Theoretical and functional studies predicted a highly non-uniform distribution of voltage-gated ion channels on the neuronal surface. This was confirmed by recent immunolocalization experiments for Na+, Ca2+, hyperpolarization activated mixed cation and K+ channels. These experiments also indicated that some K+ channels were clustered in synaptic or non-synaptic membrane specializations. Here we analysed the subcellular distribution of Kv4.2 and Kv4.3 subunits in the rat main olfactory bulb at high resolution to address whether clustering characterizes their distribution, and whether they are concentrated in synaptic or non-synaptic junctions. The cell surface distribution of the Kv4.2 and Kv4.3 subunits is highly non-uniform. Strong Kv4.2 subunit-immunopositive clusters were detected in intercellular junctions made by mitral, external tufted and granule cells (GCs). We also found Kv4.3 subunit-immunopositive clusters in periglomerular (PGC), deep short-axon and GCs. In the juxtaglomerular region some calretinin-immunopositive glial cells enwrap neighboring PGC somata in a cap-like manner. Kv4.3 subunit clusters are present in the cap membrane that directly contacts the PGC, but not the one that faces the neuropil. In membrane specializations established by members of the same cell type, K+ channels are enriched in both membranes, whereas specializations between different cell types contain a high density of channels asymmetrically. None of the K+ channel-rich junctions showed any of the ultrastructural features of known chemical synapses. Our study provides evidence for highly non-uniform subcellular distributions of A-type K+ channels and predicts their involvements in novel forms of intercellular communication in the olfactory pathway.