Regulation of main olfactory bulb mitral cell excitability by metabotropic glutamate receptor mGluR1

Journal of Neurophysiology

Volumn 92, Issue 5, 2004, Pages 3085-3096

  Heinbockel, Thomas ^a,b   Heyward, Philip ^c   Conquet, François ^d   Ennis, Matthew ^e  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d GlaxoSmithKline   (Switzerland)

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 3,5 DIHYDROXYPHENYLGLYCINE; 4 CARBOXY 2 METHYLPHENYLGLYCINE; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; CALCIUM CHANNEL; GLUTAMIC ACID; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST; POTASSIUM CHANNEL; RECEPTOR SUBTYPE; 3,4 DIHYDROXYPHENYLETHYLENE GLYCOL; 4 HYDROXY 3 METHOXYPHENYLETHYLENE GLYCOL; BETA GALACTOSIDASE; DRUG DERIVATIVE; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1; METABOTROPIC RECEPTOR; PRIMER DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM CURRENT; CHELATION; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC POTENTIAL; FEMALE; GENE EXPRESSION; INTRACELLULAR CALCIUM CHELATION; KNOCKOUT MOUSE; LATENT PERIOD; MALE; MITRAL CELL; MOUSE; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; OLFACTORY BULB; OLFACTORY NERVE; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SPIKE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP; ANIMAL; CELL MEMBRANE POTENTIAL; DRUG EFFECT; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; GENETICS; IN VITRO STUDY; METABOLISM; NERVE CELL; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BASE SEQUENCE; BETA-GALACTOSIDASE; DNA PRIMERS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; FEMALE; MALE; MEMBRANE POTENTIALS; METHOXYHYDROXYPHENYLGLYCOL; MICE; NEURONS; OLFACTORY BULB; OLFACTORY NERVE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 14844300926     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00349.2004     Document Type: Article

References (66)

