Inhibitory synaptic transmission in area postrema neurons of the rat showing robust presynaptic facilitation mediated by nicotinic ACh receptors

Brain Research

Volumn 1130, Issue 1, 2007, Pages 83-94

  Kawa, Kazuyoshi ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Area postrema; GABAergic transmission; Nicotinic receptor; Patch clamp; Presynaptic facilitation; Synapse

Indexed keywords

1,1 DIMETHYL 4 PHENYLPIPERAZINIUM IODIDE; 4 AMINOBUTYRIC ACID; ACETYLCHOLINE; ALPHA BUNGAROTOXIN; BICUCULLINE; CALCIUM ION; CHLORIDE; CHOLINE; CYTISINE; DIHYDRO BETA ERYTHROIDINE; GLYCINE; MAGNESIUM ION; MECAMYLAMINE; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; RECEPTOR SUBTYPE; STRYCHNINE; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; AREA POSTREMA; ARTICLE; BRAIN SLICE; CALCIUM TRANSPORT; CONTROLLED STUDY; FACILITATION; FEMALE; GABAERGIC SYSTEM; GENE EXPRESSION; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MEDULLA OBLONGATA; MEMBRANE VESICLE; NERVE ENDING; NEUROMODULATION; NONHUMAN; PERINATAL PERIOD; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; AREA POSTREMA; FEMALE; GAMMA-AMINOBUTYRIC ACID; MALE; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, GABA; RECEPTORS, GLYCINE; RECEPTORS, NICOTINIC; SYNAPTIC TRANSMISSION;

RATTUS; STRYCHNOS TOXIFERA;

EID: 33846001315     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.10.001     Document Type: Article

References (66)

