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The glomeruli of the olfactory bulb are the first site of synaptic processing in the olfactory system. The glomeruli contain three types of neurons that are referred to collectively as juxtaglomerular (JG) cells: external tufted (ET), periglomerular (PG), and short axon (SA) cells. JG cells are thought to interact synaptically, but little is known about the circuitry linking these neurons or their functional roles in olfactory processing. Single and paired whole-cell recordings were performed to investigate these questions. ET cells spontaneously fired rhythmic spike bursts in the theta frequency range and received monosynaptic olfactory nerve (ON) input. In contrast, all SA and most PG cells lacked monosynaptic ON input. PG and SA cells exhibited spontaneous, intermittent bursts of EPSCs that were highly correlated with spike bursts of ET cells in the same but not in different glomeruli. Paired recording experiments demonstrated that ET cells provide monosynaptic excitatory input to PG/SA cells; the ET to PG/SA cell synapse is mediated by glutamate. ET cells thus are a major excitatory linkage between ON input and other JG cells. Spontaneous bursting is highly correlated among ET cells of the same glomerulus, and ET cell activity remains correlated when all fast synaptic activity is blocked. The findings suggest that multiple, synchronously active ET cells synaptically converge onto single PG/SA cells. Synchronous ET cell bursting may function to amplify transient sensory input and coordinate glomerular output.

External Tufted Cells: A Major Excitatory Element That Coordinates Glomerular Activity