Role of central vagal 5-HT3 receptors in gastrointestinal physiology and pathophysiology

Frontiers in Neuroscience

Volumn 9, Issue OCT, 2015, Pages

  Browning, Kirsteen N ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

5 HT; Gastrointestinal; Plasticity; Vagal afferent; Vagus

Indexed keywords

SEROTONIN; SEROTONIN 3 RECEPTOR;

ENERGY BALANCE; FOOD INTAKE; GASTROINTESTINAL DISEASE; GASTROINTESTINAL TRACT; GASTROINTESTINAL TRACT FUNCTION; HUMAN; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; REFLEX; REVIEW; SIGNAL TRANSDUCTION; STOMACH INNERVATION; TRANSLATIONAL RESEARCH; VAGOVAGAL REFLEX;

EID: 84946546547     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00413     Document Type: Review

References (138)

1. Andresen, M. C., and Kunze, D. L. (1994). Nucleus tractus solitarius-gateway to neural circulatory control. Annu. Rev. Physiol. 56, 93-116. doi: 10.1146/annurev.ph.56.030194.000521
2. Andrews, P. L., Davis, C. J., Bingham, S., Davidson, H. I., Hawthorn, J., and Maskell, L. (1990). The abdominal visceral innervation and the emetic reflex: pathways, pharmacology, and plasticity. Can. J. Physiol. Pharmacol. 68, 325-345. doi: 10.1139/y90-047
3. Andrews, P. L., and Horn, C. C. (2006). Signals for nausea and emesis: implications for models of upper gastrointestinal diseases. Auton. Neurosci. 125, 100-115. doi: 10.1016/j.autneu.2006.01.008
4. Babic, T., and Browning, K. N. (2014). The role of vagal neurocircuits in the regulation of nausea and vomiting. Eur. J. Pharmacol. 722, 38-47. doi: 10.1016/j. ejphar.2013.08.047
5. Babic, T., Troy, A. E., Fortna, S. R., and Browning, K. N. (2012). Glucose-dependent trafficking of 5-HT(3) receptors in rat gastrointestinal vagal afferent neurons. Neurogastroenterol. Motil. 24, e476-e488. doi: 10.1111/j.1365-2982.2012.01987.x
6. Baptista, V., Browning, K. N., and Travagli, R. A. (2007). Effects of cholecystokinin-8s in the nucleus tractus solitarius of vagally deafferented rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1092-R1100. doi: 10.1152/ajpregu.00517.2006
7. Berthoud, H.-R., Carlson, N. R., and Powley, T. L. (1991). Topography of efferent vagal innervation of the rat gastrointestinal tract. Am. J. Physiol. 260, R200-R207.
8. Bertrand, P. P., Kunze, W. A., Furness, J. B., and Bornstein, J. C. (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. doi: 10.1016/S0306-4522(00)00363-8
9. Beyak, M. J., and Grundy, D. (2005). "Vagal afferents innervating the gastrointestinal tract," in Advances in Vagal Afferent Neurobiology, eds B. J. Undem and D. Weinreich (Boca Raton, FL: CRC Press), 315-350.
10. Bielefeldt, K., Ozaki, N., and Gebhart, G. F. (2002a). Experimental ulcers alter voltage-sensitive sodium currents in rat gastric sensory neurons. Gastroenterology 122, 394-405. doi: 10.1053/gast.2002.31026
11. Bielefeldt, K., Ozaki, N., and Gebhart, G. F. (2002b). Mild gastritis alters voltage-sensitive sodium currents in gastric sensory neurons in rats. Gastroenterology 122, 752-761. doi: 10.1053/gast.2002.31901
12. Blackshaw, L. A., and Grundy, D. (1993). Effects of 5-hydroxytryptamine (5-HT) on the discharge of vagal mechanoreceptors and motility in the upper gastrointestinal tract of the ferret. J. Auton. Nerv. Syst. 45, 51-59. doi: 10.1016/0165-1838(93)90361-W
13. Blakelock, R. T., and Beasley, S. W. (2003). Infection and the gut. Semin. Pediatr. Surg. 12, 265-274. doi: 10.1053/j.sempedsurg.2003.08.008
14. 3 receptors in a rat model of delayed stress-induced visceral hyperalgesia. Pain 130, 56-65. doi: 10.1016/j.pain.2006.10.028
15. Browning, K. N. (2013). Modulation of gastrointestinal vagal neurocircuits by hyperglycemia. Front. Neurosci. 7:217. doi: 10.3389/fnins.2013.00217
16. Browning, K. N., Babic, T., Holmes, G. M., Swartz, E. M., and Travagli, R. A. (2013a). A critical re-evaluation of the specificity of action of perivagal capsaicin. J. Physiol. 591, 1563-1580. doi: 10.1113/jphysiol.2012.246827
17. Browning, K. N., Fortna, S. R., and Hajnal, A. (2013b). Roux-en-Y gastric bypass reverses the effects of diet-induced obesity to inhibit the responsiveness of central vagal motoneurones. J. Physiol. 591, 2357-2372. doi: 10.1113/jphysiol.2012.249268
18. Browning, K. N., and Travagli, R. A. (2001). The peptide TRH uncovers the presence of presynaptic 5-HT1A receptors via activation of a second messenger pathway in the rat dorsal vagal complex. J. Physiol. 531, 425-435. doi: 10.1111/j.1469-7793.2001.0425i.x
19. Browning, K. N., and Travagli, R. A. (2011). Plasticity of vagal brainstem circuits in the control of gastrointestinal function. Auton. Neurosci. 161, 6-13. doi: 10.1016/j.autneu.2010.11.001
20. Browning, K. N., and Travagli, R. A. (2014). Central nervous system control of gastrointestinal motility and secretion and modulation of gastrointestinal functions. Compr. Physiol. 4, 1339-1368. doi: 10.1002/cphy.c130055
21. Bulbring, E., and Lin, R. C. (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.
22. Callera, J. C., Sevoz, C., Laguzzi, R., and Machado, B. H. (1997). Microinjection of a serotonin3 receptor agonist into the NTS of unanesthetized rats inhibits the bradycardia evoked by activation of the baro-and chemoreflexes. J. Auton. Nerv. Syst. 63, 127-136. doi: 10.1016/S0165-1838(96)00140-3
23. Camilleri, M., Andrews, C. N., Bharucha, A. E., Carlson, P. J., Ferber, I., Stephens, D., et al. (2007). Alterations in expression of p11 and SERT in mucosal biopsy specimens of patients with irritable bowel syndrome. Gastroenterology 132, 17-25. doi: 10.1053/j.gastro.2006.11.020
24. 3 receptors and vagal afferent fibers. Brain Res. 688, 149-160. doi: 10.1016/0006-8993(95)00526-V
25. Chen, S., Li, J., Zhang, L., Dong, X., Gao, W., Mo, J., et al. (2009). 5-HT 3 receptors mediate the time-dependent vagal afferent modulation of nociception during chronic food allergen-sensitized visceral hyperalgesia in rats. Neurogastroenterol. Motil. 21, 1222-e113. doi: 10.1111/j.1365-2982.2009.01335.x
26. Chen, S. L., Wu, X. Y., Cao, Z. J., Fan, J., Wang, M., Owyang, C., et al. (2008). Subdiaphragmatic vagal afferent nerves modulate visceral pain. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1441-G1449. doi: 10.1152/ajpgi.00588.2007
27. Coates, M. D., Mahoney, C. R., Linden, D. R., Sampson, J. E., Chen, J., Blaszyk, H., et al. (2004). Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126, 1657-1664. doi: 10.1053/j.gastro.2004.03.013
28. 3 receptor agonist MKC-733 on upper gastrointestinal motility in humans. Aliment. Pharmacol. Ther. 18, 1039-1048. doi: 10.1046/j.1365-2036.2003.01797.x
29. Cottrell, G. T., and Ferguson, A. V. (2004). Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul. Pept. 117, 11-23. doi: 10.1016/j.regpep.2003.09.004
30. Covasa, M., Grahn, J., and Ritter, R. C. (2000a). High fat maintenance diet attenuates hindbrain neuronal response to CCK. Regul. Pept. 86, 83-88. doi: 10.1016/S0167-0115(99)00084-1
31. Covasa, M., Grahn, J., and Ritter, R. C. (2000b). Reduced hindbrain and enteric neuronal response to intestinal oleate in rats maintained on high-fat diet. Auton. Neurosci. 84, 8-18. doi: 10.1016/S1566-0702(00)00176-4
32. Cui, R. J., Roberts, B. L., Zhao, H., Zhu, M., and Appleyard, S. M. (2012). Serotonin activates catecholamine neurons in the solitary tract nucleus by increasing spontaneous glutamate inputs. J. Neurosci. 32, 16530-16538. doi: 10.1523/JNEUROSCI.1372-12.2012
