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. 2002 Jul;51(Suppl 1):i6–i10. doi: 10.1136/gut.51.suppl_1.i6

Prevertebral ganglia and intestinofugal afferent neurones

J Szurszewski, L Ermilov, S Miller
PMCID: PMC1867710  PMID: 12077055

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Figure 1 .

Figure 1

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Schematic diagram of the possible arrangement of mechanosensory afferent neurones. The intestinofugal afferent neurones (IFANs) function in an "in parallel" arrangement to the circular muscle fibres whereas intrinsic primary afferent neurones (IPANs) function in an "in series" arrangement. The physiological stimulus of the rectospinal neurones has not been identified.41,42 They may participate in the defecation reflex and are included here for completeness. DRG, dorsal root ganglion; NG, nodose ganglion; PSN, preganglionic sympathetic neurone; PVG, prevertebral ganglion.

Figure 2 .

Figure 2

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Schematic diagram of mechanosensory afferent neurones synapsing with prevertebral ganglion neurones. Pathway 1 is comprised of neurones with cell bodies in the myenteric plexus. Activation of these neurones evokes fast nicotinic excitatory postsynaptic potentials and vasoactive intestinal peptide dependent slow excitatory postsynaptic potentials in inferior mesenteric ganglion/superior mesenteric ganglion (IMG/SMG) neurones. Pathway 2 is comprised of neurones with cell bodies in the dorsal root ganglia. Activation of this pathway leads to release of substance P (SP) and calcitonin gene related peptide (CGRP) from the axon collaterals,20 and to slow excitatory synaptic potentials. IFAN, intestinofugal afferent neurone; MG, myenteric ganglion; MN, motor neurone; NA, noradrenergic neurone.

Figure 3 .

Figure 3

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Relationship between spontaneous circular muscle contraction, intraluminal pressure, and mechanosensory afferent synaptic input to a sympathetic neurone in the mouse superior mesenteric ganglion. Note that during "receptive relaxation" prior to contraction, there is an increase in the frequency of excitatory synaptic input whereas the frequency of synaptic input markedly declines at peak intraluminal pressure and contraction. These data suggest that the mechanosensory nerve fibres function as "in parallel" receptors. All recordings were made simultaneously in vitro.

Figure 4 .

Figure 4

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Examples of the shapes of two retrogradely labelled colonic myenteric neurones revealed by application of the fluorescent dye DiI to the lumbar colonic nerve of the guinea pig. Neurones were imaged with a confocal laser scanning microscope and reconstructed using ANALYZE image processing software. Fifty optical sections in 1 µm step increments were made to reconstruct the neurone in (A), and 41 sections in 1 µm step increments were made to reconstruct the neurone in (B). The arrow in (B) indicates the orientation of the circular muscle layer. Calibration bars are 50 µm.

