Mucosal stimulation activates secretomotor neurons via long myenteric pathways in guinea pig ileum

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 2, 2007, Pages

  Reed, David E ^a   Vanner, Stephen ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b HOTEL DIEU HOSPITAL   (Canada)

Author keywords

Secretion; Secretomotor reflexes; Submucosa

Indexed keywords

ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRODE; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GUINEA PIG; ILEUM; INTESTINE BLOOD FLOW; INTESTINE MOTILITY; INTESTINE SECRETION; MALE; MOTONEURON; MYENTERIC PLEXUS; NERVE CELL; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SENSORY STIMULATION;

ACTION POTENTIALS; ANIMALS; AUTONOMIC DENERVATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GUINEA PIGS; HEXAMETHONIUM; ILEUM; INHIBITORY POSTSYNAPTIC POTENTIALS; INTESTINAL MUCOSA; MALE; MOTOR NEURONS; MYENTERIC PLEXUS; PHORBOL 12,13-DIBUTYRATE; PROTEIN KINASE C; SEROTONIN; SUBMUCOUS PLEXUS;

EID: 33847022641     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00364.2006     Document Type: Article

References (43)

1. Alex G, Clerc N, Kunze WA, Furness JB. Responses of myenteric S neurones to low frequency stimulation of their synaptic inputs. Neuroscience 110: 361-373, 2002.
2. Bertrand PP, Kunze WA, Bornstein JC, Furness JB. Electrical mapping of the projections of intrinsic primary afferent neurones to the mucosa of the guinea-pig small intestine. Neurogastroenterol Motil 10: 533-541, 1998.
3. Bornstein JC, Costa M, Furness JB. Synaptic inputs to immunohistochemically identified neurones in the submucous plexus of the guinea-pig small intestine. J Physiol 381: 465-482, 1986.
4. Bornstein JC, Costa M, Furness JB. Intrinsic and extrinsic inhibitory synaptic inputs to submucous neurones of the guinea-pig small intestine. J Physiol 398: 371-390, 1988.
5. Brookes SJ. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262: 58-70, 2001.
6. Caren JF, Meyer JH, Grossman MI. Canine intestinal secretion during and after rapid distention of the small bowel. Am J Physiol 227: 183-188, 1974.
7. Carey HV, Cooke HJ, Zafirova M. Mucosal responses evoked by stimulation of ganglion cell somas in the submucosal plexus of the guinea-pig ileum. J Physiol 364: 69-79, 1985.
8. Chang EB, Rao MC. Intestinal water and electrolyte transport. In: Physiology of the Gastrointestinal Tract, edited by Johnson LR. New York: Raven, 1994, p. 2027-2081.
9. Clerc N, Furness JB. Intrinsic primary afferent neurones of the digestive tract 2. Neurogastroenterol Motil 16, Suppl 1: 24-27, 2004.
10. Clerc N, Gola M, Vogalis F, Furness JB. Controlling the excitability of IPANs: a possible route to therapeutics. Curr Opin Pharmacol 2: 657-664, 2002.
11. Cooke HJ. Neurotransmitters in neuronal reflexes regulating intestinal secretion. Ann NY Acad Sci 915: 77-80, 2000.
12. Cooke HJ. Influence of enteric cholinergic neurons on mucosal transport in guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 246: G263-G267, 1984.
13. Cooke HJ, Sidhu M, Wang YZ. Activation of 5-HT1P receptors on submucosal afferents subsequently triggers VIP neurons and chloride secretion in the guinea-pig colon. J Auton Nerv Syst 66: 105-110, 1997.
14. Costa M, Brookes SJ, Steele PA, Gibbins I, Burcher E, Kandiah CJ. Neurochemical classification of myenteric neurons in the guinea-pig ileum. Neuroscience 75: 949-967, 1996.
15. Costa M, Furness JB, Smith IJ, Davies B, Oliver J. An immunohistochemical study of the projections of somatostatin-containing neurons in the guinea-pig intestine. Neuroscience 5: 841-852, 1980.
16. Evans RJ, Jiang MM, Surprenant A. Morphological properties and projections of electrophysiologically characterized neurons in the guinea-pig submucosal plexus. Neuroscience 59: 1093-1110, 1994.
17. Foxx-Orenstein AE, Kuemmerle JF, Grider JR. Distinct 5-HT receptors mediate the peristaltic reflex induced by mucosal stimuli in human and guinea pig intestine. Gastroenterology 111: 1281-1290, 1996.
18. Furness JB, Costa M, Keast JR. Choline acetyltransferase- and peptide immunoreactivity of submucous neurons in the small intestine of the guinea-pig. Cell Tissue Res 237: 329-336, 1984.
