Disynaptic amplification of metabotropic glutamate receptor 1 responses in the olfactory bulb

Journal of Neuroscience

Volumn 27, Issue 1, 2007, Pages 132-140

  De Saint Jan, Didier ^a,b   Westbrook, Gary L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b INSERM   (France)

Author keywords

Glomerulus; Glutamate spillover; mGluR; Mitral cell; Olfactory bulb; Synaptic transmission

Indexed keywords

METABOTROPIC RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITE; EVOKED SOMATOSENSORY RESPONSE; EXCITATION; HORMONE RELEASE; MITRAL CELL; MOUSE; NONHUMAN; OLFACTORY BULB; PATCH CLAMP; PRIORITY JOURNAL; SENSORY NERVE; SENSORY STIMULATION; SYNAPTIC TRANSMISSION;

AGING; ANIMALS; CELLS, CULTURED; GLUTAMIC ACID; MICE; MICE, KNOCKOUT; NERVE NET; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; OLFACTORY BULB; RECEPTORS, METABOTROPIC GLUTAMATE; SMELL; SYNAPTIC TRANSMISSION;

EID: 33846132270     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2439-06.2007     Document Type: Article

References (60)

1. Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, Schaefer AT (2004) Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44:865-876.
2. Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48:417-430.
3. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29:83-120.
4. Aroniadou-Anderjaska V, Ennis M, Shipley MT (1997) Glomerular synaptic responses to olfactory nerve input in rat olfactory bulb slices. Neuroscience 79:425-434.
5. Axel R (2005) Scents and sensibility: a molecular logic of olfactory perception (Nobel lecture). Angew Chem Int Ed Engl 44:6110-6127.
6. Batchelor AM, Garthwaite J (1997) Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385:74-77.
7. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P (1993) The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
8. Bhandawat V, Reisert J, Yau KW (2005) Elementary response of olfactory receptor neurons to odorants. Science 308:1931-1934.
9. Brasnjo G, Otis TS (2001) Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron 31:607-616.
10. Buck LB (2005) Unraveling the sense of smell (Nobel lecture). Angew Chem Int Ed Engl 44:6128-6140.
11. Carlson GC, Shipley MT, Keller A (2000) Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20:2011-2021.
12. Chao TI, Kasa P, Wolff JR (1997) Distribution of astroglia in glomeruli of the rat main olfactory bulb: exclusion from the sensory subcompartment of neuropil. J Comp Neurol 388:191-210.
13. Charpak S, Gahwiler BH (1991) Glutamate mediates a slow synaptic response in hippocampal slice cultures. Proc Biol Sci 243:221-226.
14. Charpak S, Mertz J, Beaurepaire E, Moreaux L, Delaney K (2001) Odor-evoked calcium signals in dendrites of rat mitral cells. Proc Natl Acad Sci USA 98:1230-1234.
15. Chen WR, Shepherd GM (1997) Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb. Brain Res 745:189-196.
16. Christie JM, Westbrook GL (2006) Lateral excitation within the olfactory bulb. J Neurosci 26:2269-2277.
17. Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL (2005) Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 46:761-772.
18. Clements JD, Lester RA, Tong G, Jahr CE, Westbrook GL (1992) The time course of glutamate in the synaptic cleft. Science 258:1498-1501.
19. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F, Collingridge GL, Crépel F (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237-243.
20. Cull-Candy SG, Leszkiewicz DN (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 255:re16.
21. De Saint Jan D, Westbrook GL (2005) Detecting activity in olfactory bulb glomeruli with astrocyte recording. J Neurosci 25:2917-2924.
22. Dubnau J, Chiang AS, Tully T (2003) Neural substrates of memory: from synapse to system. J Neurobiol 54:238-253.
23. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar Purkinje neurons. Neuron 36:1159-1167.
24. Ennis M, Zimmer LA, Shipley MT (1996) Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. NeuroReport 7:989-992.
25. Ennis M, Zhu M, Heinbockel T, Hayar A (2006) Olfactory nerve-evoked metabotropic glutamate receptor-mediated synaptic responses in rat olfactory bulb mitral cells. J Neurophysiol 95:2233-2241.
26. Fletcher ML, Smith AM, Best AR, Wilson DA (2005) High-frequency oscillations are not necessary for simple olfactory discriminations in young rats. J Neurosci 25:792-798.
