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The Journal of Neuroscience, May 23, 2007, 27(21):5654-5663; doi:10.1523/JNEUROSCI.5495-06.2007

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Cellular/Molecular
Activation of Group I Metabotropic Glutamate Receptors on Main Olfactory Bulb Granule Cells and Periglomerular Cells Enhances Synaptic Inhibition of Mitral Cells

Hong-Wei Dong,¹ Abdallah Hayar,² and Matthew Ennis¹

¹Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, and ²Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205

Correspondence should be addressed to Hong-Wei Dong, Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, TN 38163. Email: hdong5{at}utmem.edu

Granule and periglomerular cells in the main olfactory bulb express group I metabotropic glutamate receptors (mGluRs). The group I mGluR agonist 3,4-dihydroxyphenylglycine (DHPG) increases GABAergic spontaneous IPSCs (sIPSCs) in mitral cells, yet the presynaptic mechanism(s) involved and source(s) of the IPSCs are unknown. We investigated the actions of DHPG on sIPSCs and TTX-insensitive miniature IPSCs (mIPSCs) recorded in mitral and external tufted cells in rat olfactory bulb slices. DHPG, acting at mGluR1 and mGluR5, increased the rate but not amplitude of sIPSCs and mIPSCs in both cell types. The increase in mIPSCs depended on voltage-gated Ca²⁺ channels but persisted when ionotropic glutamate receptors and sodium spikes were blocked. Focal DHPG puffs onto granule cells or bath application after glomerular layer (GL) excision failed to increase mIPSCs in mitral cells. Additionally, GL excision reduced sIPSCs in mitral cells by 50%, suggesting that periglomerular cells exert strong tonic GABAergic inhibition of mitral cells. In contrast, GL DHPG puffs readily increased mIPSCs. These findings indicate that DHPG-evoked GABA release from granule cells requires spikes, whereas in the GL, DHPG facilitates periglomerular cell GABA release via both spike-dependent and spike-independent presynaptic mechanisms. We speculate that mGluRs amplify spike-driven lateral inhibition through the mitral-to-granule cell circuit, whereas GL mGluRs may play a more important role in amplifying intraglomerular inhibition after subthreshold input.

Key words: GABA; glutamate; periglomerular cells; external tufted cells; olfaction; rat

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Received Dec. 19, 2006; revised April 4, 2007; accepted April 6, 2007.

Correspondence should be addressed to Hong-Wei Dong, Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, TN 38163. Email: hdong5{at}utmem.edu

This article has been cited by other articles:

				J. B. Castro and N. N. Urban Subthreshold Glutamate Release from Mitral Cell Dendrites J. Neurosci., May 27, 2009; 29(21): 7023 - 7030. [Abstract] [Full Text] [PDF]

				Q. Nai, H.-W. Dong, A. Hayar, C. Linster, and M. Ennis Noradrenergic Regulation of GABAergic Inhibition of Main Olfactory Bulb Mitral Cells Varies as a Function of Concentration and Receptor Subtype J Neurophysiol, May 1, 2009; 101(5): 2472 - 2484. [Abstract] [Full Text] [PDF]

				H. Matsumoto, H. Kashiwadani, H. Nagao, A. Aiba, and K. Mori Odor-Induced Persistent Discharge of Mitral Cells in the Mouse Olfactory Bulb J Neurophysiol, April 1, 2009; 101(4): 1890 - 1900. [Abstract] [Full Text] [PDF]

				J. B. Castro, K. R. Hovis, and N. N. Urban Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors J. Neurosci., May 23, 2007; 27(21): 5664 - 5671. [Abstract] [Full Text] [PDF]

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