19. Greenwood B, Davison JS. Role of extrinsic and intrinsic nerves in the relationship between intestinal motility and transmural potential difference in the anesthetized ferret. Gastroenterology 89: 1286-1292, 1985.
20. Grider JR, Foxx-Orenstein AE, Jin JG. 5-Hydroxytryptamine4 receptor agonists initiate the peristaltic reflex in human, rat, and guinea pig intestine. Gastroenterology 115: 370-380, 1998.
21. Hirst GD, McKirdy HC. Synaptic potentials recorded from some neurones of the submucous plexus of guinea-pig intestine. J Physiol 244: 35P-36P, 1975.
22. Hubel KA. The effects of electrical field stimulation and tetrodotoxin on ion transport by the isolated rabbit ileum. J Clin Invest 62: 1039-1047, 1978.
23. Hubel KA, Renquist KS, Varley G. Secretory reflexes in ileum and jejunum: absence of remote effects. J Auton Nerv Syst 35: 53-62, 1991.
24. Jodal M, Holmgren S, Lundgren O, Sjoqvist A. Involvement of the myenteric plexus in the cholera toxin-induced net fluid secretion in the rat small intestine. Gastroenterology 105: 1286-1293, 1993.
25. Kawai M, Nguyen TV, Stebbing MJ, Clerc N, Komori S, Furness JB. Comparison of the effects of phorbol dibutyrate and low-frequency stimulation of synaptic inputs on the excitability of myenteric AH neurons. Pflügers Arch 447: 298-304, 2003.
26. - secretion via afferent neurons and 5-HT4 receptors. Am J Physiol Gastrointest Liver Physiol 277: G515-G520, 1999.
27. Kunze WA, Bertrand PP, Furness JB, Bornstein JC. Influence of the mucosa on the excitability of myenteric neurons. Neuroscience 76: 619-634, 1997.
28. Meedeniya AC, Brookes SJ, Hennig GW, Costa M. The projections of 5-hydroxytryptamine-accumulating neurones in the myenteric plexus of the small intestine of the guinea-pig. Cell Tissue Res 291: 375-384, 1998.
29. Moore BA, Vanner S. Properties of synaptic inputs from myenteric neurons innervating submucosal S neurons in guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 278: G273-G280, 2000.
30. Neunlist M, Frieling T, Rupprecht C, Schemann M. Polarized enteric submucosal circuits involved in secretory responses of the guinea-pig proximal colon. J Physiol 506: 539-550, 1998.
31. Nguyen TV, Stebbing MJ, Clerc N, Kawai M, Harvey JR, Furness JB. Evidence for protein kinase involvement in long-term postsynaptic excitation of intrinsic primary afferent neurons in the intestine. Auton Neurosci 115: 1-6, 2004.
32. Pan H, Gershon MD. Activation of intrinsic afferent pathways in submucosal ganglia of the guinea pig small intestine. J Neurosci 20: 3295-3309, 2000.
33. Read NW, Smallwood RH, Levin RJ, Holdsworth CD, Brown BH. Relationship between changes in intraluminal pressure and transmural potential difference in the human and canine jejunum in vivo. Gut 18: 141-151, 1977.
34. Reed DE, Vanner SJ. Converging and diverging cholinergic inputs from submucosal neurons amplify activity of secretomotor neurons in guinea-pig ileal submucosa. Neuroscience 107: 685-696, 2001.
35. Reed DE, Vanner SJ. Long vasodilator reflexes projecting through the myenteric plexus in guinea-pig ileum. J Physiol 553: 911-924, 2003.
36. Sidhu M, Cooke HJ. Role for 5-HT and ACh in submucosal reflexes mediating colonic secretion. Am J Physiol Gastrointest Liver Physiol 269: G346-G351, 1995.
37. Song ZM, Brookes SJ, Costa M. Projections of specific morphological types of neurons within the myenteric plexus of the small intestine of the guinea-pig. Cell Tissue Res 285: 149-156, 1996.
38. Song ZM, Brookes SJ, Steele PA, Costa M. Projections and pathways of submucous neurons to the mucosa of the guinea-pig small intestine. Cell Tissue Res 269: 87-98, 1992.
39. Surprenant A. Two types of neurones lacking synaptic input in the submucous plexus of guinea-pig small intestine. J Physiol 351: 363-378, 1984.
40. Tonini M, Costa M. A pharmacological analysis of the neuronal circuitry involved in distension-evoked enteric excitatory reflex. Neuroscience 38: 787-795, 1990.
41. Vanner S. Myenteric neurons activate submucosal vasodilator neurons in guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 279: G380-G387, 2000.
42. Vanner S, Macnaughton WK. Submucosal secretomotor and vasodilator reflexes. Neurogastroenterol Motil 16, Suppl 1: 39-43, 2004.
43. Weber E, Neunlist M, Schemann M, Frieling T. Neural components of distension-evoked secretory responses in the guinea-pig distal colon. J Physiol 536: 741-751, 2001.