Previous work has established that stellate cells of the medial entorhinal cortex produce prominent intrinsic subthreshold oscillations in the voltage response concentrated within the theta range (3–7 Hz). It has been speculated that these oscillations play an important role in vivo in establishing network behavior both in the entorhinal cortex and hippocampus. Consequently, it is important to investigate under what conditions theta oscillations in stellate cells can be generated and whether the spike-train power spectral density (PSD) also carries power at theta. We investigated the ability of stellate cells to generate theta oscillations in the presence of generic in vivo-like patterns of stimulation. Inputs were Poisson process-driven excitatory and inhibitory synaptic conductances or currents, introduced via dynamic clamp. We analyzed the subthreshold membrane oscillations and spike-train behavior in the presence of comparable synaptic conductance- or current-mediated membrane fluctuations. In the presence of conductance-based synapses, subthreshold oscillations are highly attenuated or entirely eliminated. Conversely, with current-based synapses stellate cells retain their ability to generate subthreshold oscillations in the theta band. These results also extend into the spiking regime, where only under current-based synapses does the PSD of the spike train show a prominent peak at theta. Furthermore, the peak in the spike-train PSD and spike clustering results from an increased probability of firing after a spike afterhyperpolarization and not directly from subthreshold oscillatory dynamics as has been previously suggested. Our results suggest that subthreshold oscillations may contribute less to in vivo response properties than has been hypothesized.