Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Chambers, Jordan D ^a   Bornstein, Joel C ^a   Thomas, Evan A ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CLOTRIMAZOLE; DECANOIC ACID; 1 (2 METHOXYPHENYL) 4 (4 (2 PHTHALIMIDO)BUTYL)PIPERAZINE; 1-(2-METHOXYPHENYL)-4-(4-(2-PHTHALIMIDO)BUTYL)PIPERAZINE; N TERT BUTYL 3 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL] 2 PHENYLPROPIONAMIDE; PIPERAZINE DERIVATIVE; PYRAZOLE DERIVATIVE; TRAM 34;

ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEEDBACK SYSTEM; FEMALE; HYPERPOLARIZATION; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTESTINE CONTRACTION; INTESTINE MOTILITY; MALE; MUSCLE ACTION POTENTIAL; NONHUMAN; OSCILLATORY POTENTIAL; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECT; FEEDING BEHAVIOR; GUINEA PIG; JEJUNUM; MOTONEURON; MOTOR ACTIVITY; MUSCLE; MUSCLE CONTRACTION; NERVE CELL INHIBITION; NERVE CELL NETWORK; PHYSIOLOGY; SENSORY RECEPTOR;

CAVIA;

ACTION POTENTIALS; ANIMALS; CLOTRIMAZOLE; EXCITATORY POSTSYNAPTIC POTENTIALS; FEEDBACK, PHYSIOLOGICAL; FEEDING BEHAVIOR; GUINEA PIGS; JEJUNUM; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLES; NERVE NET; NEURAL INHIBITION; PIPERAZINES; PYRAZOLES; SENSORY RECEPTOR CELLS;

EID: 79955865899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019597     Document Type: Article

References (64)

