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The Journal of Neuroscience, April 25, 2007, 27(17):4697-4706; doi:10.1523/JNEUROSCI.4699-06.2007

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Development/Plasticity/Repair
Localization of HCN1 Channels to Presynaptic Compartments: Novel Plasticity That May Contribute to Hippocampal Maturation

Roland A. Bender,^1 * Timo Kirschstein,^2 * Oliver Kretz,³ Amy L. Brewster,¹ Cristina Richichi,¹ Christiane Rüschenschmidt,⁴ Ryuichi Shigemoto,⁵ Heinz Beck,⁴ Michael Frotscher,³ and Tallie Z. Baram¹

¹Departments of Anatomy, Neurobiology, and Pediatrics, University of California, Irvine, Irvine, California 92697-4475, ²Department of Physiology, University of Rostock, D-18055 Rostock, Germany, ³Institute of Anatomy and Cell biology, University of Freiburg, D-76104 Freiburg, Germany, ⁴Department Epileptology, University of Bonn, Medical Center, D-53105 Bonn, Germany, and ⁵Division of Cerebral Structure, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8787, Japan

Correspondence should be addressed to Dr. Roland A. Bender, Institute of Anatomy I, University of Hamburg, D-20246 Hamburg. Email: r.bender{at}uke.uni-hamburg.de

Increasing evidence supports roles for the current mediated by hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, I_h, in hippocampal maturation and specifically in the evolving changes of intrinsic properties as well as network responses of hippocampal neurons. Here, we describe a novel developmental plasticity of HCN channel expression in axonal and presynaptic compartments: HCN1 channels were localized to axon terminals of the perforant path (the major hippocampal afferent pathway) of immature rats, where they modulated synaptic efficacy. However, presynaptic expression and functions of the channels disappeared with maturation. This was a result of altered channel transport to the axons, because HCN1 mRNA and protein levels in entorhinal cortex neurons, where the perforant path axons originate, were stable through adulthood. Blocking action potential firing in vitro increased presynaptic expression of HCN1 channels in the perforant path, suggesting that network activity contributed to regulating this expression. These findings support a novel developmentally regulated axonal transport of functional ion channels and suggest a role for HCN1 channel-mediated presynaptic I_h in hippocampal maturation.

Key words: ion channel; entorhinal cortex; synaptic plasticity; development; perforant path; neuronal activity

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Received Oct. 28, 2006; revised March 21, 2007; accepted March 22, 2007.

Correspondence should be addressed to Dr. Roland A. Bender, Institute of Anatomy I, University of Hamburg, D-20246 Hamburg. Email: r.bender{at}uke.uni-hamburg.de

This article has been cited by other articles:

				T. Tokay, M. Rohde, S. Krabbe, M. Rehberg, R. A. Bender, R. Kohling, and T. Kirschstein HCN1 channels constrain DHPG-induced LTD at hippocampal Schaffer collateral-CA1 synapses Learn. Mem., November 25, 2009; 16(12): 769 - 776. [Abstract] [Full Text] [PDF]

				M. Krause, Z. Yang, G. Rao, F. P. Houston, and C. A. Barnes Altered Dendritic Integration in Hippocampal Granule Cells of Spatial Learning-Impaired Aged Rats J Neurophysiol, June 1, 2008; 99(6): 2769 - 2778. [Abstract] [Full Text] [PDF]

				M. F. Nolan, J. T. Dudman, P. D. Dodson, and B. Santoro HCN1 Channels Control Resting and Active Integrative Properties of Stellate Cells from Layer II of the Entorhinal Cortex J. Neurosci., November 14, 2007; 27(46): 12440 - 12451. [Abstract] [Full Text] [PDF]

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