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The Journal of Neuroscience, February 16, 2005, 25(7):1750-1760; doi:10.1523/JNEUROSCI.4217-04.2005

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Cellular/Molecular
Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Jun Xu,1 Ning Kang,1 Li Jiang,2 Maiken Nedergaard,3 and Jian Kang1

1Department of Cell Biology and Anatomy, New York Medical College, Valhalla, New York 10595, 2The Center for Neurobiology and Behavior, Columbia University, New York, New York 10032, and 3The Center for Aging and Developmental Biology, Rochester University Medical Center, Rochester, New York 14642

The efficiency of neural circuits is enhanced not only by increasing synaptic strength but also by increasing intrinsic excitability. In contrast to the detailed analysis of long-term potentiation (LTP), less attention has been given to activity-dependent changes in the intrinsic neuronal excitability. By stimulating hippocampal CA1 pyramidal neurons with synaptic inputs correlating with postsynaptic neuronal spikes, we elicited an LTP of intrinsic excitability (LTP-IE) concurring with synaptic LTP. LTP-IE was manifested as a decrease in the action potential threshold that was attributable to a hyperpolarized shift in the activation curve of voltage-gated sodium channels (VGSCs) rather than activity-dependent changes in synaptic inputs or A-type K+ channels. Cell-attached patch recording of VGSC activities indicated such an activity-dependent change in VGSCs. Induction of LTP-IE was blocked by the NMDA receptor antagonist APV, intracellular BAPTA, the CaM kinase inhibitors KN-62 and autocamtide-2-related inhibitory peptide, and the protein synthesis inhibitors emetine and anisomycin. The results suggest that induction of LTP-IE shares a similar signaling pathway with the late phase of synaptic LTP and requires activation of the NMDA glutamate receptor subtype, Ca2+ influx, activity of CaM kinase II, and function of the protein synthesis. This new form of hippocampal neuronal plasticity could be a cellular correlate of learning and memory besides synaptic LTP.

Key words: long-term potentiation; intrinsic excitability; Na+ channel; NMDA receptors; CaM kinases; protein synthesis

Received July 1, 2004; revised December 30, 2004; accepted January 5, 2005.




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