]
  27. Schwartz G. J., Moran T. H. Sub-diaphragmatic vagal afferent integration of meal-related gastrointestinal signals. Neurosci Biobehav Rev. 1996;20(1):47–56. doi: 10.1016/0149-7634(95)00039-h. [DOI] [PubMed] [Google Scholar]
  28. Walls E. K., Phillips R. J., Wang F. B., Holst M. C., Powley T. L. Suppression of meal size by intestinal nutrients is eliminated by celiac vagal deafferentation. Am J Physiol. 1995 Dec;269(6 Pt 2):R1410–R1419. doi: 10.1152/ajpregu.1995.269.6.R1410. [DOI] [PubMed] [Google Scholar]
  29. Walls E. K., Wang F. B., Holst M. C., Phillips R. J., Voreis J. S., Perkins A. R., Pollard L. E., Powley T. L. Selective vagal rhizotomies: a new dorsal surgical approach used for intestinal deafferentations. Am J Physiol. 1995 Nov;269(5 Pt 2):R1279–R1288. doi: 10.1152/ajpregu.1995.269.5.R1279. [DOI] [PubMed] [Google Scholar]
  30. Watkins L. R., Maier S. F., Goehler L. E. Cytokine-to-brain communication: a review & analysis of alternative mechanisms. Life Sci. 1995;57(11):1011–1026. doi: 10.1016/0024-3205(95)02047-m. [DOI] [PubMed] [Google Scholar]
  31. Watkins L. R., Maier S. F., Goehler L. E. Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain. 1995 Dec;63(3):289–302. doi: 10.1016/0304-3959(95)00186-7. [DOI] [PubMed] [Google Scholar]
  32. Yaksh T. L., Rudy T. A. Studies on the direct spinal action of narcotics in the production of analgesia in the rat. J Pharmacol Exp Ther. 1977 Aug;202(2):411–428. [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES