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The Journal of Neuroscience, August 17, 2005, 25(33):7538-7547; doi:10.1523/JNEUROSCI.1927-05.2005

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Cellular/Molecular
High-Concentration Rapid Transients of Glutamate Mediate Neural-Glial Communication via Ectopic Release

Ko Matsui,¹ Craig E. Jahr,¹ and Maria E. Rubio²

¹Vollum Institute, Oregon Health and Science University, Portland, Oregon 97239, and ²Department of Physiology and Neurobiology, University of Connecticut, Storrs, Connecticut 06269

Until recently, communication from neurons to astrocytes was thought to be mediated by low-concentration transients of glutamate caused by spillover from the synaptic cleft. However, quantal events recorded in rat cerebellar Bergmann glial cells (BGs) have fast kinetics, comparable with those recorded in neurons. By combining outside-out patch recordings of BG AMPA receptors and quantitative electron microscopic analysis of glutamate receptor subunit 1 (GluR1) and GluR4 immunogold labeling measurements, at both the soma and membranes surrounding synapses, we estimate the absolute density of functional AMPA receptors. Using a kinetic model of BG AMPA receptors, we find that quantal events recorded in BGs are produced by high-concentration (1-1.5 mM), fast transients (0.5 ms decay) of glutamate, similar to transients within the synaptic cleft. Our results indicate that neural signaling to BGs is mediated by ectopic release of transmitter from presynaptic elements directly facing the BG membrane.

Key words: Bergmann glial cell; Purkinje cell; glutamate; ectopic release; synaptic transmission; immunogold electron microscopy

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Received May 13, 2005; revised July 6, 2005; accepted July 7, 2005.

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