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Conductances Mediating Intrinsic Theta-Frequency Membrane Potential Oscillations in Layer II Parasubicular Neurons

Center for Studies in Behavioral Neurobiology, Department of Psychology, Concordia University, Montreal, Quebec, Canada

Submitted 10 March 2008; accepted in final form 18 September 2008

Ionic conductances that generate membrane potential oscillations in neurons of layer II of the parasubiculum were studied using whole cell current-clamp recordings in horizontal slices from the rat brain. Blockade of ionotropic glutamate and GABA synaptic transmission did not reduce the power of the oscillations, indicating that oscillations are not dependent on synaptic inputs. Oscillations were eliminated when cells were hyperpolarized 6–10 mV below spike threshold, indicating that they are mediated by voltage-dependent conductances. Application of TTX completely eliminated oscillations, suggesting that Na⁺ currents are required for the generation of the oscillations. Oscillations were not reduced by blocking Ca²⁺ currents with Cd²⁺ or Ca²⁺-free artificial cerebrospinal fluid, or by blocking K⁺ conductances with either 50 µM or 5 mM 4-aminopyridine (4-AP), 30 mM tetraethylammonium (TEA), or Ba²⁺(1–2 mM). Oscillations also persisted during blockade of the muscarinic-dependent K⁺ current, I_M, using the selective antagonist XE-991 (10 µM). However, oscillations were significantly attenuated by blocking the hyperpolarization-activated cationic current I_h with Cs⁺ and were almost completely blocked by the more potent I_h blocker ZD7288 (100 µM). Intrinsic membrane potential oscillations in neurons of layer II of the parasubiculum are therefore likely driven by an interaction between an inward persistent Na⁺ current and time-dependent deactivation of I_h. These voltage-dependent conductances provide a mechanism for the generation of membrane potential oscillations that can help support rhythmic network activity within the parasubiculum during theta-related behaviors.