1. Alkondon M., and Albuquerque E.X. Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J. Neurophysiol. 86 (2001) 3043-3055
2. Alkondon M., Pereira E.F., Barbosa C.T., and Albuquerque E.X. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J. Pharmacol. Exp. Ther. 283 (1997) 1396-1411
3. Alkondon M., Pereira E.F., Eisenberg H.M., and Albuquerque E.X. Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. J. Neurosci. 19 (1999) 2693-2705
4. Atkinson L., Batten T.F., and Deuchars J. P2X(2) receptor immunoreactivity in the dorsal vagal complex and area postrema of the rat. Neuroscience 99 (2000) 683-696
5. Barazangi N., and Role L.W. Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. J. Neurophysiol. 86 (2001) 463-474
6. Bauer S., Hay M., Amilhon B., Jean A., and Moyse E. In vivo neurogenesis in the dorsal vagal complex of the adult rat brainstem. Neuroscience 130 (2005) 75-90
7. Beleslin D.B., and Krstic S.K. Further studies on nicotine-induced emesis: nicotinic mediation in area postrema. Physiol. Behav. 39 (1987) 681-686
8. Bertolino M., Kellar K.J., Vicini S., and Gillis R.A. Nicotinic receptor mediates spontaneous GABA release in the rat dorsal motor nucleus of the vagus. Neuroscience 79 (1997) 671-681
9. Cai Y., Hay M., and Bishop V.S. Synaptic connections and interactions between area postrema and nucleus tractus solitarius. Brain Res. 724 (1996) 121-124
10. Clarke P.B., and Reuben M. Release of [3H]-noradrenaline from rat hippocampal synaptosomes by nicotine: mediation by different nicotinic receptor subtypes from striatal [3H]-dopamine release. Br. J. Pharmacol. 117 (1996) 595-606
11. Cordero-Erausquin M., Marubio L.M., Klink R., and Changeux J.P. Nicotinic receptor function: new perspectives from knockout mice. Trends Pharmacol. Sci. 21 (2000) 211-217
12. Dajas-Bailador F., and Wonnacott S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol. Sci. 25 (2004) 317-324
13. 2+ stores. J. Neurochem. 81 (2002) 606-614
14. De Filippi G., Baldwinson T., and Sher E. Nicotinic receptor modulation of neurotransmitter release in the cerebellum. Prog. Brain Res. 148 (2005) 307-320
15. Engelman H.S., and MacDermott A.B. Presynaptic ionotropic receptors and control of transmitter release. Nat. Rev., Neurosci. 5 (2004) 135-145
16. Ferguson A.V., and Bains J.S. Electrophysiology of the circumventricular organs. Front. Neuroendocrinol. 17 (1996) 440-475
17. Ferreira M., Ebert S.N., Perry D.C., Yasuda R.P., Baker C.M., Davila-Garcia M.I., Kellar K.J., and Gillis R.A. Evidence of a functional alpha7-neuronal nicotinic receptor subtype located on motoneurons of the dorsal motor nucleus of the vagus. J. Pharmacol. Exp. Ther. 296 (2001) 260-269
18. Fisher J.L., Pidoplichko V.I., and Dani J.A. Nicotine modifies the activity of ventral tegmental area dopaminergic neurons and hippocampal GABAergic neurons. J. Physiol. (Paris) 92 (1998) 209-213
19. Fong A.Y., Stornetta R.L., Foley C.M., and Potts J.T. Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J. Comp. Neurol. 493 (2005) 274-290
20. Frank M.G., Srere H., Ledezma C., O'Hara B., and Heller H.C. Prenatal nicotine alters vigilance states and AchR gene expression in the neonatal rat: implications for SIDS. Am. J. Physiol. Reg. Int. Comp. Physiol. 280 (2001) 1134-1140
21. 2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35 (2004) 1-8
22. Funahashi M., Mitoh Y., Kohjitani A., and Matsuo R. Role of the hyperpolarization-activated cation current (Ih) in pacemaker activity in area postrema neurons of rat brain slices. J. Physiol. 552 (2003) 135-148
23. Funahashi M., Mitoh Y., and Matsuo R. Nicotinic modulation of area postrema neuronal excitability in rat brain slices. Brain Res. 1017 (2004) 227-233
24. Funahashi M., Mitoh Y., and Matsuo R. Activation of presynaptic 5-HT3 receptors facilitates glutamatergic synaptic inputs to area postrema neurons in rat brain slices. Methods Find. Exp. Clin. Pharmacol. 26 (2004) 615-622
25. Funahashi M., Mitoh Y., Akaike T., and Matsuo R. Variety of morphological and electrophysiological properties of area postrema neurons in adult rat brain slices. Neurosci. Res. 54 (2006) 43-48
26. Guan J.L., Wang Q.P., Shioda S., Ochiai H., and Nakai Y. GABAergic synaptic innervation of catecholaminergic neurons in the area postrema of the rat. Acta. Anat. (Basel) 156 (1996) 46-52
27. Hay M. Subcellular mechanisms of area postrema activation. Clin. Exp. Pharmacol. Physiol. 28 (2001) 551-557
28. Hornby P.J. Central neurocircuitry associated with emesis. Am. J. Med. 111 Suppl. 8A (2001) 106S-112S
29. Ichikawa T., Ajiki K., Matsuura J., and Misawa H. Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J. Chem. Neuroanat. 13 (1997) 23-39
30. Jaszai J., Farkas L.M., Gallatz K., and Palkovits M. Effects of glutamate-induced excitotoxicity on calretinin-expressing neuron populations in the area postrema of the rat. Cell Tissue Res. 293 (1998) 227-233
31. Kawa K. Acute synaptic modulation by nicotinic agonists in developing cerebellar Purkinje cells of the rat. J. Physiol. 538 (2002) 87-102
32. Kawa K. Glycine receptors and glycinergic synaptic transmission in the deep cerebellar nuclei of the rat: a patch-clamp study. J. Neurophysiol. 90 (2003) 3490-3500
33. Kawa K. Presynaptic nicotinic receptors mediate robust GABA release in the autonomic medullary neurons of the rat. Jpn. J. Physiol. 55 (2005) S147 (Suppl.)
34. Kawai Y., and Senba E. Electrophysiological and morphological characterization of cytochemically-defined neurons in the caudal nucleus of tractus solitarius of the rat. Neuroscience 89 (1999) 1347-1355
35. Kiyosawa A., Katsurabayashi S., Akaike N., and Pang Z.P. Nicotine facilitates glycine release in the rat spinal dorsal horn. J. Physiol. 536 (2001) 101-110
