5-hydroxytryptamine 2C receptors tonically augment synaptic currents in the nucleus tractus solitarii

Journal of Neurophysiology

Volumn 108, Issue 8, 2012, Pages 2292-2305

  Austgen, James R ^a   Dantzler, Heather A ^a   Barger, Brenna K ^a   Kline, David D ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Aautonomic nervous system; Carotid body; Electrophysiology; Immunohistochemistry; Rrespiratory system; Serotonin

Indexed keywords

GLUTAMIC ACID; SEROTONIN; SEROTONIN 2 RECEPTOR; SEROTONIN 2C ANTAGONIST; SEROTONIN 2C RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MEMBRANE POTENTIAL; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SOLITARY TRACT NUCLEUS; SYNAPTIC TRANSMISSION;

AFFERENT PATHWAYS; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2C; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS; SOLITARY NUCLEUS; SYNAPSES;

EID: 84867719878     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00049.2012     Document Type: Article

References (73)

1. Abbas AI, Yadav PN, Yao WD, Arbuckle MI, Grant SG, Caron MG, Roth BL. PSD-95 is essential for hallucinogen and atypical antipsychotic drug actions at serotonin receptors. J Neurosci 29: 7124-7136, 2009.
2. Accorsi-Mendonca D, Castania JA, Bonagamba LG, Machado BH, Leao RM. Synaptic profile of nucleus tractus solitarius neurons involved with the peripheral chemoreflex pathways. Neuroscience 197: 107-120, 2011.
3. Alheid GF, Jiao W, McCrimmon DR. Caudal nuclei of the rat nucleus of the solitary tract differentially innervate respiratory compartments within the ventrolateral medulla. Neuroscience 190: 207-227, 2011.
4. Aloyo VJ, Berg KA, Spampinato U, Clarke WP, Harvey JA. Current status of inverse agonism at serotonin2A (5-HT2A) and 5-HT2C receptors. Pharmacol Ther 121: 160-173, 2009.
5. Anastasio NC, Lanfranco MF, Bubar MJ, Seitz PK, Stutz SJ, McGinnis AG, Watson CS, Cunningham KA. Serotonin 5-HT2C receptor protein expression is enriched in synaptosomal and post-synaptic compartments of rat cortex. J Neurochem 113: 1504-1515, 2010.
6. Andresen MC, Kunze DL. Nucleus tractus solitarius- gateway to neural circulatory control. Annu Rev Physiol 56: 93-116, 1994.
7. Andresen MC, Mendelowitz D. Sensory afferent neurotransmission in caudal nucleus tractus solitarius-common denominators. Chem Senses 21: 387-395, 1996.
8. Andresen MC, Peters JH. Comparison of baroreceptive to other afferent synaptic transmission to the medial solitary tract nucleus. Am J Physiol Heart Circ Physiol 295: H2032-H2042, 2008.
9. Austgen JR, Dantzler HA, Kline DD. 5-Hydroxytryptamine receptor 2C (5-HT2C) augments synaptic currents in the nucleus tractus solitarii (nTS) (Abstract). FASEB J 25: 844, 2011
10. Austgen JR, Fong AY, Foley CM, Mueller PJ, Kline DD, Heesch CM, Hasser EM. Expression of Group I metabotropic glutamate receptors on phenotypically different cells within the nucleus of the solitary tract in the rat. Neuroscience 159: 701-716, 2008.
11. Austgen JR, Hermann G, Dantzler HA, Rogers RC, Kline DD. Hydrogen sulfide (H2S) augments synaptic neurotransmission in the nucleus of the solitary (NTS). J Neurophysiol 106: 1822-1832, 2011b.
12. Bayliss DA, Li YW, Talley EM. Effects of serotonin on caudal raphe neurons: activation of an inwardly rectifying potassium conductance. J Neurophysiol 77: 1349-1361, 1997.
13. Bonhaus DW, Weinhardt KK, Taylor M, DeSouza A, McNeeley PM, Szczepanski K, Fontana DJ, Trinh J, Rocha CL, Dawson MW, Flippin LA, Eglen RM. RS-102221: a novel high affinity and selective, 5-HT2C receptor antagonist. Neuropharmacology 36: 621-629, 1997.
