The vestibulo-ocular and vestibulo-spinal network provides the ability to hold gaze fixed on an object during passive head movement. Within that network, most of the second-order neurons of the medial vestibular nucleus (MVNn) compute internal representations of head movement velocity in the horizontal plane. Our previous in vitro studies of the MVNn membrane properties indicated that they may play a major role in determining the dynamic properties of these neurons independently of their connectivity. The present study investigated that hypothesis at a theoretical level. Biophysical models of type A and B MVNn were developed. Two factors were found to be important in modeling tonic and phasic firing activity: the activation of the delayed potassium current and the rate of calcium flux. In addition, the model showed that the strength of the delayed potassium current may determine the different forms of action potentials observed experimentally. These two models (type A and B cells) were examined using depolarizing stimulation, random noise, step, ramp and sinusoidal inputs. For random noise, type A cells showed stable (regular) firing frequencies, while type B cells exhibited irregular activity. With step stimulation, the models exhibited tonic and phasic firing responses, respectively. Using ramp stimulations, frequency versus current curves showed a linear response for the type B neuron model. Finally, with sinusoidal stimulation of increasing frequencies, the type A model demonstrated a decrease in sensitivity, while the type B model exhibited an increase in sensitivity. These theoretical results support the hypothesis that MVNn intrinsic membrane properties specify various types of dynamic properties amongst these cells and therefore contribute to the wide range of dynamic responses which characterize the vestibulo-ocular and vestibulo-spinal network.