36. Le Novere N., Corringer P.J., and Changeux J.P. The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J. Neurobiol. 53 (2002) 447-456
37. Léna C., Changeux J.-P., and Mulle C. Evidence for "preterminal" nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J. Neurosci. 13 (1993) 2680-2688
38. Lloyd G.K., and Williams M. Neuronal nicotinic acetylcholine receptors as novel drug targets. J. Pharmacol. Exp. Ther. 292 (2000) 461-467
39. Lucas-Meunier E., Fossier P., Baux G., and Amar M. Cholinergic modulation of the cortical neuronal network. Pflugers. Arch. 446 (2003) 17-29
40. Maggi L., Le Magueresse C., Changeux J.P., and Cherubini E. Nicotine activates immature "silent" connections in the developing hippocampus. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2059-2064
41. Mazda T., Yamamoto H., Fujimura M., and Fujimiya M. Gastric distension-induced release of 5-HT stimulates c-fos expression in specific brain nuclei via 5-HT3 receptors in conscious rats. Am. J. Physiol.: Gastrointest. Liver Physiol. 287 (2004) G228-G235
42. Morest D.K. A study of the structure of the area postrema with Golgi methods. Am. J. Anat. 107 (1960) 291-303
43. Mori M., Gahwiler B.H., and Gerber U. Beta-alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro. J. Physiol. 539 (2002) 191-200
44. Nabekura J., Katsurabayashi S., Kakazu Y., Shibata S., Matsubara A., Jinno S., Mizoguchi Y., Sasaki A., and Ishibashi H. Developmental switch from GABA to glycine release in single central synaptic terminals. Nat. Neurosci. 7 (2004) 17-23
45. Newton B.W., and Maley B.E. A comparison of GABA- and GAD-like immunoreactivity within the area postrema of the rat and cat. J. Comp. Neurol. 255 (1987) 208-216
46. Radcliffe K.A., Fisher J.L., Gray R., and Dani J.A. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann. N. Y. Acad. Sci. 868 (1999) 591-610
47. Riediger T., Schmid H.A., Lutz T., and Simon E. Amylin potently activates AP neurons possibly via formation of the excitatory second messenger cGMP. Am. J. Physiol.: Regul., Integr. Comp. Physiol. 281 (2001) R1833-R1843
48. Rinaman L. Postnatal development of hypothalamic inputs to the dorsal vagal complex in rats. Physiol. Behav. 79 (2003) 65-70
49. Roghani A., Shirzadi A., Kohan S.A., Edwards R.H., and Butcher L.L. Differential distribution of the putative vesicular transporter for acetylcholine in the rat central nervous system. Brain Res. Mol. Brain Res. 43 (1996) 65-76
50. Ruggiero D.A., Giuliano R., Anwar M., Stornetta R., and Reis D.J. Anatomical substrates of cholinergic-autonomic regulation in the rat. J. Comp. Neurol. 292 (1990) 1-53
51. Russier M., Kopysova I.L., Ankri N., Ferrand N., and Debanne D. GABA and glycine co-release optimizes functional inhibition in rat brainstem motoneurons in vitro. J. Physiol. 541 (2002) 123-137
52. Sahibzada N., Ferreira Jr. M., Williams B., Wasserman A., Vicini S., and Gillis R.A. Nicotinic ACh receptor subtypes on gastrointestinally projecting neurones in the dorsal motor vagal nucleus of the rat. J. Physiol. 545 (2002) 1007-1016
53. Shapiro R.E., and Miselis R.R. The central neural connections of the area postrema of the rat. J. Comp. Neurol. 234 (1985) 344-364
54. Strominger N.L., Hori N., Carpenter D.O., Tan Y., and Folger W.H. Effects of acetylcholine and GABA on neurons in the area postrema of Suncus murinus brainstem slices. Neurosci. Lett. 309 (2001) 77-80
55. Tanaka I., Ezure K., and Kondo M. Distribution of glycine transporter 2 mRNA-containing neurons in relation to glutamic acid decarboxylase mRNA-containing neurons in rat medulla. Neurosci. Res. 47 (2003) 139-151
56. Tribollet E., Bertrand D., Marguerat A., and Raggenbass M. Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 124 (2004) 405-420
57. Tseng C.J., Appalsamy M., Robertson D., and Mosqueda-Garcia R. Effects of nicotine on brain stem mechanisms of cardiovascular control. J. Pharmacol. Exp. Ther. 265 (1993) 1511-1518
58. Van Sickle M.D., Oland L.D., Mackie K., Davison J.S., and Sharkey K.A. Delta9-tetrahydrocannabinol selectively acts on CB1 receptors in specific regions of dorsal vagal complex to inhibit emesis in ferrets. Am. J. Physiol.: Gastrointest. Liver Physiol. 285 (2003) G566-G576
59. Vizi E.S., and Lendvai B. Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res. Rev. 30 (1999) 219-235
60. Wang J., Wang X., Irnaten M., Venkatesan P., Evans C., Baxi S., and Mendelowitz D. Endogenous acetylcholine and nicotine activation enhances GABAergic and glycinergic inputs to cardiac vagal neurons. J. Neurophysiol. 89 (2003) 2473-2481
61. Winzer-Serhan U.H., and Leslie F.M. Codistribution of nicotinic acetylcholine receptor subunit alpha3 and beta4 mRNAs during rat brain development. J. Comp. Neurol. 386 (1997) 540-554
62. Yang B., and Ferguson A.V. Orexin-A depolarizes dissociated rat area postrema neurons through activation of a nonselective cationic conductance. J. Neurosci. 22 (2002) 6303-6308
63. Zaninetti M., Tribollet E., Bertrand D., and Raggenbass M. Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motoneurons of the rat. Eur. J. Neurosci. 11 (1999) 2737-2748
64. 2+ permeation of stably transfected alpha 3/beta 4 neuronal nicotinic acetylcholine receptor. Mol. Pharmacol. 55 (1999) 970-981
65. Zhao L., Kuo Y.P., George A.A., Peng J.H., Purandare M.S., Schroeder K.M., Lukas R.J., and Wu J. Functional properties of homomeric, human alpha 7-nicotinic acetylcholine receptors heterologously expressed in the SH-EP1 human epithelial cell line. J. Pharmacol. Exp. Ther. 305 (2003) 1132-1141
66. Zoli M., Léna C., Picciotto M.R., and Changeux J.P. Identification of four classes of brain nicotinic receptors using beta2 mutant mice. J. Neurosci. 18 (1998) 4461-4472