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The Journal of Neuroscience, November 22, 2006, 26(47):12143-12151; doi:10.1523/JNEUROSCI.2667-06.2006

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Cellular/Molecular
Deletion of Kv4.2 Gene Eliminates Dendritic A-Type K⁺ Current and Enhances Induction of Long-Term Potentiation in Hippocampal CA1 Pyramidal Neurons

Xixi Chen,^1 * Li-Lian Yuan,^2 * Cuiping Zhao,² Shari G. Birnbaum,³ Andreas Frick,⁴ Wonil E. Jung,⁵ Thomas L. Schwarz,^5,6 J. David Sweatt,⁷ and Daniel Johnston¹

¹Center for Learning and Memory, University of Texas at Austin, Austin, Texas 78712, ²Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455, ³Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, Texas 75390, ⁴Department of Cell Physiology, Max Plank Institute for Medical Research, D-69120 Heidelberg, Germany, ⁵Department of Molecular and Cellular Physiology, Stanford University, Stanford, California 94305, ⁶Program in Neurobiology, Children's Hospital, Harvard Medical School, Boston, Massachusetts 02115, and ⁷Department of Neurobiology, University of Alabama at Birmingham, Birmingham, Alabama 35294

Correspondence should be addressed to Daniel Johnston, Center for Learning and Memory, University of Texas at Austin, Austin, TX 78712. Email: djohnston{at}mail.clm.utexas.edu

Dendritic, backpropagating action potentials (bAPs) facilitate the induction of Hebbian long-term potentiation (LTP). Although bAPs in distal dendrites of hippocampal CA1 pyramidal neurons are attenuated when propagating from the soma, their amplitude can be increased greatly via downregulation of dendritic A-type K⁺ currents. The channels that underlie these currents thus may represent a key regulatory component of the signaling pathways that lead to synaptic plasticity. We directly tested this hypothesis by using Kv4.2 knock-out mice. Deletion of the Kv4.2 gene and a loss of Kv4.2 protein resulted in a specific and near-complete elimination of A-type K⁺ currents from the apical dendrites of CA1 pyramidal neurons. The absence of dendritic Kv4.2-encoded A-type K⁺ currents led to an increase of bAP amplitude and an increase of concurrent Ca²⁺ influx. Furthermore, CA1 pyramidal neurons lacking dendritic A-type K⁺ currents from Kv4.2 knock-out mice exhibited a lower threshold than those of wild-type littermates for LTP induction with the use of a theta burst pairing protocol. LTP triggered with the use of a saturating protocol, on the other hand, remained indistinguishable between Kv4.2 knock-out and wild-type neurons. Our results support the hypothesis that dendritic A-type K⁺ channels, composed of Kv4.2 subunits, regulate action potential backpropagation and the induction of specific forms of synaptic plasticity.

Key words: K⁺ channels; long-term potentiation; hippocampus; dendrites; backpropagating action potential; knock-out mouse

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Received June 23, 2006; revised Oct. 3, 2006; accepted Oct. 10, 2006.

Correspondence should be addressed to Daniel Johnston, Center for Learning and Memory, University of Texas at Austin, Austin, TX 78712. Email: djohnston{at}mail.clm.utexas.edu

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