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The Journal of Neuroscience, November 22, 2006, 26(47):12274-12282; doi:10.1523/JNEUROSCI.2599-06.2006

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Cellular/Molecular
Differential Expression of I_A Channel Subunits Kv4.2 and Kv4.3 in Mouse Visual Cortical Neurons and Synapses

Andreas Burkhalter,¹ Yuri Gonchar,¹ Rebecca L. Mellor,² and Jeanne M. Nerbonne²

Departments of ¹Anatomy and Neurobiology and ²Molecular Biology and Pharmacology, Washington University School of Medicine, St. Louis, Missouri 63110

Correspondence should be addressed to Jeanne M. Nerbonne, Department of Molecular Biology and Pharmacology, Box 8103, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110. Email: jnerbonne{at}wustl.edu

In cortical neurons, pore-forming -subunits of the Kv4 subfamily underlie the fast transient outward K⁺ current (I_A). Considerable evidence has accumulated demonstrating specific roles for I_A channels in the generation of individual action potentials and in the regulation of repetitive firing. Although I_A channels are thought to play a role in synaptic processing, little is known about the cell type- and synapse-specific distribution of these channels in cortical circuits. Here, we used immunolabeling with specific antibodies against Kv4.2 and Kv4.3, in combination with GABA immunogold staining, to determine the cellular, subcellular, and synaptic localization of Kv4 channels in the primary visual cortex of mice, in which subsets of pyramidal cells express yellow fluorescent protein. The results show that both Kv4.2 and Kv4.3 are concentrated in layer 1, the bottom of layer 2/3, and in layers 4 and 5/6. In all layers, clusters of Kv4.2 and Kv4.3 immunoreactivity are evident in the membranes of the somata, dendrites, and spines of pyramidal cells and GABAergic interneurons. Electron microscopic analyses revealed that Kv4.2 and Kv4.3 clusters in pyramidal cells and interneurons are excluded from putative excitatory synapses, whereas postsynaptic membranes at GABAergic synapses often contain Kv4.2 and Kv4.3. The presence of Kv4 channels at GABAergic synapses would be expected to weaken inhibition during dendritic depolarization by backpropagating action potentials. The extrasynaptic localization of Kv4 channels near excitatory synapses, in contrast, should stabilize synaptic excitation during dendritic depolarization. Thus, the synapse-specific distribution of Kv4 channels functions to optimize dendritic excitation and the association between presynaptic and postsynaptic activity.

Key words: Kv4.2 subunit; Kv4.3 subunit; visual cortex; pyramidal cells; GABAergic neurons; excitatory synapses; inhibitory synapses; A-type K⁺ current

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Received June 20, 2006; revised Oct. 17, 2006; accepted Oct. 19, 2006.

Correspondence should be addressed to Jeanne M. Nerbonne, Department of Molecular Biology and Pharmacology, Box 8103, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110. Email: jnerbonne{at}wustl.edu

This article has been cited by other articles:

				J. M. Nerbonne, B. R. Gerber, A. Norris, and A. Burkhalter Electrical remodelling maintains firing properties in cortical pyramidal neurons lacking KCND2-encoded A-type K+ currents J. Physiol., March 15, 2008; 586(6): 1565 - 1579. [Abstract] [Full Text] [PDF]

				L.-Y. Chien, J.-K. Cheng, D. Chu, C.-F. Cheng, and M.-L. Tsaur Reduced Expression of A-Type Potassium Channels in Primary Sensory Neurons Induces Mechanical Hypersensitivity J. Neurosci., September 12, 2007; 27(37): 9855 - 9865. [Abstract] [Full Text] [PDF]

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