Subthreshold oscillations and resonant behavior: Two manifestations of the same mechanism

The ability to generate subthreshold membrane potential oscillations in neurons from the inferior olive nucleus has been attributed to the electrical properties of these neurons, as well as to the properties of the network. In the present in vitro study we quantitatively characterized both intrinsic membrane and network properties that are directly involved in the oscillatory activity of olivary neurons in the guinea-pig. We also implemented an alternating current analysis to explore the resonance behavior of these neurons and to compare the resonant properties with the properties of the oscillatory activity. Spectral analysis, used for the quantitative characterization of the oscillatory activity under various experimental conditions, revealed that the pattern of the oscillatory activity is network specific rather than cell specific. These results are in agreement with the hypothesis that the oscillatory activity of olivary neurons is generated by a network of electrically coupled neurons. Using alternating current analysis, we found that impedance-frequency curves of olivary neurons demonstrate a peak impedance (resonance) at a frequency between 3 and 10 Hz, which corresponds to the frequency of the spontaneous oscillations. Like the spontaneous oscillations, this peak is tetrodotoxin insensitive, unaffected by K⁺ channel blockers and almost completely blocked in the presence of Ni²⁺ in the physiological solution. Increasing the temperature increases the resonance frequency, as well as the frequency of the spontaneous oscillations. These results show that the resonant behavior of individual neurons is the basis of the oscillatory behavior of the network and that resonance can serve as a lumped parameter which encodes the oscillatory tendency of a neuron.