Characterization of myenteric sensory neurons in the mouse small intestine

Journal of Neurophysiology

Volumn 96, Issue 3, 2006, Pages 998-1010

  Mao, Yukang ^a   Wang, Bingxian ^a   Kunze, Wolfgang ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHARYBDOTOXIN; CLOTRIMAZOLE; POTASSIUM CHANNEL;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; GANGLION; MOUSE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SMALL INTESTINE ABSORPTION; SYNAPTIC TRANSMISSION;

ANIMALS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; FEMALE; GANGLIA, AUTONOMIC; ILEUM; INTESTINE, SMALL; MICE; MICE, INBRED C57BL; MYENTERIC PLEXUS; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES;

EID: 33748567113     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00204.2006     Document Type: Article

References (85)

1. Baidan LV, Zholos AV, Shuba MF, and Wood JD. Patch-clamp recording in myenteric neurons of guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 262: G1074-G1078, 1992.
2. 2+ buffers. Methods Cell Biol 40: 3-29, 1994.
3. Bertrand PP and Galligan JJ. Signal-transduction pathways causing slow synaptic excitation in guinea pig myenteric AH neurons. Am J Physiol Gastrointest Liver Physiol 269: G710-G720, 1995.
4. Bertrand PP, Kunze WA, Bornstein JC, Furness JB, and Smith ML. Analysis of the responses of myenteric neurons in the small intestine to chemical stimulation of the mucosa. Am J Physiol Gastrointest Liver Physiol 273: G422-G435, 1997.
5. Bertrand PP and Thomas EA. Multiple levels of sensory integration in the intrinsic sensory neurons of the enteric nervous system. Clin Exp Pharmacol Physiol 31: 745-755, 2004.
6. Bian X, Ren J, DeVries M, Schnegelsberg B, Cockayne DA, Ford AP, and Galligan JJ. Peristalsis is impaired in the small intestine of mice lacking the P2X3 subunit. J Physiol 551: 309-322, 2003.
7. Bornstein JC, Furness JB, and Kunze WA. Electrophysiological characterization of myenteric neurons: how do classification schemes relate? J Auton Nerv Syst 48: 1-15, 1994.
8. Bornstein JC, Furness JB, Kunze WAA, and Bertrand PP. Enteric reflexes that influence motility. In: Nervous Control of the Gastrointestinal Tract, edited by Costa M and Brookes SJH. London: Taylor & Francis, 2002, p. 1-55.
9. Brookes SJ. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262: 58-70, 2001.
10. Brookes SJ, Ewart WR, and Wingate DL. Intracellular recordings from myenteric neurones in the human colon. J Physiol 390: 305-318, 1987.
11. Brookes SJ, Ewart WR, and Wingate DL. Intracellular recordings from cells in the myenteric plexus of the rat duodenum. Neuroscience 24: 297-307, 1988.
12. Browning KN and Lees GM. Myenteric neurons of the rat descending colon: electrophysiological and correlated morphological properties. Neuroscience 73: 1029-1047, 1996.
13. Bullard DC and Weaver CT. Cutting-edge technology. IV. Genomic engineering for studies of the gastrointestinal tract in mice. Am J Physiol Gastrointest Liver Physiol 283: G1232-G1237, 2002.
14. Clements JD and Redman SJ. Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. J Physiol 409: 63-87, 1989.
15. Clerc N, Furness JB, Bornstein JC, and Kunze WA. Correlation of electrophysiological and morphological characteristics of myenteric neurons of the duodenum in the guinea-pig. Neuroscience 82: 899-914, 1998.
16. Cole KS. Squid axon membrane: impedance decrease to voltage clamp. Annu Rev Neurosci 5: 305-323, 1982.
17. Cornelissen W, De Laet A, Kroese AB, Van Bogaert PP, Scheuermann DW, and Timmermans JP. Electrophysiological features of morphological Dogiel type II neurons in the myenteric plexus of pig small intestine. J Neurophysiol 84: 102-111, 2000.
18. Costa M, Hennig GW, and Brookes SJ. Intestinal peristalsis: a mammalian motor pattern controlled by enteric neural circuits. Ann NY Acad Sci 860: 464-466, 1998.