14. Bonsi P, Cuomo D, Ding J, Sciamanna G, Ulrich S, Tscherter A, Bernardi G, Surmeier D, Pisani A. Endogenous serotonin excites striatal cholinergic interneurons via the activation of 5-HT2C, 5-HT6, and 5-HT7 serotonin receptors: implications for extrapyramidal side effects of serotonin reuptake inhibitors. Neuropsychopharmacology 32: 1840-1854, 2007.
15. Browning KN, Travagli RA. Characterization of the in vitro effects of 5-hydroxytryptamine (5-HT) on identified neurons of the rat dorsal motor nucleus of the vagus (DMV). Br J Pharmacol 128: 1307-1315, 1999.
16. Cayetanot F, Gros F, Larnicol N. 5-HT2A/2C receptor-mediated hypopnea in the newborn rat: relationship to fos immunoreactivity. Pediatr Res 50: 596-603, 2001.
17. Comet MA, Vernard JF, Hamon M, Laguzzi R, Sevoz-Couche C. Activation of nucleus tractus solitarius 5-HT2A but not other 5-HT2 receptor subtypes inhibits the sympathetic activity in rats. Eur J Neurosci 26: 345-354, 2007.
18. Cornea-Herbert B, Watkins K, Roth B, Kroeze W, Gaudreau P, Leclerc N, Descarries L. Similar ultra structural distribution of the 5-HT2A serotonin receptor and microtubule-associated protein MAP1A in cortical dendrites of adult rat. Neuroscience 113: 23-35, 2002.
19. Crowell MD, Wessinger SB. 5-HT and the brain-gut axis: opportunities for pharmacologic intervention. Expert Opin Investig Drugs 16: 761-765, 2007.
20. Dean JB. Theory of gastric CO2 ventilation and its control during respiratory acidosis: implications for central chemosensitivity, pH regulation, and diseases causing chronic CO2 retention. Respir Physiol Neurobiol 175: 189-209, 2011.
21. Di Giovanni G, Di Matteo V, La Grutta V, Esposito E. M-Chlorophenylpiperazine excites non-dopaminergic neurons in the rat substantia nigra and ventral tegmental area by activating serotonin-2C receptors. Neuroscience 103: 111-116, 2001.
22. Doyle MW, Andresen MC. Reliability of monosynaptic sensory transmission in brain stem neurons in vivo. J Neurophysiol 85: 2213-2223, 2001.
23. Edwards E, Paton JF. 5-HT4 receptors in nucleus tractus solitarii attenuate cardiopulmonary reflex in anesthetized rats. Am J Physiol Heart Circ Physiol 277: H1914-H1923, 1999.
24. Feldman PD. Effects of serotonin-1 and serotonin-2 receptor agonists on neuronal activity in the nucleus tractus solitarius. J Auton Nerv Syst 56: 119-124, 1995.
25. Finley JC, Katz DM. The central organization of carotid body afferent projections to the brainstem of the rat. Brain Res 572: 108-116, 1992.
26. Fonseca MI, Ni YG, Dunning DD, Miledi R. Distribution of serotonin 2A, 2C, and 3 receptor mRNA in spinal cord and medulla oblongata. Mol Brain Res 89: 11-19, 2001.
27. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74: 829-898, 1994.
28. Gordon FJ, Sved AF. Neurotransmitters in central cardiovascular regulation: glutamate and GABA. Clin Exp Pharmacol Physiol 29: 522-524, 2002.
29. Hisadome K, Reimann F, Gribble FM, Trapp S. Leptin directly depolarizes preproglucagon neurons in the nucleus tractus solitarius: electrical properties of glucagon-like Peptide 1 neurons. Diabetes 59: 1890-1898, 2010.
30. Hodges MR, Best S, Richerson GB. Altered ventilatory and thermoregulatory control in male and female adult Pet-1 null mice. Respir Physiol Neurobiol 177: 133-140, 2011.
31. Hodges MR, Richerson GB. Contributions of 5-HT neurons to respiratory control: neuromodulatory and trophic effects. Respir Physiol Neurobiol 164:222-232, 2008.
32. Jin YH, Andresen MC. GABAB restrains release from singly-evoked GABA terminals. Neuroscience 193: 54-62, 2011.
33. John J, Manchanda R. Modulation of synaptic potentials and cell excitability by dendritic KIR and KAs channels in nucleus accumbens medium spiny neurons: a computational study. J Biosci 36: 309-328, 2011.
