Potassium channels comprise the most diverse family of ion channels and play critical
roles in a large variety of physiological and pathological processes. In addition
to their molecular diversity, variations in their distributions and densities on the
axo-somato-dendritic surface of neurons are key parameters in determining their functional
impact. Despite extensive electrophysiological and anatomical investigations, the
exact location and densities of most K(+) channels in small subcellular compartments
are still unknown. Here we aimed at providing a quantitative surface map of two delayed-rectifier
(Kv1.1 and Kv2.1) and one G-protein-gated inwardly rectifying (Kir3.2) K(+) channel
subunits on hippocampal CA1 pyramidal cells (PCs). Freeze-fracture replica immunogold
labelling was employed to determine the relative densities of these K(+) channel subunits
in 18 axo-somato-dendritic compartments. Significant densities of the Kv1.1 subunit
were detected on axon initial segments (AISs) and axon terminals, with an approximately
eight-fold lower density in the latter compartment. The Kv2.1 subunit was found in
somatic, proximal dendritic and AIS plasma membranes at approximately the same densities.
This subunit has a non-uniform plasma membrane distribution; Kv2.1 clusters are frequently
adjacent to, but never overlap with, GABAergic synapses. A quasi-linear increase in
the Kir3.2 subunit density along the dendrites of PCs was detected, showing no significant
difference between apical dendritic shafts, oblique dendrites or dendritic spines
at the same distance from the soma. Our results demonstrate that each subunit has
a unique cell-surface distribution pattern, and predict their differential involvement
in synaptic integration and output generation at distinct subcellular compartments.