33. Daly, D. M., Park, S. J., Valinsky, W. C., and Beyak, M. J. (2011). Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J. Physiol. 589, 2857-2870. doi: 10.1113/jphysiol.2010.204594
34. Dang, K., Bielefeldt, K., and Gebhart, G. F. (2004). Gastric ulcers reduce A-type potassium currents in rat gastric sensory ganglion neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G573-G579. doi: 10.1152/ajpgi.00258.2003
35. Darmani, N. A., and Johnson, J. C. (2004). Central and peripheral mechanisms contribute to the antiemetic actions of delta-9-tetrahydrocannabinol against 5-hydroxytryptophan-induced emesis. Eur. J. Pharmacol. 488, 201-212. doi: 10.1016/j.ejphar.2004.02.018
36. Darmani, N. A., and Ray, A. P. (2009). Evidence for a re-evaluation of the neurochemical and anatomical bases of chemotherapy-induced vomiting. Chem. Rev. 109, 3158-3199. doi: 10.1021/cr900117p
37. de Lartigue, G. (2014). Putative roles of neuropeptides in vagal afferent signaling. Physiol. Behav. 136, 155-169. doi: 10.1016/j.physbeh.2014.03.011
38. de Lartigue, G., de La Serre, C. B., and Raybould, H. E. (2011). Vagal afferent neurons in high fat diet-induced obesity; intestinal microflora, gut inflammation and cholecystokinin. Physiol. Behav. 105, 100-105. doi: 10.1016/j.physbeh.2011.02.040
39. 3 receptors are membrane ion channels. Nature 339, 706-709. doi: 10.1038/339706a0
40. Dockray, G. J. (2013). Enteroendocrine cell signalling via the vagus nerve. Curr. Opin. Pharmacol. 13, 954-958. doi: 10.1016/j.coph.2013.09.007
41. Donovan, M. J., Paulino, G., and Raybould, H. E. (2007). CCK(1) receptor is essential for normal meal patterning in mice fed high fat diet. Physiol. Behav. 92, 969-974. doi: 10.1016/j.physbeh.2007.07.003
42. Dunn-Meynell, A. A., Sanders, N. M., Compton, D., Becker, T. C., Eiki, J., Zhang, B. B., et al. (2009). Relationship among brain and blood glucose levels and spontaneous and glucoprivic feeding. J. Neurosci. 29, 7015-7022. doi: 10.1523/JNEUROSCI.0334-09.2009
43. Endo, T., Minami, M., Hirafuji, M., Ogawa, T., Akita, K., Nemoto, M., et al. (2000). Neurochemistry and neuropharmacology of emesis-the role of serotonin. Toxicology 153, 189-201. doi: 10.1016/S0300-483X(00)00314-0
44. Endo, T., Minami, M., Monma, Y., Saito, H., and Takeuchi, M. (1990). Emesis-related biochemical and histopathological changes induced by cisplatin in the ferret. J. Toxicol. Sci. 15, 235-244. doi: 10.2131/jts.15.235
45. Foley, S., Garsed, K., Singh, G., Duroudier, N. P., Swan, C., Hall, I. P., et al. (2011). Impaired uptake of serotonin by platelets from patients with irritable bowel syndrome correlates with duodenal immune activation. Gastroenterology 140, 1434-1443. doi: 10.1053/j.gastro.2011.01.052
46. 3 receptor internalization in enteric neurons in rat ileum. Gastroenterology 131, 97-107. doi: 10.1053/j.gastro.2006.04.013
47. Fry, M., and Ferguson, A. V. (2007). The sensory circumventricular organs: brain targets for circulating signals controlling ingestive behavior. Physiol. Behav. 91, 413-423. doi: 10.1016/j.physbeh.2007.04.003
48. Gaudin-Chazal, G., Portalier, P., Barrit, M. C., and Puizillout, J. J. (1982). Serotonin-like immunoreactivity in paraffin-sections of the nodose ganglia of the cat. Neurosci. Lett. 33, 169-172. doi: 10.1016/0304-3940(82)90246-4
49. Gentilcore, D., Little, T. J., Feinle-Bisset, C., Samsom, M., Smout, A. J., Horowitz, M., et al. (2007). Role of 5-hydroxytryptamine mechanisms in mediating the effects of small intestinal glucose on blood pressure and antropyloroduodenal motility in older subjects. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G692-G698. doi: 10.1152/ajpgi.00199.2007
