Olfactory nerve-evoked, metabotropic glutamate receptor-mediated synaptic responses in rat olfactory bulb mitral cells

Journal of Neurophysiology

Volumn 95, Issue 4, 2006, Pages 2233-2241

  Ennis, Matthew ^a   Zhu, Mingyan ^a,c   Heinbockel, Thomas ^b   Hayar, Abdallah ^a,d  

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

^b HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; 4 CARBOXY 2 METHYLPHENYLGLYCINE; ASPARTIC ACID DERIVATIVE; GLUTAMATE TRANSPORTER; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR ANTAGONIST;

ANIMAL CELL; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; CONTROLLED STUDY; DENDRITE; ELECTROPHYSIOLOGY; MITRAL CELL; NERVE CELL PLASTICITY; NERVE ENDING; NERVE POTENTIAL; NERVE STIMULATION; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY NERVE; OSCILLATION; PATCH CLAMP; PRIORITY JOURNAL; RAT; STIMULATION; VOLTAGE CLAMP;

AMINO ACIDS; ANIMALS; ASPARTIC ACID; BENZOATES; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GLUTAMIC ACID; GLYCINE; MALE; NEURONAL PLASTICITY; NEURONS, AFFERENT; ODORS; OLFACTORY BULB; OLFACTORY NERVE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D2; RECEPTORS, GABA-B; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES; TACRINE; XANTHENES;

EID: 33646190466     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01150.2005     Document Type: Article

References (64)