1. Anwyl R. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Rev 29: 83-120, 1999.
2. Aroniadou-Anderjaska VA, Ennis M, and Shipley MT. Glomerular synaptic responses to olfactory nerve input in rat olfactory bulb slices. Neuroscience 79: 425-434, 1997.
3. Aroniadou-Anderjaska V, Ennis M, and Shipley MT. Current-source density analysis in the rat olfactory bulb: laminar distribution of kainate/AMPA and NMDA receptor-mediated currents. J Neurophysiol 81: 15-28, 1999a.
4. Aroniadou-Anderjaska V, Ennis M, and Shipley MT. Dendrodendritic recurrent excitation in mitral cells of the rat olfactory bulb. J Neurophysiol 82: 489-494, 1999b.
5. Bandrowski AE, Huguenard JR, and Prince DA. Baseline glutamate levels affect group I and II mGluRs in layer V pyramidal neurons of rat sensorimotor cortex. J Neurophysiol 89: 1308-1316, 2003.
6. Bardoni R, Puopolo M, Magherini PC, and Belluzzi O. Potassium currents in periglomerular cells of frog olfactory bulb in vitro. Neurosci Lett 210: 95-98, 1996.
7. Carlson GC, Shipley MT, and Keller A. Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20: 2011-2021, 2000.
8. 2+ stores in cultured olfactory bulb neurons. J Neurophysiol 78: 2176-2185, 1997.
9. Chao TI, Kasa P, and Wolff JR. Distribution of astroglia in glomeruli of the rat main olfactory bulb: exclusion from the sensory compartment of neuropil. J Comp Neurol 388: 191-210, 1997.
10. Charpak S, Gähwiler BH, Do KQ, and Knöpfel T. Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature 347: 765-767, 1990.
11. Chavis P, Fagni L, Bockaert J, and Lansman JB. Modulation of calcium channels by metabotropic glutamate receptors in cerebellar granule cells. Neuropharmacology 34: 929-937, 1995.
12. Chen WR and Shepherd GM. Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb. Brain Res 745: 189-196, 1997.
13. Chiamulera C, Epping-Jordan MP, Zocchi A, Marcon C, Cottiny C, Tacconi S, Corsi M, Orzi F, and Conquet F. Reinforcing and locomotor stimulant effects of cocaine are absent in mGluR5 null mutant mice. Nat Neurosci 4: 873-874, 2001.
14. Clark BP, Baker SR, Goldsworthy J, Harris JR, and Kingston AE. 2-Methyl-4-carboxyphenylglycine (LY367385) selectively antagonizes metabotropic glutamate mGluR1 receptors. Bioorg Med Chem Lett 7: 2777-2870, 1997.
15. Congar P, Leinekugel X, Ben-Ari Y, and Crepel V. A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J Neurosci 17: 5366-5379, 1997.
16. Conn PJ and Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37: 205-237, 1997.
17. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Condé F, Collingridge GL, and Crépel F. Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372: 237-243, 1994.
18. 2+-activated nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol 72: 1561-1569, 1994.
19. Ennis M, Zhou FM, Ciombor KJ, Aroniadou-Anderjaska V, Hayar A, Borrelli E, Zimmer LA, Margolis F, and Shipley MT. Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. J Neurophysiol 86: 2986-2997, 2001.
20. Ennis M, Zimmer LA, and Shipley MT. Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. Neuroreport 7: 989-992, 1996.
21. Friedman D and Strowbridge BW. Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84: 39-50, 2000.
22. Friedrich R and Laurent G. Dynamic optimization of odor representations by slow temporal patterning of mitra cell activity. Science 291: 889-894, 2001.
23. 2+ in mitral cells of the olfactory bulb. J Neurophysiol 76: 563-570, 1996.
24. Guérineau NC, Bossu JL, Gähwiler BH, and Gerber U. Activation of a nonselective cationic conductance by metabotropic glutamatergic and muscarinic agonist in CA3 pyramidal neurons of the rat hippocampus. J Neurosci 15: 4395-4407, 1995.
25. + current by metabotropic glutamate and muscarinic receptors in rat CA3 cells: mediation by G-proteins. J Physiol 474: 27-33, 1994.
26. Hayar A, Karnup S, Shipley MT, and Ennis M. Synchronous activity among juxtaglomerular neurons of the rat main olfactory bulb (MOB) in vitro. Soc Neurosci Abstr 27: 459.4, 2001.
27. Heinbockel T and Ennis M. Metabotropic glutamate receptor mGluR1 directly and potently activates mitral cells in main olfactory bulb slices (Abstract). Chem Senses 11: A109, 2002.
28. Heinbockel T, Hayar A, Heyward PM, Shipley MT, and Ennis M. Neural activity is modulated by metabotropic glutamate receptors in rat olfactory bulb slices (Abstract). Chem Senses 26: 1065, 2001a.
29. Heinbockel T, Hayar A, Laaris N, Shipley MT, and Ennis M. Metabotropic glutamate receptors shape neuronal excitability and synaptic responsiveness in mouse olfactory bulb slices. Soc Neurosci Abstr 27: 623.5, 2001b.
30. Heyward P, Ennis M, Keller A, and Shipley MT. Membrane bistability in olfactory bulb mitral cells. J Neurosci 21: 5311-5320, 2001.
31. Isaacson JS. Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23: 377-384, 1999.
32. Isaacson JS and Strowbridge BW. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20: 749-761, 1998.
33. Kasowski HJ, Kim H, and Greer CA. Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407: 261-274, 1999.
34. Kauer JS. Olfactory processing: a time and place for everything. Curr Biol 8: R282-283, 1998.