1. Furness JB, (2006) The Enteric Nervous System. Malden, Mass Blackwell Pub.
2. Hasler W, (2003) Motility of the small intestine and colon. In: TY, editors. Textbook of Gastroenterology Philadelphia Lippincott Williams & Wilkins pp. 220-247.
3. Hasler WL, (2008) Motility of the Small Intestine and Colon. In: Yamada T, editors. Textbook of Gastroenterology Wiley-Blackwell 5th ed.
4. Huge A, Weber E, Ehrlein HJ, (1995) Effects of enteral feedback inhibition on motility, luminal flow, and absorption of nutrients in proximal gut of minipigs. Dig Dis Sci 40: 1024-1034.
5. Schemann M, Ehrlein HJ, (1986) Postprandial patterns of canine jejunal motility and transit of luminal content. Gastroenterology 90: 991-1000.
6. Schmid HR, Ehrlein HJ, (1993) Effects of enteral infusion of hypertonic saline and nutrients on canine jejunal motor patterns. Dig Dis Sci 38: 1062-1072.
7. Sarr MG, Kelly KA, Phillips SF, (1980) Canine jejunal absorption and transit during interdigestive and digestive motor states. Am J Physiol 239: G167-172.
8. Siegle ML, Ehrlein HJ, (1988) Digestive motor patterns and transit of luminal contents in canine ileum. Am J Physiol 254: G552-559.
9. Gwynne RM, Bornstein JC, (2007) Mechanisms underlying nutrient induced segmentation in isolated guinea-pig small intestine. Am J Physiol Gastrointest Liver Physiol.
10. Gwynne RM, Thomas EA, Goh SM, Sjovall H, Bornstein JC, (2004) Segmentation induced by intraluminal fatty acid in isolated guinea-pig duodenum and jejunum. J Physiol 556: 557-569.
11. Huizinga JD, Lammers WJ, (2009) Gut peristalsis is governed by a multitude of cooperating mechanisms. Am J Physiol Gastrointest Liver Physiol 296: G1-8.
12. Brookes SJ, (2001) Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262: 58-70.
13. Furness JB, Jones C, Nurgali K, Clerc N, (2004) Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol 72: 143-164.
14. Gwynne R, Bornstein J, (2007) Synaptic transmission at functionally identified synapses in the enteric nervous system: roles for both ionotropic and metabotropic receptors. Curr Neuropharmacol 5: 1-17.
15. Bornstein JC, Furness JB, Kunze WAA, Bertrand PP, (2002) Enteric reflexes that influence motility. In: Costa M, Brookes SJH, editors. Nervous control of the gastrointestinal tract London Taylor & Francis pp. 1-55.
16. Song ZM, Brookes SJ, Costa M, (1994) All calbindin-immunoreactive myenteric neurons project to the mucosa of the guinea-pig small intestine. Neurosci Lett 180: 219-222.
17. Bertrand PP, Kunze WA, Furness JB, Bornstein JC, (2000) The terminals of myenteric intrinsic primary afferent neurons of the guinea-pig ileum are excited by 5-hydroxytryptamine acting at 5-hydroxytryptamine-3 receptors. Neuroscience 101: 459-469.
18. Ellis M, Gwynne RM, Bornstein JC, (2009) Nutrient induced segmentation is mediated by serotonin and cholecystokinin in isolated guinea pig small intestine. Auton Neurosci 149: 42.
19. Gwynne RM, Bornstein JC, (2007) Local Inhibitory Reflexes Excited by Mucosal Application of Nutrient Amino Acids in Guinea-Pig Jejunum. Am J Physiol Gastrointest Liver Physiol.
20. Bertrand PP, (2006) Real-time measurement of serotonin release and motility in guinea pig ileum. J Physiol 577: 689-704.
21. Costa M, Brookes SH, (2008) Architecture of enteric neural circuits involved in intestinal motility. Eur Rev Med Pharmacol Sci 12 (Suppl 1): 3-19.
22. Spencer NJ, Walsh M, Smith TK, (2000) Purinergic and cholinergic neuro-neuronal transmission underlying reflexes activated by mucosal stimulation in the isolated guinea-pig ileum. J Physiol 522 (Pt 2): 321-331.
23. Bian X, Bertrand PP, Bornstein JC, (2000) Descending inhibitory reflexes involve P2X receptor-mediated transmission from interneurons to motor neurons in guinea-pig ileum. J Physiol 528: 551-560.
24. Chambers JD, Bornstein JC, Thomas EA, (2008) Insights into mechanisms of intestinal segmentation in guinea pigs: a combined computational modeling and in vitro study. Am J Physiol Gastrointest Liver Physiol.
25. Ferens D, Baell J, Lessene G, Smith JE, Furness JB, (2007) Effects of modulators of Ca(2+)-activated, intermediate-conductance potassium channels on motility of the rat small intestine, in vivo. Neurogastroenterol Motil 19: 383-389.
26. Thomas EA, Bornstein JC, (2003) Inhibitory cotransmission or after-hyperpolarizing potentials can regulate firing in recurrent networks with excitatory metabotropic transmission. Neuroscience 120: 333-351.
27. Thomas EA, Bertrand PP, Bornstein JC, (2000) A computer simulation of recurrent, excitatory networks of sensory neurons of the gut in guinea-pig. Neurosci Lett 287: 137-140.
28. Johnson PJ, Bornstein JC, (2004) Neurokinin-1 and-3 receptor blockade inhibits slow excitatory synaptic transmission in myenteric neurons and reveals slow inhibitory input. Neuroscience 126: 137-147.
29. Chambers JD, Bornstein JC, Thomas EA, (2008) Insights into mechanisms of intestinal segmentation in guinea pigs: a combined computational modeling and in vitro study. Am J Physiol Gastrointest Liver Physiol 295: G534-541.
30. Fung C, Ellis M, Bornstein JC, (2010) Luminal cholera toxin alters motility in isolated guinea-pig jejunum via a pathway independent of 5-HT3 receptors. Frontiers in Enteric Neuroscience In press.
31. Nguyen TV, Matsuyama H, Baell J, Hunne B, Fowler CJ, et al. (2007) Effects of compounds that influence IK (KCNN4) channels on afterhyperpolarizing potentials, and determination of IK channel sequence, in guinea pig enteric neurons. J Neurophysiol 97: 2024-2031.
32. Foong JP, Pary LJ, Bornstein JC, (2010) 5-HT1A, SST1 and SST2 receptors mediate inhibitory postsynaptic potentials in the submucous plexus of the guinea-pig ileum. Am J Physiol Gastrointest Liver Physiol In press.
33. Grafe P, Mayer CJ, Wood JD, (1980) Synaptic modulation of calcium-dependent potassium conductance in myenteric neurones in the guinea-pig. J Physiol 305: 235-248.
