In the olfactory bulb, axons of olfactory sensory neurons (OSNs) expressing the same olfactory receptor converge on specific glomeruli. These afferents form axodendritic synapses with mitral/tufted and periglomerular cell dendrites, whereas the dendrites of mitral/tufted cells and periglomerular interneurons form dendrodendritic synapses. The two types of intraglomerular synapses appear to be spatially isolated in subcompartments delineated by astrocyte processes. Because each astrocyte sends processes into a single glomerulus, we used astrocyte recording as an intraglomerular detector of neuronal activity. In glomerular astrocytes, a single shock in the olfactory nerve layer evoked a prolonged inward current, the major part of which was attributable to a barium-sensitive potassium current. The K+ current closely reflected the time course of depolarization of mitral/tufted cells, indicating that K+ accumulation mainly reflects the activity of mitral/tufted cells. The astrocyte K+ current was dependent on AMPA and NMDA receptors in mitral/tufted cells as well as on a previously undescribed metabotropic glutamate receptor 1 component. Block of the K+ current with barium unmasked a synaptic glutamate transporter current. Perhaps surprisingly, the transporter current had components caused by glutamate released at both olfactory nerve terminals and mitral/tufted cell dendrites. The time course of the transporter currents suggested that rapid synchronous glutamate release at OSN terminals triggers asynchronous glutamate release from mitral/tufted cells. Glomerular astrocyte recording provides a sensitive means to examine functional compartmentalization within and between olfactory bulb glomeruli.
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