35. Kay LM and Laurent G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2: 1003-1009, 1999.
36. 2+ exchange in rat basolateral amygdala neurones. J Physiol 499: 87-104, 1997.
37. Keller A, Yagodin S, Aroniadou-Anderjaska A, Zimmer LA, Ennis M, Sheppard NF, and Shipley MT. Functional organization of rat olfactory bulb glomeruli revealed by optical imaging. J Neurosci 18: 2602-2612, 1998.
38. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S, and Schoepp DD. LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37: 1-12, 1998.
39. Kinoshita A, Shigemoto R, Ohishi H, van der Putten H, and Mizuno N. Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol 393: 332-352, 1998.
40. Kinzie JM, Saugstad JA, Westbrook GL, and Segerson TP. Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neuroscience 69: 167-176, 1995.
41. Kinzie JM, Westbrook GL, and Segerson TP. Metabotropic glutamate receptors in the olfactory bulb. In: Metabotropic Glutamate Receptors and Brain Function, edited by Moroni F, Nicoletti F, and Pellegrini-Giampietro DE. London: Portland, 59-69, 1998.
42. Lee K and Boden PR. Characterization of the inward current induced by metabotropic glutamate receptor stimulation in rat ventromedial hypothalamic neurones. J Physiol 504.3: 649-663, 1997.
43. Luo M and Katz LC. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32: 1165-1179, 2001.
44. Marino MJ, Wittmann M, Bradley SR, Hubert GW, Smith Y, and Conn PJ. Activation of group I metabotropic glutamate receptors produces a direct excitation and disinhibition of GABAergic projection neurons in the substantia nigra pars reticulata. J Neurosci 21: 7001-7012, 2001.
45. Martin LJ, Blackstone CD, Huganir RL, and Price DL. Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9: 259-270, 1992.
46. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, and Nakanishi S. Sequence and expression of a metabotropic glutamate receptor. Nature 349: 760-765, 1991.
47. Petralia RS, Wang YX, Singh S, Wu C, Shi L, Wei J, and Wenthold RJ. A monoclonal antibody shows discrete cellular and subcellular localizations of mGluR1 alpha metabotropic glutamate receptors. J Chem Neuroanat 13: 77-93, 1997.
48. Puche AC and Shipley MT. Radial glia development in the mouse olfactory bulb. J Comp Neurol 434: 1-12, 2001.
49. Raggenbass M, Pierson P, Metzger D, and Alberi S. Action of a metabotropic glutamate receptor agonist in rat lateral septum: induction of a sodium-dependent inward aftercurrent. Brain Res 776: 75-87, 1997.
50. Rivadulla C, Martinez LM, Varela C, and Cudeiro J. Completing the corticofugal loop: a visual role for the corticogeniculate type 1 metabotropic glutamate receptor. J Neurosci 22: 2956-2962, 2002.
51. Sahara Y, Kubota T, and Ichikawa M. Cellular localization of metabotropic glutamate receptors mGluR1, 2/3, 5 and 7 in the main and accessory olfactory bulb of the rat. Neurosci Lett 312: 59-62, 2001.
52. Salin PA, Lledo PM, Vincent JD, and Charpak S. Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J Neurophysiol 85: 1275-1282, 2001.
53. Salt TE, Turner JP, and Kingston AE. Evaluation of agonists and antagonists acting at group I metabotropic glutamate receptors in the thalamus in vivo. Neuropharmacohgy 38: 1505-1510, 1999.
54. Saugstad JA, Kinzie JM, Shinohara MM, Segerson TP, and Westbrook GL. Cloning and expression of rat metabotropic glutamate receptor 8 reveals a distinct pharmacological profile. Mol Pharmacol 51: 119-125, 1997.
55. Schoepp DD, Jane DE, and Monn JA. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38: 1431-1476, 1999.
56. Schoppa NE and Westbrook GL. Modulation of mEPSCs in olfactory bulb mitral cells by metabotropic glutamate receptors. J Neurophysiol 78: 1468-1475, 1997.
57. Schoppa NE and Westbrook GL. Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31: 639-651, 2001.
58. Schoppa NE, Kinzie JM, Sahara Y, Segerson TP, and Westbrook GL. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18: 6790-6802, 1998.
59. Shigemoto R, Nakanishi S, and Mizuno N. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322: 121-135, 1992.
60. Spors H and Grinvald A. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34: 301-315, 2002.
61. Staub C, Vranesic I, and Knöpfel T. Responses to metabotropic glutamate receptor activation in cerebellar purkinje cells: induction of an inward current. Eur J Neurosci 4: 832-839, 1992.
62. Stuart GJ, Dodt HU, and Sakmann B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pfluegers 423: 511-518, 1993.
63. Tsien RY. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19: 2396-2404, 1980.
64. Trombley PQ and Westbrook GL. L-AP4 inhibits calcium currents and synaptic transmission via a G-protein-coupled glutamate receptor. J Neurosci 12: 2043-2050, 1992.
65. van den Pol A. Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J Comp Neurol 253-271, 1995.
66. Wada E, Shigemoto R, Kinoshita A, Ohishi H, and Mizuno N. Metabotropic glutamate receptor subtypes in axon terminals of projection fibers from the main and accessory olfactory bulbs: a light and electron microscopic immunohistochemical study in the rat. J Comp Neurol 393: 493-504, 1998.