50. Gershon, M. D., and Tack, J. (2007). The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132, 397-414. doi: 10.1053/j.gastro.2006.11.002
51. 3 receptors in the rat gastrointestinal tract. Gastroenterology 123, 217-226. doi: 10.1053/gast.2002.34245
52. Glaum, S. R., Brooks, P. A., Spyer, K. M., and Miller, R. J. (1992). 5-Hydroxytryptamine-3 receptors modulate synaptic activity in the rat nucleus tractus solitarius in vitro. Brain Res. 589, 62-68. doi: 10.1016/0006-8993(92)91162-8
53. Grabauskas, G., Song, I., Zhou, S. Y., and Owyang, C. (2010). Electrophysiological identifications of glucose-sensing neurons in the rat nodose ganglia. J. Physiol. 588, 617-632. doi: 10.1113/jphysiol.2009.182147
54. Gwynne, R. M., and Bornstein, J. C. (2007). Local inhibitory reflexes excited by mucosal application of nutrient amino acids in guinea pig jejunum. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1660-G1670. doi: 10.1152/ajpgi.00580.2006
55. Hagbom, M., Istrate, C., Engblom, D., Karlsson, T., Rodriguez-Diaz, J., Buesa, J., et al. (2011). Rotavirus stimulates release of serotonin (5-HT) from human enterochromaffin cells and activates brain structures involved in nausea and vomiting. PLoS Pathog. 7:e1002115. doi: 10.1371/journal.ppat.1002115
56. Hawthorn, J., Ostler, K. J., and Andrews, P. L. (1988). The role of the abdominal visceral innervation and 5-hydroxytryptamine M-receptors in vomiting induced by the cytotoxic drugs cyclophosphamide and cis-platin in the ferret. Q. J. Exp. Physiol. 73, 7-21. doi: 10.1113/expphysiol.1988.sp003124
57. 3 receptors participate in control of meal size and mediate CCK-induced satiation. Brain Res. 1103, 99-107. doi: 10.1016/j.brainres.2006.05.058
58. 3 receptors. Brain Res. 1088, 120-130. doi: 10.1016/j.brainres.2006.03.018
59. Hermes, S. M., Mitchell, J. L., Silverman, M. B., Lynch, P. J., McKee, B. L., Bailey, T. W., et al. (2008). Sustained hypertension increases the density of AMPA receptor subunit, GluR1, in baroreceptive regions of the nucleus tractus solitarii of the rat. Brain Res. 1187, 125-136. doi: 10.1016/j.brainres.2007.10.041
60. Hillsley, K., and Grundy, D. (1998). Sensitivity to 5-hydroxytryptamine in different afferent subpopulations within mesenteric nerves supplying the rat jejunum. J. Physiol. 509(Pt 3), 717-727. doi: 10.1111/j.1469-7793.1998.717bm.x
61. Hillsley, K., Kirkup, A. J., and Grundy, D. (1998). Direct and indirect actions of 5-hydroxytryptamine on the discharge of mesenteric afferent fibres innervating the rat jejunum. J. Physiol. 506(Pt 2), 551-561. doi: 10.1111/j.1469-7793.1998.551bw.x
62. Horn, C. C., Richardson, E. J., Andrews, P. L., and Friedman, M. I. (2004). Differential effects on gastrointestinal and hepatic vagal afferent fibers in the rat by the anti-cancer agent cisplatin. Auton. Neurosci. 115, 74-81. doi: 10.1016/j.autneu.2004.08.011
63. Hosford, P. S., Mifflin, S. W., and Ramage, A. G. (2014). 5-hydroxytryptamine-mediated neurotransmission modulates spontaneous and vagal-evoked glutamate release in the nucleus of the solitary tract effect of uptake blockade. J. Pharmacol. Exp. Ther. 349, 288-296. doi: 10.1124/jpet.113.211334
64. Houghton, L. A., Atkinson, W., Whitaker, R. P., Whorwell, P. J., and Rimmer, M. J. (2003). Increased platelet depleted plasma 5-hydroxytryptamine concentration following meal ingestion in symptomatic female subjects with diarrhoea predominant irritable bowel syndrome. Gut 52, 663-670. doi: 10.1136/gut.52.5.663
65. 3A receptor subunits in the rat medial nucleus of the solitary tract: subcellular distribution and relation to the serotonin transporter. Brain Res. 1028, 156-169. doi: 10.1016/j.brainres.2004.09.009