34. Jordan D. Vagal control of the heart: central serotonergic (5-HT) mechanisms. Exp Physiol 90: 175-181, 2005.
35. Khater-Boidin J, Rose D, Glerant JC, Duron B. Central effects of 5-HT on respiratory rhythm in newborn rats in vivo. Eur J Neurosci 11: 3433-3440, 1999.
36. Kline DD. Plasticity in glutamatergic NTS neurotransmission. Respir Physiol Neurobiol 164: 105-111, 2008.
37. Kline DD, King TL, Austgen JR, Heesch CM, Hasser EM. Sensory afferent and hypoxia-mediated activation of nucleus tractus solitarius neurons that project to the rostral ventrolateral medulla. Neuroscience 167: 510-527, 2010.
38. Kline DD, Takacs KN, Ficker E, Kunze DL. Dopamine modulates synaptic transmission in the nucleus of the solitary tract. J Neurophysiol 88: 2736-2744, 2002.
39. Kung LH, Scrogin KE. Serotonin nerve terminals in the dorsomedial medulla facilitate sympathetic and ventilatory responses to hemorrhage and peripheral chemoreflex activation. Am J Physiol Regul Integr Comp Physiol 301: R1367-R1379, 2011.
40. Laaris N, Weinreich D. Prostaglandin E2 depresses solitary tract-mediated synaptic transmission in the nucleus tractus solitarius. Neuroscience 146: 792-801, 2007.
41. Lawrence AJ, Jarrott B. Neurochemical modulation of cardiovascular control in the nucleus tractus solitarius. Prog Neurobiol 48: 21-53, 1996.
42. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DeltaDeltaC(T) method. Methods 25: 402-408, 2001.
43. Luscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA. G protein-coupled inwardly rectifying K_ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19: 687-695, 1997.
44. McDonald DM. Morphology of the rat carotid sinus nerve. I. Course, connections, dimensions, and ultra structure. J Neurocytol 12: 345-372, 1983.
45. Merahi N, Orer HS, Laguzzi R. 5-HT2 receptors in the nucleus tractus solitarius: characterisation and role in cardiovascular regulation in the rat. Brain Res 575: 74-78, 1992.
46. Miles R. Frequency dependence of synaptic transmission in nucleus of the solitary tract in vitro. J Neurophysiol 55: 1076-1090, 1986.
47. Morrison SF, Nakamura K. Central neural pathways for thermoregulation. Front Biosci 16: 74-104, 2011.
48. Nalivaiko E, Sgoifo A. Central 5-HT receptors in cardiovascular control during stress. Neurosci Biobehav Rev 33: 95-106, 2009.
49. Nosjean A, Compoint C, Buisseret-Delmas C, Orer HS, Merahi N, Puizillout JJ, Laguzzi R. 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, 1990.
50. Nunez-Abades PA, Morillo AM, Pasaro R. Brainstem connections of the rat ventral respiratory subgroups: afferent projections. J Auton Nerv Syst 42: 99-118, 1993.
51. Oskutyte D, Jordan D, Ramage AG. Evidence that 5-hydroxytryptamine7 receptors play a role in the mediation of afferent transmission within the nucleus tractus solitarius in anaesthetized rats. Br J Pharmacol 158: 1387-1394, 2009.
52. + currents through a cAMP-dependent protein kinase A-independent mechanism. Neuroscience 167: 678-690, 2010.
53. Prabhakar NR. Sensory plasticity of the carotid body: role of reactive oxygen species and physiological significance. Respir Physiol Neurobiol 178: 375-380, 2011.
54. Qui J, Xue C, Bosch MA, Murphy JG, Fan W, Ronnekleiv OK, Kelly MJ. Serotonin 5-hydroxytryptamine2C receptor signaling in hypothalamic proopiomelanocortin neurons: role in energy homeostasis in females. Mol Pharmacol 72: 885-896, 2007.
55. Ramage A. Central cardiovascular regulation and 5-hydroxytryptamine receptors. Brain Res Bull 56: 425-439, 2001.
