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The Journal of Neuroscience, May 28, 2008, 28(22):5846-5860; doi:10.1523/JNEUROSCI.0835-08.2008

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Behavioral/Systems/Cognitive
The h Channel Mediates Location Dependence and Plasticity of Intrinsic Phase Response in Rat Hippocampal Neurons

Rishikesh Narayanan and Daniel Johnston

Center for Learning and Memory, The University of Texas at Austin, Austin, Texas 78712

Correspondence should be addressed to Dr. Daniel Johnston, Center for Learning and Memory, The University of Texas at Austin, 1, University Station Stop, C7000, Austin, TX 78712-0805. Email: djohnston{at}mail.clm.utexas.edu

The presence of phenomenological inductances in neuronal membrane has been known for more than one-half a century. Despite this, the dramatic contributions of such inductive elements to the amplitude and, especially, phase of neuronal impedance, and their roles in modulating temporal dynamics of neuronal responses have surprisingly remained unexplored. In this study, we demonstrate that the h channel contributes a location-dependent and plastic phenomenological inductive component to the input impedance of CA1 pyramidal neurons. Specifically, we show that the h channels introduce an apparent negative delay in the local voltage response of these neurons with respect to the injected current within the theta frequency range. The frequency range and the extent of this lead expand with increases in h current either through hyperpolarization, or with increasing distance of dendritic location from the soma. We also demonstrate that a spatially widespread increase in this inductive phase component accompanies long-term potentiation. Finally, using impedance analysis, we show that both location and activity dependence of intrinsic phase response are attributable not to changes in a capacitive or a leak component, but to changes in h-channel properties. Our results suggest that certain voltage-gated ion channels can differentially regulate internal time delays within neurons, thus providing them with an independent control mechanism in temporal coding of neuronal information. Our analyses and results also establish impedance as a powerful measure of intrinsic dynamics and excitability, given that it quantifies temporal relationships among signals and excitability as functions of input frequency.

Key words: activity-dependent plasticity; dendrite; h channel; hippocampus; impedance phase; inductance; temporal coding

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Received Feb. 25, 2008; revised April 25, 2008; accepted April 28, 2008.

Correspondence should be addressed to Dr. Daniel Johnston, Center for Learning and Memory, The University of Texas at Austin, 1, University Station Stop, C7000, Austin, TX 78712-0805. Email: djohnston{at}mail.clm.utexas.edu

This article has been cited by other articles:

				B. N. Routh, D. Johnston, K. Harris, and R. A. Chitwood Anatomical and Electrophysiological Comparison of CA1 Pyramidal Neurons of the Rat and Mouse J Neurophysiol, October 1, 2009; 102(4): 2288 - 2302. [Abstract] [Full Text] [PDF]

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