Differences in subthreshold resonance of hippocampal pyramidal cells and interneurons: the role of h-current and passive membrane characteristics

The intrinsic properties of distinct types of neuron play important roles in cortical network dynamics. One crucial determinant of neuronal behaviour is the cell's response to rhythmic subthreshold input, characterised by the input impedance, which can be determined by measuring the amplitude and phase of the membrane potential response to sinusoidal currents as a function of input frequency. In this study, we determined the impedance profiles of anatomically identified neurons in the CA1 region of the rat hippocampus (pyramidal cells as well as interneurons located in the stratum oriens, including OLM cells, fast-spiking perisomatic region-targeting interneurons and cells with axonal arbour in strata oriens and radiatum). The basic features of the impedance profiles, as well as the passive membrane characteristics and the properties of the sag in the voltage response to negative current steps, were cell-type specific. With the exception of fast-spiking interneurons, all cell types showed subthreshold resonance, albeit with distinct features. The HCN channel blocker ZD7288 (10 microM) eliminated the resonance and changed the shape of the impedance curves, indicating the involvement of the hyperpolarization-activated cation current I(h). Whole-cell voltage-clamp recordings uncovered differences in the voltage-dependent activation and kinetics of I(h) between different cell types. Biophysical modelling demonstrated that the cell-type specificity of the impedance profiles can be largely explained by the properties of I(h) in combination with the passive membrane characteristics. We conclude that differences in I(h) and passive membrane properties result in a cell-type-specific response to inputs at given frequencies, and may explain, at least in part, the differential involvement of distinct types of neuron in various network oscillations.