Visceral afferents - Determinants and modulation of excitability

Autonomic Neuroscience: Basic and Clinical

Volumn 153, Issue 1-2, 2010, Pages 69-78

  Beyak, Michael J ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Excitability; Ion channels; Pharmacology; Visceral afferent

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; CARBON MONOXIDE; G PROTEIN COUPLED RECEPTOR; HYDROGEN SULFIDE; ION CHANNEL; METABOTROPIC RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEINASE ACTIVATED RECEPTOR; PURINERGIC P2X RECEPTOR; SEROTONIN; SOMATOSTATIN; VANILLOID RECEPTOR; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

BLADDER INNERVATION; GASTROINTESTINAL TRACT; HUMAN; INFLAMMATION; INTESTINE INNERVATION; MICROENVIRONMENT; NERVE ENDING; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SATIETY; SENSORY NERVE; VISCERA;

HORMONES; ION CHANNEL GATING; ION CHANNELS; MEMBRANE POTENTIALS; NEURONS, AFFERENT; NEUROTRANSMITTER AGENTS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PROTEINASE-ACTIVATED; VISCERAL AFFERENTS;

EID: 73949124819     PISSN: 15660702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.autneu.2009.07.019     Document Type: Review

References (105)

1. Abbott C.R., Monteiro M., Small C.J., Sajedi A., Smith K.L., Parkinson J.R., Ghatei M.A., and Bloom S.R. The inhibitory effects of peripheral administration of peptide YY (3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway. Brain Res. 1044 (2005) 127-131
2. Aerssens J., Hillsley K., Peeters P.J., de H.R., Stanisz A., Lin J.H., Van dW I., Gohlmann H.W., Grundy D., Stead R.H., and Coulie B. Alterations in the brain-gut axis underlying visceral chemosensitivity in Nippostrongylus brasiliensis-infected mice. Gastroenterology 132 (2007) 1375-1387
3. Amadesi S., Cottrell G.S., Divino L., Chapman K., Grady E.F., Bautista F., Karanjia R., Barajas-Lopez C., Vanner S., Vergnolle N., and Bunnett N.W. Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon- and A-dependent mechanisms in rats and mice. J. Physiol. 575 (2006) 555-571
4. Berthoud H.R., and Neuhuber W.L. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci. 85 (2000) 1-17
5. Beyak M.J., Ramji N., Krol K.M., Kawaja M.D., and Vanner S.J. Two TTX-resistant Na+ currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am. J. Physiol.: Gastrointest. Liver Physiol. 287 (2004) G845-G855
6. Beyak M., Bulmer D.C., Jiang W., Keating C., Rong W., and Grundy D. Sensory afferent nerves innervating the gastrointestinal tract. In: Johnson L.R. (Ed). Physiology of the Gastrointestinal Tract (2006), Elsevier Press, New York
7. Beyak M.J., Surprenant A., and Grundy D. Stimulation of CCK-1 receptors activates a TRPC like inward current in GI vagal afferent neurons. Gastroenterology 130 4 (2006) A74 (Ref Type: Abstract)
8. Beyak M.J., Bulmer D.C., Sellers D., and Grundy D. Impairment of rectal afferent mechanosensitivity in experimental diabetes in the rat. Neurogastroenterol. Motil. 21 6 (2009) 678-681
9. Bielefeldt K., and Davis B.M. Differential effects of ASIC3 and TRPV1 deletion on gastroesophageal sensation in mice. Am. J. Physiol.: Gastrointest. Liver Physiol. 294 (2008) G130-G138
10. Bielefeldt K., Ozaki N., and Gebhart G.F. Experimental ulcers alter voltage-sensitive sodium currents in rat gastric sensory neurons. Gastroenterology 122 (2002) 394-405
11. Bielefeldt K., Ozaki N., and Gebhart G.F. Mild gastritis alters voltage-sensitive sodium currents in gastric sensory neurons in rats. Gastroenterology 122 (2002) 752-761
