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J Neurophysiol 86: 261-268, 2001;
0022-3077/01 $5.00
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The Journal of Neurophysiology Vol. 86 No. 1 July 2001, pp. 261-268
Copyright ©2001 by the American Physiological Society

Contribution of the Hyperpolarization-Activated Current (Ih) to Membrane Potential and GABA Release in Hippocampal Interneurons

Carl R. Lupica,1 James A. Bell,2 Alexander F. Hoffman,2 and Patricia L. Watson1

 1Department of Pharmacology, University of Arizona Health Sciences Center, Tucson, Arizona 85724; and  2The National Institute on Drug Abuse, Intramural Research Program, Baltimore, Maryland 21224

Lupica, Carl R., James A. Bell, Alexander F. Hoffman, and Patricia L. Watson. Contribution of the Hyperpolarization-Activated Current (Ih) to Membrane Potential and GABA Release in Hippocampal Interneurons. J. Neurophysiol. 86: 261-268, 2001. Intrinsic GABAergic interneurons provide inhibitory input to the principal neurons of the hippocampus. The majority of interneurons located in stratum oriens (s.o.) of the CA1 region express the hyperpolarization-activated cation current known as Ih. In an effort to elucidate the role of this current in regulating the baseline excitability of these neurons and its participation in the regulation of the release of GABA onto CA1 pyramidal neurons, we utilized whole cell electrophysiological recordings from both populations of cells. In voltage-clamp experiments, hyperpolarization of the interneuron membrane initiated a large inward current with an estimated activation threshold of 51.6 ± 7.6 mV and a half-maximal voltage of -73.0 ± 7.0 mV. This current was blocked by bath application of the Ih inhibitors ZD 7288 (50 µM) or cesium (2 mM). Current-clamp experiments at the interneuron resting membrane potential (-61.3 ± 1.2 mV) revealed a significant hyperpolarization, a decrease in the rate of spontaneous action potential discharge, an increase in the cellular input resistance, and the elimination of rebound afterdepolarizations during blockade of Ih with ZD 7288 (50 µM). The hyperpolarizing effect of ZD 7288 was also substantially larger in interneurons clamped near -80 mV using current injection through the pipette. In addition to neurons exhibiting Ih, recordings were obtained from a small population of s.o. interneurons that did not exhibit this current. These cells demonstrated resting membrane potentials that were significantly more negative (-73.6 ± 5.5 mV) than those observed in neurons expressing Ih, suggesting that this current contributes to more depolarized membrane potentials in these cells. Recordings from postsynaptic pyramidal neurons demonstrated that blockade of Ih with ZD 7288 caused a substantial reduction (~43%) in the frequency of spontaneous action potential-dependent inhibitory postsynaptic currents (IPSCs), without altering their average amplitude. However, miniature action-potential-independent IPSC frequency, amplitude, and decay kinetics were unaltered by ZD 7288. These data suggest that Ih is active at the resting membrane potential in s.o. interneurons and as a result contributes to the spontaneous activity of these cells and to the tonic inhibition of CA1 pyramidal neurons in the hippocampus.




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