A Model of Intracellular Theta Phase Precession Dependent on Intrinsic Subthreshold Membrane Currents

Abstract

A hippocampal place cell fires at an increasingly earlier phase in relation to the extracellular theta rhythm as a rodent moves through the place field. The present report presents a compartment model of a CA1 pyramidal cell that explains the increase in amplitude and the phase precession of intracellular theta oscillations, with the assumption that the cell receives an asymmetric ramp depolarization (<10 mV) in the place field and rhythmic inhibitory and/or excitatory synaptic driving. Intracellular subthreshold membrane potential oscillations (MPOs) increase in amplitude and frequency, and show phase precession within the place field. Theta phase precession and MPO power and frequency increase in the place field are caused by a shift in excitatory-inhibitory response, intrinsic theta-frequency resonance, and intrinsic oscillations that depend on voltage-dependent persistent Na(+) and slowly inactivating K(+) currents, but not on I(h). Phase precession is diminished when theta-frequency resonance is decreased. Simulated spikes fire near the peak of MPOs and precess similarly as the MPOs. The phase of the MPOs/spikes codes for distance in a one-dimensional place field, and phase precession is only weakly dependent on firing rate, running speed, or the duration needed to cross the place field. In addition, phase precession within the place field resumes quickly after disruption by maximal afferent pulse stimulation.