12. Black J.A., Cummins T.R., Yoshimura N., de Groat W.C., and Waxman S.G. Tetrodotoxin-resistant sodium channels Na (v)1.8/SNS and Na (v)1.9/NaN in afferent neurons innervating urinary bladder in control and spinal cord injured rats. Brain Res. 963 (2003) 132-138
13. Blackshaw L.A., and Grundy D. Effects of cholecystokinin (CCK-8) on two classes of gastroduodenal vagal afferent fibre. J. Auton. Nerv. Syst. 31 (1990) 191-201
14. Blackshaw L.A., and Gebhart G.F. The pharmacology of gastrointestinal nociceptive pathways. Curr. Opin. Pharmacol. 2 (2002) 642-649
15. Blackshaw L.A., Brookes S.J., Grundy D., and Schemann M. Sensory transmission in the gastrointestinal tract. Neurogastroenterol. Motil. 19 (2007) 1-19
16. Blackshaw L.A., Smid S.D., O'Donnell T.A., and Dent J. GABA (B) receptor-mediated effects on vagal pathways to the lower oesophageal sphincter and heart. Br. J. Pharmacol. 130 (2000) 279-288
17. Booth C.E., Kirkup A.J., Hicks G.A., Humphrey P.P., and Grundy D. Somatostatin sst (2) receptor-mediated inhibition of mesenteric afferent nerves of the jejunum in the anesthetized rat. Gastroenterology 121 (2001) 358-369
18. Brierley S.M., Page A.J., Hughes P.A., Adam B., Liebregts T., Cooper N.J., Holtmann G., Liedtke W., and Blackshaw L.A. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 134 (2008) 2059-2069
19. Brouns I., Adriaensen D., Burnstock G., and Timmermans J.P. Intraepithelial vagal sensory nerve terminals in rat pulmonary neuroepithelial bodies express P2X (3) receptors. Am. J. Respir. Cell Mol. Biol. 23 (2000) 52-61
20. Bucinskaite V., Tolessa T., Pedersen J., Rydqvist B., Zerihun L., Holst J.J., and Hellstrom P.M. Receptor-mediated activation of gastric vagal afferents by glucagon-likepeptide-1 in the rat. Neurogastroenterol. Motil. 21 9 (2009) 978-984
21. Burdyga G., Lal S., Spiller D., Jiang W., Thompson D., Attwood S., Saeed S., Grundy D., Varro A., Dimaline R., and Dockray G.J. Localization of orexin-1 receptors to vagal afferent neurons in the rat and humans. Gastroenterology 124 (2003) 129-139
22. Buyse M., Ovesjo M.L., Goiot H., Guilmeau S., Peranzi G., Moizo L., Walker F., Lewin M.J., Meister B., and Bado A. Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur. J. Neurosci. 14 (2001) 64-72
23. Caruana B.J., Wald A., Hinds J.P., and Eidelman B.H. Anorectal sensory and motor function in neurogenic fecal incontinence. Comparison between multiple sclerosis and diabetes mellitus. Gastroenterology 100 (1991) 465-470
24. Castelucci P., Robbins H.L., and Furness J.B. P2X (2) purine receptor immunoreactivity of intraganglionic laminar endings in the mouse gastrointestinal tract. Cell Tissue Res. 312 (2003) 167-174
25. Cockayne D.A., Dunn P.M., Zhong Y., Rong W., Hamilton S.G., Knight G.E., Ruan H.Z., Ma B., Yip P., Nunn P., McMahon S.B., Burnstock G., and Ford A.P. P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J. Physiol. 567 (2005) 621-639
26. Coelho A.M., Ossovskaya V., and Bunnett N.W. Proteinase-activated receptor-2: physiological and pathophysiological roles. Curr. Med. Chem. Cardiovasc. Hematol. Agents 1 (2003) 61-72
27. Cottrell G.S., Amadesi S., Schmidlin F., and Bunnett N. Protease-activated receptor 2: activation, signalling and function. Biochem. Soc. Trans. 31 (2003) 1191-1197
28. Covasa M., Grahn J., and Ritter R.C. High fat maintenance diet attenuates hindbrain neuronal response to CCK. Regul. Pept. 86 (2000) 83-88
29. Covasa M., Grahn J., and Ritter R.C. Reduced hindbrain and enteric neuronal response to intestinal oleate in rats maintained on high-fat diet. Auton. Neurosci. 84 (2000) 8-18
30. Cox J.E., and Randich A. CCK-8 activates hepatic vagal C-fiber afferents. Brain Res. 776 (1997) 189-194
