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.