34. Johnson PJ, Bornstein JC, Burcher E, (1998) Roles of neuronal NK1 and NK3 receptors in synaptic transmission during motility reflexes in the guinea-pig ileum. Br J Pharmacol 124: 1375-1384.
35. Johnson PJ, Bornstein JC, Yuan SY, Furness JB, (1996) Analysis of contributions of acetylcholine and tachykinins to neuro-neuronal transmission in motility reflexes in the guinea-pig ileum. Br J Pharmacol 118: 973-983.
36. Tonini M, Costa M, (1990) A pharmacological analysis of the neuronal circuitry involved in distension-evoked enteric excitatory reflex. Neuroscience 38: 787-795.
37. Kunze WA, Furness JB, Bertrand PP, Bornstein JC, (1998) Intracellular recording from myenteric neurons of the guinea-pig ileum that respond to stretch. J Physiol 506 (Pt 3): 827-842.
38. Bertrand PP, (2004) Bursts of recurrent excitation in the activation of intrinsic sensory neurons of the intestine. Neuroscience 128: 51-63.
39. Neylon CB, Nurgali K, Hunne B, Robbins HL, Moore S, et al. (2004) 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.
40. Furness JB, Robbins HL, Selmer IS, Hunne B, Chen MX, et al. (2003) Expression of intermediate conductance potassium channel immunoreactivity in neurons and epithelial cells of the rat gastrointestinal tract. Cell Tissue Res 314: 179-189.
41. Furness JB, Kearney K, Robbins HL, Hunne B, Selmer IS, et al. (2004) Intermediate conductance potassium (IK) channels occur in human enteric neurons. Auton Neurosci 112: 93-97.
42. Wang B, Mao YK, Diorio C, Wang L, Huizinga JD, et al. (2010) Lactobacillus reuteri ingestion and IK(Ca) channel blockade have similar effects on rat colon motility and myenteric neurones. Neurogastroenterol Motil 22: 98-107, e133.
43. Thompson-Vest N, Shimizu Y, Hunne B, Furness JB, (2006) The distribution of intermediate-conductance, calcium-activated, potassium (IK) channels in epithelial cells. J Anat 208: 219-229.
44. Joiner WJ, Basavappa S, Vidyasagar S, Nehrke K, Krishnan S, et al. (2003) Active K+ secretion through multiple KCa-type channels and regulation by IKCa channels in rat proximal colon. Am J Physiol Gastrointest Liver Physiol 285: G185-196.
45. Zhu Y, Ye J, Huizinga JD, (2007) Clotrimazole-sensitive K+ currents regulate pacemaker activity in interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 292: G1715-1725.
46. Parsons SP, Huizinga JD, (2010) Transient outward potassium current in ICC. Am J Physiol Gastrointest Liver Physiol 298: G456-466.
47. Foong JP, Parry LJ, Gwynne RM, Bornstein JC, (2010) 5-HT(1A), SST(1), and SST(2) receptors mediate inhibitory postsynaptic potentials in the submucous plexus of the guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 298: G384-394.
48. Pan H, Galligan JJ, (1994) 5-HT1A and 5-HT4 receptors mediate inhibition and facilitation of fast synaptic transmission in enteric neurons. Am J Physiol 266: G230-238.
49. Pan H, Galligan JJ, (1995) Effects of 5-HT1A and 5-HT4 receptor agonists on slow synaptic potentials in enteric neurons. Eur J Pharmacol 278: 67-74.
50. Foong JP, Bornstein JC, (2009) 5-HT antagonists NAN-190 and SB 269970 block alpha2-adrenoceptors in the guinea pig. Neuroreport 20: 325-330.
51. Wilson HR, Cowan JD, (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12: 1-24.
52. Bertrand PP, Thomas EA, Kunze WA, Bornstein JC, (2000) A simple mathematical model of second-messenger mediated slow excitatory postsynaptic potentials. J Comput Neurosci 8: 127-142.
53. Alex G, Kunze WA, Furness JB, Clerc N, (2001) Comparison of the effects of neurokinin-3 receptor blockade on two forms of slow synaptic transmission in myenteric AH neurons. Neuroscience 104: 263-269.
54. Heredia DJ, Dickson EJ, Bayguinov PO, Hennig GW, Smith TK, (2009) Localized release of serotonin (5-hydroxytryptamine) by a fecal pellet regulates migrating motor complexes in murine colon. Gastroenterology 136: 1328-1338.
55. Keating DJ, Spencer NJ, (2010) Release of 5-hydroxytryptamine from the mucosa is not required for the generation or propagation of colonic migrating motor complexes. Gastroenterology 138: 659-670 670 e651-652.
56. Ellis M, Gwynne RM, Bornstein JC, (2009) Nutrient induced segmentation is mediated by serotonin and cholecystokinin in isolated guinea pig small intestine. Autonomic Neuroscience 149: S11.15.
57. Bertrand PP, Bornstein JC, (2002) ATP as a putative sensory mediator: activation of intrinsic sensory neurons of the myenteric plexus via P2X receptors. J Neurosci 22: 4767-4775.
58. Alex G, Clerc N, Kunze WA, Furness JB, (2002) Responses of myenteric S neurones to low frequency stimulation of their synaptic inputs. Neuroscience 110: 361-373.
59. Thornton PD, Bornstein JC, (2002) Slow excitatory synaptic potentials evoked by distension in myenteric descending interneurones of guinea-pig ileum. J Physiol 539: 589-602.
60. Hennig GW, Costa M, Chen BN, Brookes SJ, (1999) Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps. J Physiol 517 (Pt 2): 575-590.
61. Bertrand PP, Kunze WA, Bornstein JC, Furness JB, Smith ML, (1997) Analysis of the responses of myenteric neurons in the small intestine to chemical stimulation of the mucosa. Am J Physiol 273: G422-435.
62. Bulbring E, Lin RC, (1958) The effect of intraluminal application of 5-hydroxytryptamine and 5-hydroxytryptophan on peristalsis; the local production of 5-HT and its release in relation to intraluminal pressure and propulsive activity. J Physiol 140: 381-407.
63. Tabak J, Senn W, O'Donovan MJ, Rinzel J, (2000) Modeling of spontaneous activity in developing spinal cord using activity-dependent depression in an excitatory network. J Neurosci 20: 3041-3056.
64. Chambers JD, Bornstein JC, Sjovall H, Thomas EA, (2005) Recurrent networks of submucous neurons controlling intestinal secretion: a modeling study. Am J Physiol Gastrointest Liver Physiol 288: G887-896.