31. Daly D., Rong W., Chess-Williams R., Chapple C., and Grundy D. Bladder afferent sensitivity in wild-type and TRPV1 knockout mice. J. Physiol. 583 (2007) 663-674
32. Dang K., Bielefeldt K., and Gebhart G.F. Gastric ulcers reduce A-type potassium currents in rat gastric sensory ganglion neurons. Am. J. Physiol.: Gastrointest. Liver Physiol. 286 (2004) G573-G579
33. Dang K., Bielfeldt K., Lamb K., and Gebhart G.F. Gastric ulcers evoke hyperexcitability and enhance P2X receptor function in rat gastric sensory neurons. J. Neurophysiol. 93 (2005) 3112-3119
34. Dang K., Lamb K., Cohen M., Bielefeldt K., and Gebhart G.F. Cyclophosphamide-induced bladder inflammation sensitizes and enhances P2X receptor function in rat bladder sensory neurons. J. Neurophysiol. 99 (2008) 49-59
35. Date Y., Murakami N., Toshinai K., Matsukura S., Niijima A., Matsuo H., Kangawa K., and Nakazato M. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology 123 (2002) 1120-1128
36. De Schepper H.U., De Winter B.Y., Van N.L., Timmermans J.P., Herman A.G., Pelckmans P.A., and De Man J.G. TRPV1 receptors on unmyelinated C-fibres mediate colitis-induced sensitization of pelvic afferent nerve fibres in rats. J. Physiol. 586 (2008) 5247-5258
37. Distrutti E., Sediari L., Mencarelli A., Renga B., Orlandi S., Antonelli E., Roviezzo F., Morelli A., Cirino G., Wallace J.L., and Fiorucci S. Evidence that hydrogen sulfide exerts antinociceptive effects in the gastrointestinal tract by activating KATP channels. J. Pharmacol. Exp. Ther. 316 (2006) 325-335
38. Fang X., Djouhri L., McMullan S., Berry C., Waxman S.G., Okuse K., and Lawson S.N. Intense isolectin-B4 binding in rat dorsal root ganglion neurons distinguishes C-fiber nociceptors with broad action potentials and high Nav1.9 expression. J. Neurosci. 26 (2006) 7281-7292
39. Gaisano G., and Beyak M. The GLP-1 agonist exendin-4 excites nodose ganglion neurons and inhibits voltage-gated potassium currents. Gastroenterology 132 4 (suppl2) (2007) A36 (Ref Type: Abstract)
40. Gallego D., Clave P., Donovan J., Rahmati R., Grundy D., Jimenez M., and Beyak M.J. The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum. Neurogastroenterol. Motil. 20 (2008) 1306-1316
41. Gladman M.A., Aziz Q., Scott S.M., Williams N.S., and Lunniss P.J. Rectal hyposensitivity: pathophysiological mechanisms. Neurogastroenterol. Motil. 21 (2009) 508-5
42. Hay M., and Kunze D.L. An intermediate conductance calcium-activated potassium channel in rat visceral sensory afferent neurons. Neurosci. Lett. 167 (1994) 179-182
43. Hay M., and Kunze D.L. Calcium-activated potassium channels in rat visceral sensory afferents. Brain Res. 639 (1994) 333-336
44. Hicks G.A., Coldwell J.R., Schindler M., Ward P.A., Jenkins D., Lynn P.A., Humphrey P.P., and Blackshaw L.A. Excitation of rat colonic afferent fibres by 5-HT (3) receptors. J. Physiol. 544 (2002) 861-869
45. Hille B. Classical biophysics of the squid giant axon. Ion Channels of Excitable Membranes (2001), Sinauer Associates, Sunderland 25-59
46. Hillsley K., and Grundy D. Sensitivity to 5-hydroxytryptamine in different afferent subpopulations within mesenteric nerves supplying the rat jejunum. J. Physiol. 509 Pt 3 (1998) 717-727
47. Hillsley K., Kirkup A.J., and Grundy D. Direct and indirect actions of 5-hydroxytryptamine on the discharge of mesenteric afferent fibres innervating the rat jejunum. J. Physiol. 506 Pt 2 (1998) 551-561
48. Hillsley K., Lin J.H., Stanisz A., Grundy D., Aerssens J., Peeters P.J., Moechars D., Coulie B., and Stead R.H. Dissecting the role of sodium currents in visceral sensory neurons in a model of chronic hyperexcitability using Nav1.8 and Nav1.9 null mice. J. Physiol. 576 (2006) 257-267