66. 3 receptors in vagal reflex inputs to neurones in the nucleus tractus solitarius of anaesthetized rats. J. Physiol. 566, 939-953. doi: 10.1113/jphysiol.2005.085845
67. Jensen, G. M., Grondahl, M. L., Nielsen, C. G., Skadhauge, E., Olsen, J. E., and Hansen, M. B. (1997). Effect of ondansetron on Salmonella typhimurium-induced net fluid accumulation in the pig jejunum in vivo. Comp. Biochem. Physiol. A Physiol. 118, 297-299. doi: 10.1016/S0300-9629(96)00308-8
68. Jiang, W., Kreis, M. E., Eastwood, C., Kirkup, A. J., Humphrey, P. P., and Grundy, D. (2000). 5-HT(3) and histamine H(1) receptors mediate afferent nerve sensitivity to intestinal anaphylaxis in rats. Gastroenterology 119, 1267-1275. doi: 10.1053/gast.2000.19461
69. Jordan, D. (2005). Vagal control of the heart: central serotonergic (5-HT) mechanisms. Exp. Physiol. 90, 175-181. doi: 10.1113/expphysiol.2004.029058
70. Kang, Y. M., Bielefeldt, K., and Gebhart, G. F. (2004). Sensitization of mechanosensitive gastric vagal afferent fibers in the rat by thermal and chemical stimuli and gastric ulcers. J. Neurophysiol. 91, 1981-1989. doi: 10.1152/jn.01097.2003
71. Kang, Y. M., Lamb, K., Gebhart, G. F., and Bielefeldt, K. (2005). Experimentally induced ulcers and gastric sensory-motor function in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G284-G291. doi: 10.1152/ajpgi.00250.2004
72. Keating, D. J., and Spencer, N. J. (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. doi: 10.1053/j.gastro.2009.09.020
73. Kentish, S. J., O'donnell, T. A., Wittert, G. A., and Page, A. J. (2014). Diet-dependent modulation of gastro-oesphageal vagal afferent mechanosensitivity by endogenous nitric oxide. J. Physiol. 592, 3287-3301. doi: 10.1113/jphysiol.2014.272674
74. Kentish, S. J., and Page, A. J. (2014). Plasticity of gastro-intestinal vagal afferent endings. Physiol. Behav. 136, 170-178. doi: 10.1016/j.physbeh.2014.03.012
75. Kentish, S., Li, H., Philp, L. K., O'donnell, T. A., Isaacs, N. J., Young, R. L., et al. (2012). Diet-induced adaptation of vagal afferent function. J. Physiol. 590, 209-221. doi: 10.1113/jphysiol.2011.222158
76. Kollarik, M., and Undem, B. J. (2002). Mechanisms of acid-induced activation of airway afferent nerve fibres in guinea-pig. J. Physiol. 543, 591-600. doi: 10.1113/jphysiol.2002.022848
77. Kreis, M. E., Jiang, W., Kirkup, A. J., and Grundy, D. (2002). Cosensitivity of vagal mucosal afferents to histamine and 5-HT in the rat jejunum. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G612-G617. doi: 10.1152/ajpgi.00206.2001
78. 3 receptors. Neuroscience 143, 273-287. doi: 10.1016/j.neuroscience.2006.07.032
79. Lacolley, P., Owen, J. R., Sandock, K., Lewis, T. H., Bates, J. N., Robertson, T. P., et al. (2006b). Occipital artery injections of 5-HT may directly activate the cell bodies of vagal and glossopharyngeal afferent cell bodies in the rat. Neuroscience 143, 289-308. doi: 10.1016/j.neuroscience.2006.08.047
80. Leal-Cardoso, H., Koschorke, G. M., Taylor, G. E., and Weinreich, D. (1993). Electrophysiological properties and chemosensitivity of acutely isolated nodose ganglion neurons of the rabbit. JANS 45, 29-39. doi: 10.1016/0165-1838(93)90359-3
81. 3 recognition sites on vagal afferent terminals in the brainstem of the ferret. Neuroscience 38, 667-673. doi: 10.1016/0306-4522(90)90060-H
82. Liu, Y., Hamaue, N., Endo, T., Hirafuji, M., and Minami, M. (2003). 5-hydroxytryptamine (5-HT) concentrations in the hippocampus, the hypothalamus and the medulla oblongata related to cisplatin-induced pica of rats. Res. Commun. Mol. Pathol. Pharmacol. 113-114, 97-113.
83. MacGregor, I. L., Gueller, R., Watts, H. D., and Meyer, J. H. (1976). The effect of acute hyperglycemia on gastric emptying in man. Gastroenterology 70, 190-196.
