T-type Ca²⁺ channels give rise to low-threshold inward currents which are central determinants of neuronal excitability. The availability of T-type Ca²⁺ channels is strongly influenced by voltage-dependent inactivation and recovery from inactivation. Here, we show that native and cloned T-type Ca²⁺ channel subunits selectively encode specific aspects of prior membrane potential changes via a powerful modulation of the rates with which these channels recover from inactivation. Increasing the duration of subthreshold (-70 to -55 mV) conditioning depolarizations caused a pronounced slowing of subsequent recovery from inactivation of both cloned (Ca_v3.1-3.3) and native T-type channels (thalamic neurons). The scaling of recovery rates with increasing duration of conditioning depolarizations could be well described by a power law function. Different T-type channel isoforms exhibited overlapping but complementary ranges of recovery rates. Intriguingly, scaling of recovery rates was dramatically reduced in Ca_v3.2 and Ca_v3.3, but not Ca_v3.1 subunits when mock action potentials were superimposed on conditioning depolarizations. Our results suggest that different T-type channel subunits exhibit dramatic differences in scaling relationships, in addition to well-described differences in other biophysical properties. Furthermore, the availability of T-type channels is powerfully modulated over time, depending on the patterns of prior activity these channels have encountered. These data provide a novel mechanism for cellular short term plasticity on the millisecond to second time scale that relies on biophysical properties of specific T-type Ca²⁺ channel subunits.