Oxytocin (OT) and vasopressin (VP) synthesizing magnocellular cells (MNCs) in the supraoptic nucleus (SON) display distinct firing patterns during the physiological demands for these hormones. Depolarizing afterpotentials (DAPs) in these neurons are involved in controlling phasic bursting in VP neurons. Our whole cell recordings demonstrated a Cs⁺-resistant fast DAP (fDAP; decay tau = ~200ms) that has not been previously reported, in addition to the well known Cs⁺-sensitive slower DAP (sDAP; decay tau = ~2 s). Immunoidentification of recorded neurons revealed that all VP neurons, but only 16 % of OT neurons, expressed the fDAP. The activation of the fDAP required influx of Ca⁺⁺ through voltage-gated Ca⁺⁺ channels, as it was strongly suppressed in Ca⁺⁺-free extracellular solution or by bath application of Cd⁺⁺. Additionally, the current underlying the fDAP (I_fDAP) is a Ca⁺⁺-activated current, rather than a Ca⁺⁺ current per se, as it was abolished by strongly buffering intracellular Ca⁺⁺with BAPTA. The I-V relationship of the I_fDAP was linear at potentials <-60 mV but showed pronounced outward rectification near -50 mV. I_fDAP is sensitive to changes in extracellular Na⁺ and K⁺, but not Cl^-. A blocker of Ca⁺⁺-activated non-selective cation (CAN) currents, flufenamic acid, blocked the fDAP, suggesting the involvement of a CAN current in the generation of fDAP in VP neurons. We speculate that the two DAPs have different roles in generating after burst discharges and could play important roles in determining the distinct firing properties of VP neurons in the SON neurons.