1. Anson LC, Chen PE, Wyllie DJ, Colquhoun D, and Schoepfer R. Identification of amino acid residues of the NR2A subunit that control glutamate potency in recombinant NR1/NR2A NMDA receptors. J Neurosci 18: 581-589, 1998.
2. 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.
3. 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.
4. Aroniadou-Anderjaska V, Zhou FM, Priest CA, Ennis M, and Shipley MT. Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. J Neurophysiol 84: 1194-1203, 2000.
5. 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.
6. Baker H. Unilateral neonatal olfactory deprivation alters tyrosine hydroxylase expression but not aromatic amino acid decarboxylase or GABA immunoreactivity. Neuroscience 36: 761-771, 1990.
7. Baker H, Kawano T, Albert V, Joh TH, Reis DJ, and Margolis FL. Olfactory bulb dopamine neurons survive deafferentation-induced loss of tyrosine hydroxylase. Neuroscience 11: 605-615, 1984.
8. Baker H, Kawano T, Margolis FL, and Joh TH. Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3: 69-78, 1983.
9. Balcar VJ, Johnston GAR, and Twitchin B. Stereospecificity of the inhibition of L-glutamate and L-aspartate high affinity uptake in rat brain slices by threo-3-hydroxyasparate. J Neurochem 28: 1145-1146, 1977.
10. 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.
11. Batchelor AM and Garthwaite J. Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385: 74-77, 1997.
12. Berkowicz DA, Trombley PQ, and Shepherd GM. Evidence for glutamate as the olfactory receptor cell neurotransmitter. J Neurophysiol 71: 2557-2561, 1994.
13. Brunjes PC, Smith-Crafts LK, and McCarty R. Unilateral odor deprivation: effects on the development of olfactory bulb catecholamines and behavior. Dev Brain Res 22: 1-6, 1985.
14. Carlson GC, Shipley MT, and Keller A. Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20: 2011-2021, 2000.
15. Casabona G, Catania MV, Storto M, Ferraris N, Perroteau I, Fasolo A, Nicoletti F, and Bovolin P. Deafferentation up-regulates the expression of the mGlu1a metabotropic glutamate receptor protein in the olfactory bulb. Eur J Neurosci 10: 771-776, 1998.
16. Chen WR and Shepherd GM. Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb. Brain Res 745: 189-196, 1997.
17. De Saint Jan D and Westbrook GL. Detecting activity in olfactory bulb glomeruli with astrocyte recording. J Neurosci 25: 2917-2924, 2005.
18. Diamond JS and Jahr CE. Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation. J Neurophysiol 83: 2835-2843, 2000.
19. Dorries KM and Kauer JS. Relationships between odor-elicited oscillations in the salamander olfactory epithelium and olfactory bulb. J Neurophysiol 83: 754-765, 2000.
20. Duchamp-Viret D, Chaput MA, and Duchamp A. Odor response properties of rat olfactory receptor neurons. Science 284: 2171-2174, 1999.
21. 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.
22. 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.
23. Ferraris N, Perroteau I, De Marchis S, Fasolo A, and Bovolin P. Glutamatergic deafferentation of olfactory bulb modulates the expression of mGluR1a mRNA. Neuroreport 8: 1949-1953, 1997.
24. Friedman D and Strowbridge BW. Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84: 39-50, 2000.
25. Giustetto M, Bovolin P, Fasolo A, Bonino M, Cantino D, and Sassoe-Pognetto M. Glutamate receptors in the olfactory bulb synaptic circuitry: heterogeneity and synaptic localization of N-methyl-D-aspartate receptor subunit 1 and AMPA receptor subunit 1. Neuroscience 76: 787-798, 1997.
26. Hayar A, Heyward PM, Heinbockel T, Shipley MT, and Ennis M. Direct excitation of mitral cells via activation of alpha1-noradrenergic receptors in rat olfactory bulb slices. J Neurophysiol 86: 2173-2182, 2001.
27. Hayar A, Karnup S, Ennis M, and Shipley MT. External tufted cells: a major excitatory element that coordinates glomerular activity. J Neurosci 24: 6676-6685, 2004b.
28. Hayar A, Karnup S, Shipley MT, and Ennis M. Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J Neurosci 24: 1190-1199, 2004a.
29. Hayar A, Shipley MT, and Ennis M. Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms. J Neurosci 25: 8197-8208, 2005.
30. Heinbockel T, Heyward P, Conquet F, and Ennis M. Regulation of main olfactory bulb mitral cell excitability by metabotropic glutamate receptor mGluR1. J Neurophysiol 92: 3085-3096, 2004.
31. Heyward PM and Clarke IJ. A transient effect of estrogen on calcium currents and electrophysiological responses to gonadotropin-releasing hormone in ovine gonadotropes. Neuroendocrinology 62: 543-552, 1995.
32. Heyward PM, Ennis M, Keller A, and Shipley MT. Membrane bistability in olfactory bulb mitral cells. J Neurosci 21: 5311-5320, 2001.
33. Huang YH, Sinha SR, Tanaka K, Rothstein JD, and Bergles DE. Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J Neurosci 24: 4551-4559, 2004.
34. Isaacson JS. Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23: 377-384, 1999.
35. Isaacson JS and Strowbridge BW. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20: 749-761, 1998.
36. Jabaudon D, Shimamato K, Yasuda-Kamatani Y, Scanzini M, Gahwiler BH, and Gerber U. Inhibition of uptake unmasks rapid extracellular turnover of glutamate of non-vesicular origin. Proc Natl Acad Sci USA 96: 8733-8738, 1999.
37. Karakossian MH and Otis TS. Excitation of cerebellar interneurons by group I metabotropic glutamate receptors. J Neurophysiol 92: 1558-1565, 2004.
38. 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.
39. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, and Mishina M. Molecular diversity of the NMDA receptor channel. Nature 358: 36-41, 1992.
40. Laaris N and Ennis M. Distinct activity patterns evoked by activation of mitral/tufted cell and centrifugal fiber inputs to main olfactory bulb (MOB) granule cells. Soc Neurosci Abstr 561: 14, 2002.
41. Martin LJ, Blackstone CD, Huganir RL, and Price DL. Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9: 259-270, 1992.
42. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, and Nakanishi S. Sequence and expression of a metabotropic glutamate receptor. Nature 349: 760-765, 1991.
43. McBain CJ and Mayer ML. N-Methyl-D-aspartic acid receptor structure and function. Physiol Rev 74: 723-760, 1994.
44. Montague AA and Greer CA. Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb. J Comp Neurol 405: 233-246, 1999.
45. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, and Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature 354: 31-37, 1991.
46. Murphy GJ, Darcy DP, and Isaacson JS. Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit. Nat Neurosci 8: 354-364, 2005.
47. Mutoh H, Yuan Q, and Knopfel T. Long-term depression at olfactory nerve synapses. J Neurosci 25: 4252-4259, 2005.
48. Patneau DK and Mayer ML. Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10: 2385-2399, 1990.
49. Pin JP and Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1-26, 1995.
50. Reichelt W and Knopfel T. Glutamate uptake controls expression of a slow postsynaptic current mediated by mGluRs in cerebellar Purkinje cells. J Neurophysiol 87: 1974-1980, 2002.
51. Reisert J and Matthews HR. Response properties of isolated mouse olfactory receptor cells. J Physiol 530: 113-122, 2001.
52. 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.
53. 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.
54. Schoppa NE and Westbrook GL. Modulation of mEPSCs in olfactory bulb mitral cells by metabotropic glutamate receptors. J Neurophysiol 78: 1468-1475, 1997.
55. Schoppa NE and Westbrook GL. Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31: 639-651, 2001.
56. Shen K-Z and Johnson SW. A slow excitatory postsynaptic current mediated by G-protein-coupled metabotropic glutamate receptors in rat ventral tegmental dopamine neurons. Eur J Neurosci 9: 48-54, 1997.
57. 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.
58. Shipley MT, McLean JH, Zimmer LA, and Ennis M. The olfactory system. In: Integrated Systems of the CNS, edited by Swanson LW, Bjorklund A, and Hokfelt T. New York: Elsevier, 1996, pt. III, p. 469-575.
59. Tempia F, Alojado ME, Strata P, and Knopfel T. Characterization of the mGluR(1)-mediated electrical and calcium signaling in Purkinje cells of mouse cerebellar slices. J Neurophysiol 86: 1389-1397, 2001.
60. Tempia F, Miniaci MC, Anchisi D, and Strata P. Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J Neurophysiol 80: 520-528, 1998.
61. Utsumi M, Ohno K, Onchi H, Sato K, and Tohyama M. Differential expression patterns of three glutamate transporters (GLAST, GLT1 and EAAC1) in the rat main olfactory bulb. Brain Res Mol Brain Res 92: 1-11, 2001.
62. Van den Pol AN. Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J Comp Neurol 359: 253-271, 1995.
63. Wachowiak M, McGann JP, Heyward PM, Shao Z, Puche AC, and Shipley MT. Inhibition of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J Neurophysiol 94: 2700-2712, 2005.
64. Wang SS, Denk W, and Hausser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3: 1266-1273, 2000.