Elsevier

Neuroscience

Volume 84, Issue 1, 3 February 1998, Pages 37-48
Neuroscience

The K+ channel, Kv2.1, is apposed to astrocytic processes and is associated with inhibitory postsynaptic membranes in hippocampal and cortical principal neurons and inhibitory interneurons

https://doi.org/10.1016/S0306-4522(97)00519-8Get rights and content

Abstract

A variety of voltage-gated ion channels are expressed on principal cell dendrites and have been proposed to play a pivotal role in the regulation of dendritic excitability. Previous studies at the light microscopic level demonstrated that the K+ channel subunit Kv2.1 expression was polarized to the cell soma and dendrites of principal neurons throughout the central nervous system. Here, using double immunostaining we now show that Kv2.1 protein is similarly expressed in the majority of cortical and hippocampal parvalbumin, calbindin and somatostatin-containing inhibitory interneurons. At the electron microscopic level Kv2.1 immunoreactivity was primarily observed on the plasma membrane of the somata and proximal dendrites of both principal neurons and inhibitory interneurons; expression was low on smaller dendritic branches, and absent on axons and presynaptic terminals. Kv2.1 subunit expression was highly concentrated on the cell surface membrane immediately facing astrocytic processes. Kv2.1 expression was also concentrated in specific cytoplasmic compartments and on the subsurface cisterns underlying the plasma membrane facing astrocytes. In addition, Kv2.1 subunit immunoreactivity was associated with postsynaptic densities of a fraction of inhibitory symmetric synapses; while expression at asymmetric synapses was rare.

These data demonstrate that channels formed by Kv2.1 subunits are uniquely positioned on the soma and principal dendrites of both pyramidal cells and inhibitory interneurons at sites immediately adjacent to astrocytic processes. This close apposition to astrocytes will ensure a rapid removal and limit the influence of K+ released into the extracellular space. This expression pattern suggests that channels formed by Kv2.1 are poised to provide a role in the regulation of neuronal dendritic excitability.

Section snippets

Double immunostaining of Kv2.1 with parvalbumin, somatostatin and calbindin D28K

Adult Sprague–Dawley rats (Taconic, New York) were anaesthetized by volatile inhalation and perfused with ice-cold phosphate-buffered saline (PBS) followed by 4% paraformaldehyde in PBS, according to the NIH Animal Welfare Guidelines. The heads were decapitated and fixed overnight in 1% paraformaldehyde in PBS at 4°C. Serial sagittal sections (20 μm) of hippocampus and cortex were cut on a freezing microtome. Floating sections were incubated in a blocking solution of 10% normal goat serum, 0.2%

Kv2.1 expression in parvalbumin-, somatostatin-, calbindin D28K-immunoreactive interneurons

Previous studies have shown the Kv2.1 subunit to be expressed in the majority of principal neurons throughout the CNS including the hippocampus and cortex.7, 12, 19, 23The observation that the Kv2.1 protein was also widely expressed in presumed non-principal cells in the hippocampus and cortex, prompted us to first investigate Kv2.1 expression in defined populations of inhibitory interneurons in both the hippocampus and cortex. The calcium binding proteins, parvalbumin and calbindin D28K and

Discussion

The main findings of this study are: (1) Similar to the distribution in principal CNS neurons, Kv2.1 subunit protein is highly expressed across the somatodendritic axis of parvalbumin, somatostatin and calbindin D28K GABAergic inhibitory interneurons of the cortex and hippocampus. (2) Electron micrographs revealed that the distribution of Kv2.1 subunits on the plasma membrane of somata and proximal dendrites of both principal neurons and inhibitory interneurons was neither homogeneous nor

Conclusions

We have described that the dendritic expression of Kv2.1 subunits in principal neurons and inhibitory interneurons is not random across the somatodendritic axis but is specifically associated with intracellular subsurface cisterns and extracellularly with plasma membranes apposed to astrocytic processes. The clustered expression of Kv2.1 subunits on neuronal membranes adjacent to astrocytic processes strongly argues that K+ released into the extracellular space through these channels will be

Acknowledgements

The authors would like to thank Drs Mark Mayer and Vittorio Gallo for their comments on the manuscript.

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