49. Hu Y., Dong L., Sun B., Guillon M.A., Burbach L.R., Nunn P.A., Liu X., Vilenski O., Ford A.P., Zhong Y., and Rong W. The role of metabotropic glutamate receptor mGlu5 in control of micturition and bladder nociception. Neurosci. Lett. 450 (2009) 12-17
50. Hughes P.A., Brierley S.M., Martin C.M., Brookes S.J., Linden D.R., and Blackshaw L.A. Post-inflammatory colonic afferent sensitization: different subtypes, different pathways, and different time-courses. Gut. 58 (2009) 1333-1431
51. Ibeakanma C.O., Miranda-Morales M., Richards M., Bautista-Cruz F., Martin N., Hurlbut D., and Vanner S. Citrobacter rodentium colitis evokes post-infectious hyperexcitability of mouse nociceptive colonic DRG neurons. J. Physiol. 587 (2009) 3505-3521
52. Jones R.C., Xu L., and Gebhart G.F. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J. Neurosci. 25 (2005) 10981-10989
53. Kakei M., Yada T., Nakagawa A., and Nakabayashi H. Glucagon-like peptide-1 evokes action potentials and increases cytosolic Ca2+ in rat nodose ganglion neurons. Auton. Neurosci. 102 (2002) 39-44
54. Kayssi A., Amadesi S., Bautista F., Bunnett N.W., and Vanner S. Mechanisms of protease-activated receptor 2-evoked hyperexcitability of nociceptive neurons innervating the mouse colon. J. Physiol. 580 (2007) 977-991
55. Keating C., Beyak M., Foley S., Singh G., Marsden C., Spiller R., and Grundy D. Afferent hypersensitivity in a mouse model of post-inflammatory gut dysfunction: role of altered serotonin metabolism. J. Physiol. 586 (2008) 4517-4530
56. Kim D.S., Choi J.O., Rim H.D., and Cho H.J. Downregulation of voltage-gated potassium channel alpha gene expression in dorsal root ganglia following chronic constriction injury of the rat sciatic nerve. Brain Res. Mol. Brain Res. 105 (2002) 146-152
57. King D.E., Macleod R.J., and Vanner S.J. Trinitrobenzenesulphonic acid colitis alters Na 1.8 channel expression in mouse dorsal root ganglia neurons. Neurogastroenterol. Motil. 21 8 (2009) 880-e64
58. Kirkup A.J., Booth C.E., Chessell I.P., Humphrey P.P., and Grundy D. Excitatory effect of P2X receptor activation on mesenteric afferent nerves in the anaesthetised rat. J. Physiol. 520 Pt. 2 (1999) 551-563
59. Kirkup A.J., Brunsden A.M., and Grundy D. Receptors and transmission in the brain-gut axis: potential for novel therapies. I. Receptors on visceral afferents. Am. J. Physiol.: Gastrointest. Liver Physiol. 280 (2001) G787-G794
60. Kirkup A.J., Jiang W., Bunnett N.W., and Grundy D. Stimulation of proteinase-activated receptor 2 excites jejunal afferent nerves in anaesthetised rats. J. Physiol. 552 (2003) 589-601
61. Li Y., Zhu J., and Owyang C. Electrical physiological evidence for highand low-affinity vagal CCK-A receptors. Am. J. Physiol. 277 (1999) G469-G477
62. Li Y., Wu X.Y., and Owyang C. Serotonin and cholecystokinin synergistically stimulate rat vagal primary afferent neurones. J. Physiol. 559 (2004) 651-662
63. Lindstrom E., Brusberg M., Hughes P.A., Martin C.M., Brierley S.M., Phillis B.D., Martinsson R., Abrahamsson C., Larsson H., Martinez V., and Blackshaw L.A. Involvement of metabotropic glutamate 5 receptor in visceral pain. Pain 137 (2008) 295-305
64. Matsunami M., Tarui T., Mitani K., Nagasawa K., Fukushima O., Okubo K., Yoshida S., Takemura M., and Kawabata A. Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut 58 (2009) 751-761
65. McIlwrath S.L., Davis B.M., and Bielefeldt K. Deletion of P2X3 receptors blunts gastro-oesophageal sensation in mice. Neurogastroenterol. Motil. 21 8 (2009) 890-e66