84. Mawe, G. M., and Hoffman, J. M. (2013). Serotonin signalling in the gut-functions, dysfunctions and therapeutic targets. Nat. Rev. Gastroenterol. Hepatol. 10, 473-486. doi: 10.1038/nrgastro.2013.105
85. 3 receptors in conscious rats. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G228-G235. doi: 10.1152/ajpgi.00373.2003
86. Mei, N. (1978). Vagal glucoreceptors in the small intestine of the cat. J. Physiol. 282, 485-506. doi: 10.1113/jphysiol.1978.sp012477
87. Meller, S. T., Lewis, S. J., Brody, M. J., and Gebhart, G. F. (1992). Vagal afferent-mediated inhibition of a nociceptive reflex by i.v. serotonin in the rat. II. Role of 5-HT receptor subtypes. Brain Res. 585, 71-86. doi: 10.1016/0006-8993(92)91192-H
88. Moore, K. A., Oh, E. J., and Weinreich, D. (2002). 5-HT(3) receptors mediate inflammation-induced unmasking of functional tachykinin responses in vitro. J. Appl. Physiol. 92, 2529-2534. doi: 10.1152/japplphysiol.00974.2001
89. Moore, K. A., Taylor, G. E., and Weinreich, D. (1999). Serotonin unmasks functional NK-2 receptors in vagal sensory neurons of the guinea-pig. J. Physiol. 514, 111-124. doi: 10.1111/j.1469-7793.1999.111af.x
90. Moore, K. A., Undem, B. J., and Weinreich, D. (2000). Antigen inhalation unmasks NK-2 tachykinin receptor-mediated responses in vagal afferents. Am. J. Resp. Crit. Care Med. 161, 232-236. doi: 10.1164/ajrccm.161.1.9903091
91. Mulak, A., Taché, Y., and Larauche, M. (2014). Sex hormones in the modulation of irritable bowel syndrome. World J. Gastroenterol. 20, 2433-2448. doi: 10.3748/wjg.v20.i10.2433
92. Mussa, B. M., Sartor, D. M., and Verberne, A. J. (2008). Activation of cholecystokinin (CCK 1) and serotonin (5-HT 3) receptors increases the discharge of pancreatic vagal afferents. Eur. J. Pharmacol. 601, 198-206. doi: 10.1016/j.ejphar.2008.11.007
93. 3 receptor stimulation. Auton. Neurosci. 156, 36-43. doi: 10.1016/j.autneu.2010.03.001
94. Nakata-Fukuda, M., Hirata, T., Keto, Y., Yamano, M., Yokoyama, T., and Uchiyama, Y. (2014). Inhibitory effect of the selective serotonin 5-HT(3) receptor antagonist ramosetron on duodenal acidification-induced gastric hypersensitivity in rats. Eur. J. Pharmacol. 731, 88-92. doi: 10.1016/j.ejphar.2014.02.040
95. Nefti, W., Chaumontet, C., Fromentin, G., Tomé, D., and Darcel, N. (2009). A high-fat diet attenuates the central response to within-meal satiation signals and modifies the receptor expression of vagal afferents in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R1681-R1686. doi: 10.1152/ajpregu.90733.2008
96. Nosjean, A., Compoint, C., Buisseret-Delmas, C., Orer, H. S., Merahi, N., Puizillout, J. J., et al. (1990). Serotonergic projections from the nodose ganglia to the nucleus tractus solitarius: an immunohistochemical and double labeling study in the rat. Neurosci. Lett. 114, 22-26. doi: 10.1016/0304-3940(90)90422-6
97. Oh, E. J., and Weinreich, D. (2002). Chemical communication between vagal afferent somata in nodose Ganglia of the rat and the Guinea pig in vitro. J. Neurophysiol. 87, 2801-2807.
