Large diameter cells in rat deep cerebellar nuclei (DCN) can be distinguished according to the generation of a Transient or Weak rebound burst and the expression of T-type Ca2⁺ channel isoforms. We investigated the ionic basis for the distinction in burst phenotypes in rat DCN cells in vitro. Following a hyperpolarization Transient Burst cells generated a high frequency spike burst of up to 450 Hz while Weak Burst cells generated a lower frequency increase (<140 Hz) . Both cell types expressed a low voltage-activated (LVA) Ca²⁺ current near threshold for rebound burst discharge (-50 mV) that was consistent with T-type Ca²⁺ current, but on average seven times more current was recorded in Transient Burst cells. The number and frequency of spikes in rebound bursts was tightly correlated with the peak Ca²⁺ current at -50 mV, revealing a direct relationship between the availability of LVA Ca²⁺ current and spike output. Transient Burst cells exhibited a larger spike depolarizing afterpotential that was insensitive to blockers of voltage-gated Na⁺ or Ca²⁺ channels. In comparison, Weak Burst cells exhibited larger afterhyperpolarizations (AHPs) that reduced cell excitability and rebound spike output. The sensitivity of AHPs to Ca²⁺ channel blockers suggests that both LVA and high voltage-activated (HVA) Ca²⁺ channels trigger AHPs in Weak Burst compared to only HVA Ca²⁺ channels in Transient Burst cells. The two burst phenotypes in rat DCN cells thus derive in part from a difference in the availability of LVA Ca²⁺ current following a hyperpolarization, and a differential activation of AHPs that establish distinct levels of membrane excitability.