66. Moore B.A., Stewart T.M., Hill C., and Vanner S.J. TNBS ileitis evokes hyperexcitability and changes in ionic membrane properties of nociceptive DRG neurons. Am. J. Physiol.: Gastrointest. Liver Physiol. 282 (2002) G1045-G1051
67. Moore P.K., Bhatia M., and Moochhala S. Hydrogen sulfide: from the smell of the past to the mediator of the future?. Trends Pharmacol. Sci. 24 (2003) 609-611
68. Nakagawa A., Satake H., Nakabayashi H., Nishizawa M., Furuya K., Nakano S., Kigoshi T., Nakayama K., and Uchida K. Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Auton. Neurosci. 110 (2004) 36-43
69. Nishizawa M., Nakabayashi H., Kawai K., Ito T., Kawakami S., Nakagawa A., Niijima A., and Uchida K. The hepatic vagal reception of intraportal GLP-1 is via receptor different from the pancreatic GLP-1 receptor. J. Auton. Nerv. Syst. 80 (2000) 14-21
70. Page A.J., and Blackshaw L.A. GABA (B) receptors inhibit mechanosensitivity of primary afferent endings. J. Neurosci. 19 (1999) 8597-8602
71. Page A.J., Young R.L., Martin C.M., Umaerus M., O'Donnell T.A., Cooper N.J., Coldwell J.R., Hulander M., Mattsson J.P., Lehmann A., and Blackshaw L.A. Metabotropic glutamate receptors inhibit mechanosensitivity in vagal sensory neurons. Gastroenterology 128 (2005) 402-410
72. Page A.J., Slattery J.A., Milte C., Laker R., O'Donnell T., Dorian C., Brierley S.M., and Blackshaw L.A. Ghrelin selectively reduces mechanosensitivity of upper gastrointestinal vagal afferents. Am. J. Physiol.: Gastrointest. Liver Physiol. 292 (2007) G1376-G1384
73. Page A.J., O'Donnell T.A., Cooper N.J., Young R.L., and Blackshaw L.A. Nitric oxide as an endogenous peripheral modulator of visceral sensory neuronal function. J. Neurosci. 29 (2009) 7246-7255
74. Park S.Y., Choi J.Y., Kim R.U., Lee Y.S., Cho H.J., and Kim D.S. Downregulation of voltage-gated potassium channel alpha gene expression by axotomy and neurotrophins in rat dorsal root ganglia. Mol. Cells 16 (2003) 256-259
75. Partosoedarso E.R., Young R.L., and Blackshaw L.A. GABA (B) receptors on vagal afferent pathways: peripheral and central inhibition. Am. J. Physiol.: Gastrointest. Liver Physiol. 280 (2001) G658-G668
76. Patacchini R., Santicioli P., Giuliani S., and Maggi C.A. Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder. Br. J. Pharmacol. 142 (2004) 31-34
77. Patapoutian A., Tate S., and Woolf C.J. Transient receptor potential channels: targeting pain at the source. Nat. Rev. Drug Discov. 8 (2009) 55-68
78. Peters J.H., Ritter R.C., and Simasko S.M. Leptin and CCK modulate complementary background conductances to depolarize cultured nodose neurons. Am. J. Physiol., Cell Physiol. 290 (2006) C427-C432
79. Peters J.H., Ritter R.C., and Simasko S.M. Leptin and CCK selectively activate vagal afferent neurons innervating the stomach and duodenum. Am. J. Physiol., Regul. Integr. Comp. Physiol. 290 (2006) R1544-R1549
80. Phillis B.D., Martin C.M., Kang D., Larsson H., Lindstrom E.A., Martinez V., and Blackshaw L.A. Role of TRPV1 in high-threshold rat colonic splanchnic afferents is revealed by inflammation. Neurosci. Lett. 459 (2009) 57-61
81. Roberts D.J., Hasler W.L., and Owyang C. GABA mediation of the dual effects of somatostatin on guinea pig ileal myenteric cholinergic transmission. Am. J. Physiol. 264 (1993) G953-G960
82. Rong, W., Beyak, M.J., Bulmer, D.C.E., Jiang, W., Winchester, W., & Grundy, D., (5 A.D.) Hydrogen sulphide activates small intestinal afferent fibres through a purinergic mechanism. Gastroenterology 128[4 (2)], S1483. (Ref Type: Abstract).