98. Page, A. J., Symonds, E., Peiris, M., Blackshaw, L. A., and Young, R. L. (2012). Peripheral neural targets in obesity. Br. J. Pharmacol. 166, 1537-1558. doi: 10.1111/j.1476-5381.2012.01951.x
99. Paintal, A. S. (1951). A method of locating the receptors of visceral afferent fibers. J. Physiol. 124, 166-172. doi: 10.1113/jphysiol.1954.sp005095
100. Paulino, G., Barbier de la Serre, C., Knotts, T. A., Oort, P. J., Newman, J. W., Adams, S. H., et al. (2009). Increased expression of receptors for orexigenic factors in nodose ganglion of diet-induced obese rats. Am. J. Physiol. Endocrinol. Metab. 296, E898-E903. doi: 10.1152/ajpendo.90796.2008
101. 3 receptors of rabbit nodose ganglion neurones in culture. Br. J. Pharmacol. 110, 665-676. doi: 10.1111/j.1476-5381.1993.tb13863.x
102. 3 receptors in the nucleus tractus solitarius and other brainstem areas modulate the vagal bradycardia evoked by activation of the von Bezold-Jarisch reflex in the anesthetized rat. Brain Res. 791, 229-234. doi: 10.1016/S0006-8993(98)00109-7
103. Powley, T. L., and Phillips, R. J. (2002). Musings on the wanderer: what's new in our understanding of vago-vagal reflexes? I. Morphology and topography of vagal afferents innervating the GI tract. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G1217-G1225. doi: 10.1152/ajpgi.00249.2002
104. Powley, T. L., Spaulding, R. A., and Haglof, S. A. (2011). Vagal afferent innervation of the proximal gastrointestinal tract mucosa: chemoreceptor and mechanoreceptor architecture. J. Comp. Neurol. 519, 644-660. doi: 10.1002/cne.22541
105. 3 receptors in the anesthetized rat. J. Physiol. 509P, 129P.
106. Ramage, A. G., and Villalon, C. M. (2008). 5-Hydroxytryptamine and cardiovascular regulation. Trends Pharmacol. Sci. 29, 472-481. doi: 10.1016/j.tips.2008.06.009
107. Randich, A., and Gebhart, D. F. (1992). Vagal afferent modulation of nociception. Brain Res. Rev. 17, 77-99. doi: 10.1016/0165-0173(92)90009-B
108. 3 receptors by extrinsic duodenal afferents contribute to intestinal inhibition of gastric emptying. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G367-G372. doi: 10.1152/ajpgi.00292.2001
109. Raybould, H. E., and Zittel, T. T. (1995). Inhibition of gastric motility induced by intestinal glucose in awake rats: role of Na(+)-glucose co-transporter. Neurogastroenterol. Motil. 7, 9-14. doi: 10.1111/j.1365-2982.1995.tb00203.x
110. Rayner, C. K., Samsom, M., Jones, K. L., and Horowitz, M. (2001). Relationships of upper gastrointestinal motor and sensory function with glycemic control. Diabetes Care 24, 371-381. doi: 10.2337/diacare.24.2.371
111. Ren, K., Randich, A., and Gebhart, G. F. (1990). Modulation of spinal nociceptive transmission from nuclei tractus solitarii: a relay for effects of vagal afferent stimulation. J. Neurophysiol. 63, 971-986.
112. 3 receptor antagonist granisetron (BRL 43694). Brain Res. 565, 231-236. doi: 10.1016/0006-8993(91)91654-J
113. Scott, R. B., Tan, D. T., Miampamba, M., and Sharkey, K. A. (1998). Anaphylaxis-induced alterations in intestinal motility: role of extrinsic neural pathways. Am. J. Physiol. 275, G812-G821.
114. Sévoz, C., Callera, J. C., Machado, B. H., Hamon, M., and Laguzzi, R. (1997). Role of serotonin3 receptors in the nucleus tractus solitarii on the carotid chemoreflex. Am. J. Physiol. 272, H1250-H1259.
115. 3 receptors in the NTS inhibits the cardiac Bezold-Jarisch reflex response. Am. J. Physiol. 271, H80-H87.
116. Spencer, N. J., Nicholas, S. J., Robinson, L., Kyloh, M., Flack, N., Brookes, S. J., et al. (2011). Mechanisms underlying distension-evoked peristalsis in guinea pig distal colon: is there a role for enterochromaffin cells? Am. J. Physiol. Gastrointest. Liver Physiol. 301, G519-G527. doi: 10.1152/ajpgi.00101.2011
117. Steinbusch, H. W. (1981). Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6, 557-618. doi: 10.1016/0306-4522(81)90146-9
118. Swartz, T. D., Savastano, D. M., and Covasa, M. (2010). Reduced sensitivity to cholecystokinin in male rats fed a high-fat diet is reversible. J. Nutr. 140, 1698-1703. doi: 10.3945/jn.110.124149
119. Takenaka, R., Ohi, Y., and Haji, A. (2011). Distinct modulatory effects of 5-HT on excitatory synaptic transmissions in the nucleus tractus solitarius of the rat. Eur. J. Pharmacol. 671, 45-52. doi: 10.1016/j.ejphar.2011.09.164
120. Thor, K. B., and Helke, C. J. (1987). Serotonin-and substance P-containing projections to the nucleus tractus solitarii of the rat. J. Comp. Neurol. 265, 275-293. doi: 10.1002/cne.902650210
121. Thor, K. B., and Helke, C. J. (1989). Serotonin and substance P colocalization in medullary projections to the nucleus tractus solitarius: dual-colour immunohistochemistry combined with retrograde tracing. J. Chem. Neuroanat. 2, 139-148.