27. Friedrich RW (2006) Mechanisms of odor discrimination: neurophysiological and behavioral approaches. Trends Neurosci 29:40-47.
28. Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291:889-894.
29. Giustetto M, Bovolin P, Fasolo A, Bonino M, Cantino D, Sassoe-Pognetto M (1997) 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.
30. Hayar A, Karnup S, Ennis M, Shipley MT (2004) External tufted cells: a major excitatory element that coordinates glomerular activity. J Neurosci 24:6676-6685.
31. Heinbockel T, Heyward P, Conquet F, Ennis M (2004) Regulation of main olfactory bulb mitral cell excitability by metabotropic glutamate receptor mGluR1. J Neurophysiol 92:3085-3096.
32. Hormuzdi SG, Pais I, LeBeau FEN, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H (2001) Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31:487-495.
33. Huang YH, Sinha SR, Tanaka K, Rothstein JD, Bergles DE (2004) Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J Neurosci 24:4551-4559.
34. Isaacson JS (1999) Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23:377-384.
35. Kasowski HJ, Kim H, Greer CA (1999) Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274.
36. Khan RM, Sobel N (2004) Neural processing at the speed of smell. Neuron 44:744-747.
37. Kim H, Greer CA (2000) The emergence of compartmental organization in olfactory bulb glomeruli during postnatal development. J Comp Neurol 422:297-311.
38. Lagier S, Carleton A, Lledo PM (2004) Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J Neurosci 24:4382-4392.
39. Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837-3847.
40. Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci 24:263-297.
41. LeMasurier M, Gillespie PG (2005) Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403-415.
42. Luo M, Katz LC (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32:1165-1179.
43. MacLeod K, Laurent G (1996) Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274:976-979.
44. Mayer ML, Westbrook GL (1985) The action of N-methyl-D-aspartic acid on mouse spinal neurones in culture. J Physiol (Lond) 361:65-90.
45. Miller LD, Petrozzino JJ, Connor JA (1995) G-protein-coupled receptors mediate a fast excitatory postsynaptic current in CA3 pyramidal neurons in hippocampal slices. J Neurosci 15:8320-8330.
46. Montague AA, Greer CA (1999) Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb. J Comp Neurol 405:233-246.
47. Murphy GJ, Glickfeld LL, Balsen Z, Isaacson JS (2004) Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals. J Neurosci 24:3023-3030.
48. Nowycky MC, Mori K, Shepherd GM (1981) Blockade of synaptic inhibition reveals long-lasting synaptic excitation in isolated turtle olfactory bulb. J Neurophysiol 46:649-658.
49. Rossi DJ, Alford S, Mugnaini E, Slater NT (1995) Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. J Neurophysiol 74:24-42.
50. Salin PA, Lledo PM, Vincent JD, Charpak S (2001) Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J Neurophysiol 85:1275-1282.
51. Schoppa NE, Westbrook GL (2001) Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31:639-651.
52. Schoppa NE, Westbrook GL (2002) AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5:1194-1202.
53. Schoppa NE, Kinzie JM, Sahara Y, Segerson TP, Westbrook GL (1998) Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18:6790-6802.
54. Sterling P (2004) How retinal circuits optimize the transfer of visual information. In: The visual neurosciences (Chalupa LM, Werner JS, eds), pp 234-250. Cambridge, MA: Bradford Books.
55. Takeuchi H, Kurahashi T (2005) Mechanism of signal amplification in the olfactory sensory cilia. J Neurosci 25:11084-11091.
56. Uchida N, Mainen ZF (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6:1224-1229.
57. Urban NN, Sakmann B (2002) Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J Physiol (Lond) 542:355-367.
58. van den Pol AN (1995) Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J Comp Neurol 359:253-271.
59. Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366-370.
60. Yuan Q, Knopfel T (2006) Olfactory nerve stimulation-evoked mGluR1 slow potentials, oscillations and calcium signaling in mouse olfactory bulb mitral cells. J Neurophysiol 95:3097-3104.