19. Coste B, Osorio N, Padilla F, Crest M, and Delmas P. Gating and modulation of presumptive NaV1.9 channels in enteric and spinal sensory neurons. Mol Cell Neurosci 26: 123-134, 2004.
20. + channel Nav1.9: in search of a gating mechanism. Trends Neurosci 26: 55-57, 2003.
21. Der T, Bercik P, Donnelly G, Jackson T, Berezin I, Collins SM, and Huizinga JD. Interstitial cells of Cajal and inflammation-induced motor dysfunction in the mouse small intestine. Gastroenterology 119: 1590, 2000.
22. Dib-Hajj S, Black JA, Cummins TR, and Waxman SG. NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci 25: 253-259, 2002.
23. Franklin JL and Willard AL. Voltage-dependent sodium and calcium currents of rat myenteric neurons in cell culture. J Neurophysiol 69: 1264-1275, 1993.
24. Furness JB, Clerc N, and Kunze WA. Memory in the enteric nervous system [Discussion]. Gut 47, Suppl. 4: iv60-iv62, 2000.
25. Furness JB and Costa M. The Enteric Nervous System. New York: Churchill Livingstone, 1987.
26. Furness JB, Jones C, Nurgali K, and Clerc N. Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol 72: 143-164, 2004a.
27. Furness JB, Kearney K, Robbins HL, Hunne B, Selmer IS, Neylon CB, Chen MX, and Tjandra JJ. Intermediate conductance potassium (IK) channels occur in human enteric neurons. Auton Neurosci 112: 93-97, 2004b.
28. Furness JB, Kunze WA, Bertrand PP, Clerc N, and Bornstein JC. Intrinsic primary afferent neurons of the intestine. Prog Neurobiol 54: 1-18, 1998.
29. Furness JB, Robbins HL, Selmer IS, Hunne B, Chen MX, Hicks GA, Moore S, and Neylon CB. Expression of intermediate conductance potassium channel immunoreactivity in neurons and epithelial cells of the rat gastrointestinal tract. Cell Tissue Res 314: 179-189, 2003.
30. Furukawa K, Taylor GS, and Bywater RA. An intracellular study of myenteric neurons in the mouse colon. J Neurophysiol 55: 1395-1406, 1986.
31. Galligan JJ, Tatsumi H, Shen KZ, Surprenant A, and North RA. Cation current activated by hyperpolarization (IH) in guinea pig enteric neurons. Am J Physiol Gastrointest Liver Physiol 259: G966-G972, 1990.
32. Georgiou P, Bountra C, and House CR. Intracellular and whole-cell recordings from zona-free hamster eggs: significance of leak impalement artifact. Q J Exp Physiol 72: 105-118, 1987.
33. Gershon MD. Lessons from genetically engineered animal models. II. Disorders of enteric neuronal development: insights from transgenic mice. Am J Physiol Gastrointest Liver Physiol 277: G262-G267, 1999.
34. Gola M and Niel JP. Electrical and integrative properties of rabbit sympathetic neurones re-evaluated by patch clamping non-dissociated cells. J Physiol 460: 327-349, 1993.
35. Greffrath W, Martin E, Reuss S, and Boehmer G. Components of afterhyperpolarization in magnocellular neurones of the rat supraoptic nucleus in vitro. J Physiol 513: 493-506, 1998.
36. Hanani M, Francke M, Hartig W, Grosche J, Reichenbach A, and Pannicke T. Patch-clamp study of neurons and glial cells in isolated myenteric ganglia. Am J Physiol Gastrointest Liver Physiol 278: G644-G651, 2000.
37. 2+ concentration in cultured rat myenteric neurones. Neurogastroenterol Motil 14: 133-142, 2002.
38. Hay M and Kunze DL. An intermediate conductance calcium-activated potassium channel in rat visceral sensory afferent neurons. Neurosci Lett 167: 179-182, 1994.
39. + current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol 86: 1351-1364, 2001.
40. Hillsley K, Kenyon JL, and Smith TK. Ryanodine-sensitive stores regulate the excitability of AH neurons in the myenteric plexus of guinea-pig ileum. J Neurophysiol 84: 2777-2785, 2000.
41. Hirning LD, Fox AP, and Miller RJ. Inhibition of calcium currents in cultured myenteric neurons by neuropeptide Y: evidence for direct receptor/channel coupling. Brain Res 532: 120-130, 1990.
42. Hirst GD, Holman ME, and Spence I. Two types of neurones in the myenteric plexus of duodenum in the guinea pig. J Physiol 236: 303-326, 1974.