56. Raul L. Serotonin2 receptors in the nucleus tractus solitarius: characterization and role in the baroreceptor reflex arc. Cell Mol Neurobiol 23: 709-726, 2003.
57. Raymond JR, Turner J, Gelasco AK, Ayiku HB, Coaxum S, Arthur JM, Garnovskaya MN. 5-HT receptor signal transduction pathways. In: The Serotonin Receptors: from Molecular Pharmacology to Human Therapeutics, edited by Roth B. Totowa, NJ: Humana, 2006, p. 143-206.
58. Rick CE, Stanford IM, Lacey MG. Excitation of rat substantia nigra pars reticulata neurons by 5-hydroxytryptamine in vitro: evidence for a direct action mediated by 5-hydroxytryptamine2C receptors. Neuroscience 69: 903-913, 1995.
59. Roth BL, Willins DL, Kristiansen K, Kroeze WK. 5-Hydroxytryptamine2-family receptors (5-hydroxytryptamine2A, 5-hydroxytryptamine2B, 5-hydroxytryptamine- 2C): where structure meets function. Pharmacol Ther 79: 231-257, 1998.
60. Sakakibara S, Nakadate K, Tanaka-Nakadate S, Yoshida K, Nogami S, Shirataki H, Ueda S. Developmental and spatial expression pattern of alphataxilin in the rat central nervous system. J Comp Neurol 511: 65-80, 2008.
61. Schaffar N, Kessler JP, Bosler O, Jean A. Central serotonergic projections to the nucleus tractus solitarii: evidence from a double labeling study in the rat. Neuroscience 26: 951-958, 1988.
62. Sessle BJ, Henry JL. Effects of enkephalin and 5-hydroxytryptamine on solitary tract neurones involved in respiration and respiratory reflexes. Brain Res 327: 221-230, 1985.
63. Sevoz-Couche C, Spyer KM, Jordan D. In vivo modulation of vagalidentified dorsal medullary neurones by activation of different 5-hydroxytryptamine2 receptors in rats. Br J Pharmacol 131: 1445-1453, 2000a.
64. Sevoz-Couche C, Spyer KM, Jordan D. Inhibition of rat nucleus tractus solitarius neurones by activation of 5-HT2C receptors. Neuroreport 11: 1785-1790, 2000b.
65. Sevoz-Couche C, Wang Y, Ramage AG, Spyer KM, Jordan D. In vivo modulation of nucleus tractus solitarius (NTS) neurones by activation of 5-hydroxytryptamine2 receptors in rats. Neuropharmacology 39: 2006-2016, 2000c.
66. Sharman JL, Mpamhanga CP, Spedding M, Germain P, Staels B, Dacquet C, Laudet V, Harmar AJ, NC-IUPHAR. IUPHAR-DB: new receptors and tools for easy searching and visualization of pharmacological data. Nucleic Acids Res 39: D534-D538, 2011.
67. Siuciak JA, Chapin DS, McCarthy SA, Guanowsky V, Brown J, Chiang P, Marala R, Patterson T, Seymour PA, Swick A, Iredale PA. CP-809,101, a selective 5-HT2C agonist, shows activity in animal models of antipsychotic activity. Neuropharmacology 52: 279-290, 2007.
68. Tache Y, Yang H, Kaneko H. Caudal raphe-dorsal vagal complex peptidergic projections: role in gastric vagal control. Peptides 16: 431-435, 1995.
69. Takenaka R, Ohi Y, Haji A. Distinct modulatory effects of 5-HT on excitatory synaptic transmissions in the nucleus tractus solitarius of the rat. Eur J Pharmacol 22: 222-223, 2011.
70. Takigawa T, Alzheimer C. Phasic and tonic attenuation of EPSPs by inward rectifier K_ channels in rat hippocampal pyramidal cells. J Physiol 539: 67-75, 2002.
71. Tecott LH, Logue SF, Wehner JM, Kauer JA. Perturbed dentate gyrus function in serotonin 5-HT2C receptor mutant mice. Proc Natl Acad Sci USA 95: 15026-15031, 1998.
72. Villalon CM, Centurion D. Cardiovascular responses produced by 5-hydroxytryptamine: a pharmacological update on the receptors/mechanisms involved and therapeutic implications. Naunyn Schmiedebergs Arch Pharmacol 376: 45-63, 2007.
73. Zhang W, Carreno FR, Cunningham JT, Mifflin SW. Chronic sustained and intermittent hypoxia reduce function of ATP-sensitive potassium channels in nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 295: R1555-R1562, 2008.