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J Neurophysiol (June 22, 2004). doi:10.1152/jn.00349.2004
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00349.2004v1
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Submitted on April 5, 2004
Accepted on June 21, 2004

Regulation of Main Olfactory Bulb Mitral Cell Excitability by Metabotropic Glutamate Receptor mGluR1

Thomas Heinbockel1*, Philip Heyward2, Francois Conquet3, and Matthew Ennis4

1 Department of Physiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland, USA
2 Department of Physiology, University of Otago, Dunedin, New Zealand
3 IBCM, GlaxoSmithKline Experimental Research, Lausanne, Switzerland
4 Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee, USA

* To whom correspondence should be addressed. E-mail: thein001{at}umaryland.edu.

In the rodent main olfactory bulb (MOB), mitral cells (MCs) express high levels of the Group I metabotropic glutamate receptor (mGluR) subtype, mGluR1. The significance of this receptor in modulating MC excitability is unknown. We investigated the physiological role of mGluR1 in regulating MC activity in rat and mouse MOB slices. The selective Group I agonist DHPG, but not Group II or III agonists, induced potent, dose-dependent and reversible depolarization and increased firing of MCs. These effects persisted in the presence of blockers of fast synaptic transmission, indicating that they are due to direct activation of mGluRs on MCs. Voltage clamp recordings showed that DHPG elicited a voltage-dependent inward current consisting of multiple components sensitive to potassium and calcium channel blockade and intracellular calcium chelation. MC excitatory responses to DHPG were absent in mGluR1 knockout mice, but persisted in mGluR5 knockout mice. Broad spectrum (LY341495, MCPG) as well as preferential mGluR1 (LY367385) antagonists blocked the excitatory effects of DHPG and also potently modulated MC spontaneous and olfactory nerve-evoked excitability. mGluR antagonists altered spontaneous membrane potential bistability, increasing the duration of the up- and down-states. mGluR antagonists also substantially attenuated MC responses to sensory input, decreasing the probability and increasing the latency of olfactory nerve-evoked spikes. These findings suggest that endogenous glutamate tonically modulates MC excitability and responsiveness to olfactory nerve input, and hence the operation of the MOB circuitry, via activation of mGluR1.




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