43. Hodgkiss JP and Lees JS. Slow intracellular potentials in AH-neurons of the myenteric plexus evoked by repetitive activation of synaptic inputs. Neuroscience 11: 255-261, 1984.
44. Holzer P. Gastrointestinal afferents as targets of novel drugs for the treatment of functional bowel disorders and visceral pain. Eur J Pharmacol 429: 177-193, 2001.
45. Holzer P, Schicho R, Holzer-Petsche U, and Lippe IT. The gut as a neurological organ. Wien Klin Wochenschr 113: 647-660, 2001.
46. International Union of Basic and Clinical Pharmacology (IUPHAR). IUPHAR ion channel compendium. http://wwwiuphar-dborg/iuphar-ic/indexhtml. Accessed 2002.
47. Jensen BS, Odum N, Jorgensen NK, Christophersen P, and Olesen SP. Inhibition of T cell proliferation by selective block of Ca(2+)-activated K(+) channels. Proc Natl Acad Sci USA 96: 10917-10921, 1999.
48. Johnson SM, Katayama Y, and North RA. Slow synaptic potentials in neurones of the myenteric plexus. J Physiol 301: 505-516, 1980.
49. 2+ concentration in isolated hippocampal neurones. Br J Pharmacol 89: 191-198, 1986.
50. Kunze W, Mueller MH, Jiang GJ, and Grundy D. On the enteric sensory neuron in the mouse. Proc Neurogastroenterol Motil, Tuebingen, Germany, 2002, p. 566.
51. Kunze WA, Bornstein JC, and Furness JB. Identification of sensory nerve cells in a peripheral organ (the intestine) of a mammal. Neuroscience 66: 1-4, 1995.
52. Kunze WA, Bornstein JC, Furness JB, Hendriks R, and Stephenson DS. Charybdotoxin and iberiotoxin but not apamin abolish the slow afterhyperpolarization in myenteric plexus neurons. Pfluegers Arch 428: 300-306, 1994.
53. Kunze WA, Clerc N, Furness JB, and Gola M. The soma and neurites of primary afferent neurons in the guinea-pig intestine respond differentially to deformation. J Physiol 526: 375-385, 2000.
54. Kunze WA and Furness JB. The enteric nervous system and regulation of intestinal motility. Annu Rev Physiol 61: 117-142, 1999.
55. Kunze WA, Furness JB, Bertrand PP, and Bornstein JC. Intracellular recording from myenteric neurons of the guinea-pig ileum that respond to stretch. J Physiol 506: 827-842, 1998.
56. Kunze WA, Furness JB, and Bornstein JC. Simultaneous intracellular recordings from enteric neurons reveal that myenteric AH neurons transmit via slow excitatory postsynaptic potentials. Neuroscience 55: 685-694, 1993.
57. Kunze WA and Mueller MH. Kinetics and functions of calcium modulated potassium channels in enteric sensory neurons. Proc DDW Conf Gastroenterol, San Francisco, CA, 2002, p. A-163.
58. Lamas JA. A hyperpolarization-activated cation current (Ih) contributes to resting membrane potential in rat superior cervical sympathetic neurones. Pfluegers Arch 436: 429-435, 1998.
59. Lee RH and Heckman CJ. Essential role of a fast persistent inward current in action potential initiation and control of rhythmic firing. J Neurophysiol 85: 472-475, 2001.
60. Li WC, Soffe SR, and Roberts A. A direct comparison of whole cell patch and sharp electrodes by simultaneous recording from single spinal neurons in frog tadpoles. J Neurophysiol 92: 380-386, 2004.
61. Liu MT, Rayport S, Jiang Y, Murphy DL, and Gershon MD. Expression and function of 5-HT3 receptors in the enteric neurons of mice lacking the serotonin transporter. Am J Physiol Gastrointest Liver Physiol 283: G1398-G1411, 2002.
62. Neylon CB, Nurgali K, Hunne B, Robbins HL, Moore S, Chen MX, and Furness JB. Intermediate-conductance calcium-activated potassium channels in enteric neurones of the mouse: pharmacological, molecular and immunochemical evidence for their role in mediating the slow afterhyperpolarization. J Neurochem 90: 1414-1422, 2004.
63. Nurgali K, Stebbing MJ, and Furness JB. Correlation of electrophysiological and morphological characteristics of enteric neurons in the mouse colon. J Comp Neurol 468: 112-124, 2004.