Selected References

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

  1. Andrews P. L. Vagal afferent innervation of the gastrointestinal tract. Prog Brain Res. 1986;67:65–86. doi: 10.1016/s0079-6123(08)62757-0. [DOI] [PubMed] [Google Scholar]
  2. Barbiers M., Timmermans J. P., Adriaensen D., De Groodt-Lasseel M. H., Scheuermann D. W. Topographical distribution and immunocytochemical features of colonic neurons that project to the cranial mesenteric ganglion in the pig. J Auton Nerv Syst. 1993 Aug-Sep;44(2-3):119–127. doi: 10.1016/0165-1838(93)90024-o. [DOI] [PubMed] [Google Scholar]
  3. Berthoud H. R., Powley T. L. Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol. 1992 May 8;319(2):261–276. doi: 10.1002/cne.903190206. [DOI] [PubMed] [Google Scholar]
  4. Crowcroft P. J., Holman M. E., Szurszewski J. H. Excitatory input from the distal colon to the inferior mesenteric ganglion in the guinea-pig. J Physiol. 1971 Dec;219(2):443–461. doi: 10.1113/jphysiol.1971.sp009671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Doerffler-Melly J., Neuhuber W. L. Rectospinal neurons: evidence for a direct projection from the enteric to the central nervous system in the rat. Neurosci Lett. 1988 Oct 5;92(2):121–125. doi: 10.1016/0304-3940(88)90046-8. [DOI] [PubMed] [Google Scholar]
  6. Félix B., Catalin D., Miolan J. P., Niel J. P. Integrative properties of the major pelvic ganglion in the rat. J Auton Nerv Syst. 1998 Mar 3;69(1):6–11. doi: 10.1016/s0165-1838(97)00133-1. [DOI] [PubMed] [Google Scholar]
  7. Gebhart G. F. Visceral polymodal receptors. Prog Brain Res. 1996;113:101–112. [PubMed] [Google Scholar]
  8. Grundy D. Speculations on the structure/function relationship for vagal and splanchnic afferent endings supplying the gastrointestinal tract. J Auton Nerv Syst. 1988 Apr;22(3):175–180. doi: 10.1016/0165-1838(88)90104-x. [DOI] [PubMed] [Google Scholar]
  9. King B. F., Szurszewski J. H. Mechanoreceptor pathways from the distal colon to the autonomic nervous system in the guinea-pig. J Physiol. 1984 May;350:93–107. doi: 10.1113/jphysiol.1984.sp015190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kressel M., Radespiel-Tröger M. Anterograde tracing and immunohistochemical characterization of potentially mechanosensitive vagal afferents in the esophagus. J Comp Neurol. 1999 Sep 13;412(1):161–172. doi: 10.1002/(sici)1096-9861(19990913)412:1<161::aid-cne12>3.0.co;2-y. [DOI] [PubMed] [Google Scholar]
  11. Kunze W. A., Clerc N., Bertrand P. P., Furness J. B. Contractile activity in intestinal muscle evokes action potential discharge in guinea-pig myenteric neurons. J Physiol. 1999 Jun 1;517(Pt 2):547–561. doi: 10.1111/j.1469-7793.1999.0547t.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kunze W. A., Furness J. B., Bertrand P. P., Bornstein J. C. Intracellular recording from myenteric neurons of the guinea-pig ileum that respond to stretch. J Physiol. 1998 Feb 1;506(Pt 3):827–842. doi: 10.1111/j.1469-7793.1998.827bv.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leek B. F. Abdominal and pelvic visceral receptors. Br Med Bull. 1977 May;33(2):163–168. doi: 10.1093/oxfordjournals.bmb.a071417. [DOI] [PubMed] [Google Scholar]
  14. Lomax A. E., Sharkey K. A., Bertrand P. P., Low A. M., Bornstein J. C., Furness J. B. Correlation of morphology, electrophysiology and chemistry of neurons in the myenteric plexus of the guinea-pig distal colon. J Auton Nerv Syst. 1999 Apr 16;76(1):45–61. doi: 10.1016/s0165-1838(99)00008-9. [DOI] [PubMed] [Google Scholar]
  15. Lomax A. E., Zhang J. Y., Furness J. B. Origins of cholinergic inputs to the cell bodies of intestinofugal neurons in the guinea pig distal colon. J Comp Neurol. 2000 Jan 24;416(4):451–460. doi: 10.1002/(sici)1096-9861(20000124)416:4<451::aid-cne3>3.0.co;2-e. [DOI] [PubMed] [Google Scholar]
  16. Ma R. C., Szurszewski J. H. Modulation by opioid peptides of mechanosensory pathways supplying the guinea-pig inferior mesenteric ganglion. J Physiol. 1996 Mar 1;491(Pt 2):435–445. doi: 10.1113/jphysiol.1996.sp021227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ma R. C., Szurszewski J. H. Release of calcitonin gene-related peptide in guinea pig inferior mesenteric ganglion. Peptides. 1996;17(1):161–170. doi: 10.1016/0196-9781(95)02064-0. [DOI] [PubMed] [Google Scholar]
  18. Mann P. T., Furness J. B., Pompolo S., Mäder M. Chemical coding of neurons that project from different regions of intestine to the coeliac ganglion of the guinea pig. J Auton Nerv Syst. 1995 Dec 5;56(1-2):15–25. doi: 10.1016/0165-1838(95)00053-1. [DOI] [PubMed] [Google Scholar]
  19. Mazet B., Miller S. M., Szurszewski J. H. Electrophysiological effects of nitric oxide in mouse superior mesenteric ganglion. Am J Physiol. 1996 Feb;270(2 Pt 1):G324–G331. doi: 10.1152/ajpgi.1996.270.2.G324. [DOI] [PubMed] [Google Scholar]
  20. Mazet B., Miolan J. P., Niel J. P., Julé Y., Roman C. Modulation of synaptic transmission in the rabbit coeliac ganglia by gastric and duodenal mechanoreceptors. Neuroscience. 1989;32(1):235–243. doi: 10.1016/0306-4522(89)90122-x. [DOI] [PubMed] [Google Scholar]
