It is well established that the main intrinsic electrophysiological properties of relay cells, production of a low threshold burst upon release from hyperpolarized potential and production of a train of single spikes following stimulation from depolarized potentials, can be readily modeled using a single compartment. There is however another less well explored intrinsic electrophysiological characteristic of relay cells which models have not yet accounted for: at somatic potentials near spike threshold, relay cells produce a fast ragged high threshold oscillation in somatic voltage. Optical [Ca2+] imaging and pharmacological tests indicate this oscillation correlates with a high threshold Ca2+ current in the dendrites. Here we present the development of a new compartment model of the thalamic relay cell guided by the simultaneous constraints that it must produce the familiar regular spiking relay mode and low threshold rebound bursts which characterize these cells, as well as the less-studied fast oscillation occurring at near-threshold holding potentials. We arrive at a model cell which is capable of the production isolated high threshold Ca2+ spikes in distal branch segments, driven by a rapidly inactivating intermediate-threshold Ca2+ channel. Further, the model produces the low threshold spike behavior of the relay cell without requiring high T-current density in the distal dendritic segments. The results thus support a new picture of the dendritic tree of relay cells which may have implications for the manner in which thalamic relay cells integrate descending input from the cortex.