83. Rong W., Spyer K.M., and Burnstock G. Activation and sensitisation of low and high threshold afferent fibres mediated by P2X receptors in the mouse urinary bladder. J. Physiol. 541 (2002) 591-600
84. Rong W., Hillsley K., Davis J.B., Hicks G., Winchester W.J., and Grundy D. Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. J. Physiol. 560 (2004) 867-881
85. Rong W., Winchester W.J., and Grundy D. Spontaneous hypersensitivity in mesenteric afferent nerves of mice deficient in the sst2 subtype of somatostatin receptor. J. Physiol. 581 (2007) 779-786
86. Rong W., Keating C., Sun B., Dong L., and Grundy D. Purinergic contribution to small intestinal afferent hypersensitivity in a murine model of postinfectious bowel disease. Neurogastroenterol. Motil. 21 6 (2009) 665-e32
87. Schicho R., Krueger D., Zeller F., Von Weyhern C.W., Frieling T., Kimura H., Ishii I., De G.R., Campi B., and Schemann M. Hydrogen sulfide is a novel prosecretory neuromodulator in the guinea-pig and human colon. Gastroenterology 131 (2006) 1542-1552
88. Sipe W.E., Brierley S.M., Martin C.M., Phillis B.D., Cruz F.B., Grady E.F., Liedtke W., Cohen D.M., Vanner S., Blackshaw L.A., and Bunnett N.W. Transient receptor potential vanilloid 4 mediates protease activated receptor 2-induced sensitization of colonic afferent nerves and visceral hyperalgesia. Am. J. Physiol.: Gastrointest. Liver Physiol. 294 (2008) G1288-G1298
89. Stewart T., Beyak M.J., and Vanner S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J. Physiol. 552 (2003) 797-807
90. Sugiuar T., Bielefeldt K., and Gebhart G.F. TRPV1 function in mouse colon sensory neurons is enhanced by metabotropic 5-hydroxytryptamine receptor activation. J. Neurosci. 24 (2004) 9521-9530
91. Sugiura T., Bielefeldt K., and Gebhart G.F. Mouse colon sensory neurons detect extracellular acidosis via TRPV1. Am. J. Physiol., Cell Physiol. 292 (2007) C1768-C1774
92. Sun W.M., Katsinelos P., Horowitz M., and Read N.W. Disturbances in anorectal function in patients with diabetes mellitus and faecal incontinence. Eur. J. Gastroenterol. Hepatol. 8 (1996) 1007-1012
93. Vahl T.P., Tauchi M., Durler T.S., Elfers E.E., Fernandes T.M., Bitner R.D., Ellis K.S., Woods S.C., Seeley R.J., Herman J.P., and D'Alessio D.A. Glucagon-like peptide-1 (GLP-1) receptors expressed on nerve terminals in the portal vein mediate the effects of endogenous GLP-1 on glucose tolerance in rats. Endocrinology 148 (2007) 4965-4973
94. Wald A., and Tunuguntla A.K. Anorectal sensorimotor dysfunction in fecal incontinence and diabetes mellitus. Modification with biofeedback therapy. N. Engl. J. Med. 310 (1984) 1282-1287
95. Wang Z.J., and Neuhuber W.L. Intraganglionic laminar endings in the rat esophagus contain purinergic P2X2 and P2X3 receptor immunoreactivity. Anat. Embryol. (Berl) 207 (2003) 363-371
96. Waxman S.G., Cummins T.R., Dib-Hajj S., Fjell J., and Black J.A. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 22 (1999) 1177-1187
97. Waxman S.G., Cummins T.R., Dib-Hajj S., Fjell J., and Black J.A. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 22 (1999) 1177-1187
98. Wiley J.W., Lu Y.X., and Owyang C. Evidence for a glutamatergic neural pathway in the myenteric plexus. Am. J. Physiol. 261 (1991) G693-G700
99. Xu G.Y., Shenoy M., Winston J.H., Mittal S., and Pasricha P.J. P2X receptor-mediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut 57 (2008) 1230-1237
100. Yang E.K., Takimoto K., Hayashi Y., de Groat W.C., and Yoshimura N. Altered expression of potassium channel subunit mRNA and alpha-dendrotoxin sensitivity of potassium currents in rat dorsal root ganglion neurons after axotomy. Neuroscience 123 (2004) 867-874
101. Yang J., Li Y., Zuo X., Zhen Y., Yu Y., and Gao L. Transient receptor potential ankyrin-1 participates in visceral hyperalgesia following experimental colitis. Neurosci. Lett. 440 (2008) 237-241
102. Yoshimura N., and de Groat W.C. Plasticity of Na+ channels in afferent neurones innervating rat urinary bladder following spinal cord injury. J. Physiol. 503 Pt 2 (1997) 269-276
103. Yoshimura N., and de Groat W.C. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J. Neurosci. 19 (1999) 4644-4653
104. Yoshimura N., White G., Weight F.F., and de Groat W.C. Different types of Na+ and A-type K+ currents in dorsal root ganglion neurones innervating the rat urinary bladder. J. Physiol. 494 Pt 1 (1996) 1-16
105. Zhu J.X., Zhu X.Y., Owyang C., and Li Y. Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J. Physiol. 530 (2001) 431-442