  21. Mazet B., Miolan J. P., Niel J. P., Roman C. New insights into the organization of a gastroduodenal inhibitory reflex by the coeliac plexus. J Auton Nerv Syst. 1994 Jan-Feb;46(1-2):135–146. doi: 10.1016/0165-1838(94)90150-3. [DOI] [PubMed] [Google Scholar]
  22. McDonald F. J., Price M. P., Snyder P. M., Welsh M. J. Cloning and expression of the beta- and gamma-subunits of the human epithelial sodium channel. Am J Physiol. 1995 May;268(5 Pt 1):C1157–C1163. doi: 10.1152/ajpcell.1995.268.5.C1157. [DOI] [PubMed] [Google Scholar]
  23. Messenger J. P., Furness J. B. Distribution of enteric nerve cells projecting to the superior and inferior mesenteric ganglia of the guinea-pig. Cell Tissue Res. 1993 Feb;271(2):333–339. doi: 10.1007/BF00318620. [DOI] [PubMed] [Google Scholar]
  24. Miller S. M., Szurszewski J. H. Colonic mechanosensory afferent input to neurons in the mouse superior mesenteric ganglion. Am J Physiol. 1997 Feb;272(2 Pt 1):G357–G366. doi: 10.1152/ajpgi.1997.272.2.G357. [DOI] [PubMed] [Google Scholar]
  25. Miolan J. P., Niel J. P. The mammalian sympathetic prevertebral ganglia: integrative properties and role in the nervous control of digestive tract motility. J Auton Nerv Syst. 1996 May 6;58(3):125–138. doi: 10.1016/0165-1838(95)00128-x. [DOI] [PubMed] [Google Scholar]
  26. Neuhuber W. L., Appelt M., Polak J. M., Baier-Kustermann W., Abelli L., Ferri G. L. Rectospinal neurons: cell bodies, pathways, immunocytochemistry and ultrastructure. Neuroscience. 1993 Sep;56(2):367–378. doi: 10.1016/0306-4522(93)90338-g. [DOI] [PubMed] [Google Scholar]
  27. Neuhuber W. L. Sensory vagal innervation of the rat esophagus and cardia: a light and electron microscopic anterograde tracing study. J Auton Nerv Syst. 1987 Oct;20(3):243–255. doi: 10.1016/0165-1838(87)90153-6. [DOI] [PubMed] [Google Scholar]
  28. Parkman H. P., Ma R. C., Stapelfeldt W. H., Szurszewski J. H. Direct and indirect mechanosensory pathways from the colon to the inferior mesenteric ganglion. Am J Physiol. 1993 Sep;265(3 Pt 1):G499–G505. doi: 10.1152/ajpgi.1993.265.3.G499. [DOI] [PubMed] [Google Scholar]
  29. Phillips R. J., Baronowsky E. A., Powley T. L. Afferent innervation of gastrointestinal tract smooth muscle by the hepatic branch of the vagus. J Comp Neurol. 1997 Jul 28;384(2):248–270. [PubMed] [Google Scholar]
  30. Sengupta J. N., Kauvar D., Goyal R. K. Characteristics of vagal esophageal tension-sensitive afferent fibers in the opossum. J Neurophysiol. 1989 May;61(5):1001–1010. doi: 10.1152/jn.1989.61.5.1001. [DOI] [PubMed] [Google Scholar]
  31. Sharkey K. A., Lomax A. E., Bertrand P. P., Furness J. B. Electrophysiology, shape, and chemistry of neurons that project from guinea pig colon to inferior mesenteric ganglia. Gastroenterology. 1998 Oct;115(4):909–918. doi: 10.1016/s0016-5085(98)70263-x. [DOI] [PubMed] [Google Scholar]
  32. Stapelfeldt W. H., Szurszewski J. H. Central neurotensin nerves modulate colo-colonic reflex activity in the guinea-pig inferior mesenteric ganglion. J Physiol. 1989 Apr;411:347–365. doi: 10.1113/jphysiol.1989.sp017577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stapelfeldt W. H., Szurszewski J. H. Neurotensin facilitates release of substance P in the guinea-pig inferior mesenteric ganglion. J Physiol. 1989 Apr;411:325–345. doi: 10.1113/jphysiol.1989.sp017576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stapelfeldt W. H., Szurszewski J. H. The electrophysiological effects of neurotensin on neurones of guinea-pig prevertebral sympathetic ganglia. J Physiol. 1989 Apr;411:301–323. doi: 10.1113/jphysiol.1989.sp017575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Timmermans J. P., Barbiers M., Scheuermann D. W., Stach W., Adriaensen D., De Groodt-Lasseel M. H. Occurrence, distribution and neurochemical features of small intestinal neurons projecting to the cranial mesenteric ganglion in the pig. Cell Tissue Res. 1993 Apr;272(1):49–58. doi: 10.1007/BF00323570. [DOI] [PubMed] [Google Scholar]
  36. Trudrung P., Furness J. B., Pompolo S., Messenger J. P. Locations and chemistries of sympathetic nerve cells that project to the gastrointestinal tract and spleen. Arch Histol Cytol. 1994 May;57(2):139–150. doi: 10.1679/aohc.57.139. [DOI] [PubMed] [Google Scholar]
  37. Wang F. B., Powley T. L. Topographic inventories of vagal afferents in gastrointestinal muscle. J Comp Neurol. 2000 Jun 5;421(3):302–324. [PubMed] [Google Scholar]
  38. Weems W. A., Szurszewski J. H. An intracellular analysis of some intrinsic factors controlling neural output from inferior mesenteric ganglion of guinea pigs. J Neurophysiol. 1978 Mar;41(2):305–321. doi: 10.1152/jn.1978.41.2.305. [DOI] [PubMed] [Google Scholar]
  39. Zagorodnyuk V. P., Chen B. N., Brookes S. J. Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol. 2001 Jul 1;534(Pt 1):255–268. doi: 10.1111/j.1469-7793.2001.00255.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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