122. Thor, K. B., Hill, K. M., Harrod, C., and Helke, C. J. (1988). Immunohistochemical and biochemical analysis of serotonin and substance P colocalization in the nucleus tractus solitarii and associated afferent ganglia of the rat. Synapse 2, 225-231. doi: 10.1002/syn.890020309
123. Tolstykh, G., Belugin, S., and Mifflin, S. (2004). Responses to GABA(A) receptor activation are altered in NTS neurons isolated from chronic hypoxic rats. Brain Res. 1006, 107-113. doi: 10.1016/j.brainres.2004.01.060
124. Tonini, M. (2005). 5-Hydroxytryptamine effects in the gut: the 3, 4, and 7 receptors. Neurogastroenterol. Motil. 17, 637-642. doi: 10.1111/j.1365-2982.2005.00716.x
125. Travagli, R. A., Hermann, G. E., Browning, K. N., and Rogers, R. C. (2006). Brainstem circuits regulating gastric function. Annu. Rev. Physiol. 68, 279-305. doi: 10.1146/annurev.physiol.68.040504.094635
126. 3 mediated responses in rat gastric vagal afferents. J. Physiol. doi: 10.1113/JP271558. [Epub ahead of print].
127. 3 receptor involvement in the facilitation of peristalsis on mucosal application of 5-HT in the guinea pig isolated ileum. Br. J. Pharmacol. 122, 1174-1178. doi: 10.1038/sj.bjp.0701503
128. Vanuytsel, T., Karamanolis, G., Van, O. L., Vos, R., and Tack, J. (2011). Influence of ondansetron on gastric sensorimotor responses to short duodenal acid infusion in healthy volunteers. Neurogastroenterol. Motil. 23, 226-232, e115. doi: 10.1111/j.1365-2982.2010.01631.x
129. Wan, S., and Browning, K. N. (2008a). D-Glucose modulates synaptic transmission from the central terminals of vagal afferent fibers. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G757-G763. doi: 10.1152/ajpgi.00576.2007
130. Wan, S., and Browning, K. N. (2008b). Glucose increases synaptic transmission from vagal afferent central nerve terminals via modulation of 5HT3 receptors. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G1050-G1057. doi: 10.1152/ajpgi.90288.2008
131. 3 receptors of an excitatory effect of 5-HT on dorsal vagal preganglionic neurones in anesthetized rats: an ionophoretic study. Br. J. Pharmacol. 118, 1697-1704. doi: 10.1111/j.1476-5381.1996.tb15594.x
132. Weinreich, D., Moore, K. A., and Taylor, G. E. (1997). Allergic inflammation in isolated vagal sensory ganglia unmasks silent NK-2 tachykinin receptors. J. Neurosci. 17, 7683-7693.
133. Wu, Q., Clark, M. S., and Palmiter, R. D. (2012). Deciphering a neuronal circuit that mediates appetite. Nature 483, 594-597. doi: 10.1038/nature10899
134. Wu, X. Y., Zhu, J. X., Gao, J., Owyang, C., and Li, Y. (2005). Neurochemical phenotype of vagal afferent neurons activated to express C-FOS in response to luminal stimulation in the rat. Neuroscience 130, 757-767. doi: 10.1016/j.neuroscience.2004.09.060
135. Yan, X. J., Feng, C. C., Liu, Q., Zhang, L. Y., Dong, X., Liu, Z. L., et al. (2014). Vagal afferents mediate antinociception of estrogen in a rat model of visceral pain: the involvement of intestinal mucosal mast cells and 5-hydroxytryptamine 3 signaling. J. Pain 15, 204-217. doi: 10.1016/j.jpain.2013.10.012
136. Zhou, X., and Galligan, J. J. (1999). Synaptic activation and properties of 5-hydroxytryptamine(3) receptors in myenteric neurons of guinea pig intestine. J. Pharmacol. Exp. Ther. 290, 803-810.
137. Zhu, J. X., Wu, X. Y., Owyang, C., and Li, Y. (2001). Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J. Physiol. 530, 431-442. doi: 10.1111/j.1469-7793.2001.0431k.x
138. Zhuo, H., Ichikawa, H., and Helke, C. J. (1997). Neurochemistry of the nodose ganglion. Prog. Neurobiol. 52, 79-107. doi: 10.1016/S0301-0082(97)00003-8