64. Picciotto MR and Wickman K. Using knockout and transgenic mice to study neurophysiology and behavior. Physiol Rev 78: 1131-1163, 1998.
65. Ren J, Bian X, DeVries M, Schnegelsberg B, Cockayne DA, Ford AP, and Galligan JJ. P2X2 subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine. J Physiol 552: 809-821, 2003.
66. Rugiero F, Gola M, Kunze WA, Reynaud JC, Furness JB, and Clerc N. Analysis of whole-cell currents by patch clamp of guinea-pig myenteric neurones in intact ganglia. J Physiol 538: 447-463, 2002.
67. + current and NaV1.9 subunit in myenteric sensory neurons. J Neurosci 23: 2715-2725, 2003.
68. Schutte IW, Kroese ABA, and Akkermans LMA. Somal size and location within the ganglia for electrophysiologically identified myenteric neurons of the guinea pig ileum. J Comp Neurol 355: 563-572, 1995.
69. Shen KZ, North RA, and Surprenant A. Potassium channels opened by noradrenaline and other transmitters in excised membrane patches of guinea-pig submucosal neurones. J Physiol 445: 581-599, 1992.
70. Smith TK, Bornstein JC, and Furness JB. Convergence of reflex pathways excited by distension and mechanical stimulation of the mucosa onto the same myenteric neurons of the guinea pig small intestine. J Neurosci 12: 1502-1510, 1992.
71. Spencer NJ. Control of migrating motor activity in the colon. Curr Opin Pharmacol 1: 604-610, 2001.
72. Spencer NJ and Smith TK. Mechanosensory S-neurons rather than AH-neurons appear to generate a rhythmic motor pattern in guinea-pig distal colon. J Physiol 558: 577-596, 2004.
73. Spruston N and Johnston D. Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67: 509-529, 1992.
74. Staley KJ, Otis TS, and Mody I. Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole cell recordings. J Neurophysiol 67: 1346-1358, 1992.
75. Takaki M and Nakayama S. Effects of mesenteric nerve stimulation on the electrical activity of myenteric neurons in the guinea pig ileum. Brain Res 442: 351-353, 1988.
76. Tatsumi H, Hirai K, and Katayama Y. Measurement of the intracellular calcium concentration in guinea-pig myenteric neurons by using fura-2. Brain Res 451: 371-375, 1988.
77. Thurbon D, Luescher H, Hofstetter T, and Redman SJ. Passive electrical properties of ventral horn neurons in rat spinal cord slices. J Neurophysiol 79: 2485-2502, 1998.
78. Velumian AA and Carlen PL. Differential control of three afterhyperpolarizations in rat hippocampal neurones by intracellular calcium buffering. J Physiol 517: 201-216, 1999.
79. Vogalis F, Harvey JR, and Furness JB. TEA- and apamin-resistant K(Ca) channels in guinea-pig myenteric neurons: slow AHP channels. J Physiol 538: 421-433, 2002a.
80. + channels underlying the slow afterhyperpolarization in enteric afterhyperpolarization-generating myenteric neurons: role of calcium and phosphorylation. Clin Exp Pharmacol Physiol 29: 935-943, 2002b.
81. Wells DG and Mawe GM. Physiological and morphological properties of neurons in sphincter of Oddi region of the guinea pig. Am J Physiol Gastrointest Liver Physiol 265: G258-G269, 1993.
82. Willms AR, Baro DJ, Harris-Warrick RM, and Guckenheimer J. An improved parameter estimation method for Hodgkin-Huxley models. J Comput Neurosci 6: 145-168, 1999.
83. Wood JD and Mayer CJ. Intracellular study of tonic-type enteric neurons in guinea pig small intestine. J Neurophysiol 42: 569-581, 1979.
84. Xiao J, Nguyen TV, Ngui K, Strijbos PJ, Selmer IS, Neylon CB, and Furness JB. Molecular and functional analysis of hyperpolarisation-activated nucleotide-gated (HCN) channels in the enteric nervous system. Neuroscience 129: 603-614, 2004.
85. Zhang L, Weiner JL, Valiante TA, Velumian AA, Watson PL, Jahromi SS, Schertzer S, Pennefather P, and Carlen PL. Whole-cell recording of the Ca(2+)-dependent slow afterhyperpolarization in hippocampal neurones: effects of internally applied anions. Pfluegers Arch 426: 247-253, 1994.