The main olfactory bulb (MOB) is the first processing station of the olfactory pathway, where the axon terminals of sensory neurons establish excitatory synapses with the dendrites of mitral and tufted (M/T) cells. In the MOB the activity of the glutamatergic M/T cells is controlled by several types of GABAergic interneurons, including the granule and periglomerular cells. Our group discovered the heterogeneity of an additional interneuron type, the so called deep short-axon cells (dSACs), and revealed three distinct subpopulations. First, I will overview our results demonstrating the functional, morphological and molecular diversity of dSACs. Distinct molecular expression profiles of different dSAC subtypes will be also demonstrated, suggesting not only different roles in the MOB circuit, but forming the foundation of future subtype-specific genetic modifications. Later, I will summarize our recent results regarding the diversity in the cell surface distribution of GABAA receptors. By combining whole-cell recordings of mIPSCs and quantitative immunolocalization of synaptic GABAAR subunits we demonstrated that cerebellar stellate and MOB dSACs expressed only the α1 as synaptic α subunit, and their Zolpidem-sensitive mIPSCs had decay time constants (τw) of 4-5 ms. Nucleus reticularis thalami neurons expressed only the α3 as synaptic α subunit and exhibited slow, Zolpidem-insensitive mIPSCs (τw = 28 ms). In contrast, MOB external tufted cells contained two α subunit variants (α1 and α3) in their synapses. Quantitative analysis of multiple labeled immunofluorescent images revealed small within-cell, but large between-cell variability in synaptic α3:α1 ratios. This corresponded to large cell-to-cell variability in the decay (τw = 3-30 ms) and Zolpidem sensitivity of mIPSCs. Our results reveal a novel mechanism of generating diversity in the decay of IPSCs by independently varying the expression of different GABAAR subunits.
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