Simultaneous fluorescence imaging and electrophysiologic recordings were used to investigate the Ca²⁺ influx initiated by action potentials (APs) into dorsal cochlear nucleus (DCN) pyramidal cell (PC) and cartwheel cell (CWC) dendrites. Local application of Cd²⁺ blocked Ca²⁺ transients in PC and CWC dendrites, demonstrating that the Ca²⁺ influx was initiated by dendritic Ca²⁺ channels. In PCs, TTX eliminated the dendritic Ca²⁺ transients when APs were completely blocked. However, the Ca²⁺ influx could be partially recovered during an incomplete block of APs, or when a large depolarization was substituted for the blocked APs. In CWCs, dendritic Ca²⁺ transients evoked by individual APs, or simple spikes, were blocked by TTX and could be recovered during an incomplete block of APs or by a large depolarization. In contrast, dendritic Ca²⁺ transients evoked by complex spikes, a burst of APs superimposed upon a slow depolarization, were not blocked by TTX, despite eliminating the APs superimposed upon the slow depolarization. These results suggest two different mechanisms for the retrograde activation of dendritic Ca²⁺ channels: the first requires fast Na⁺ channel-mediated APs or a large somatic depolarization, whereas the second is independent of Na⁺ channel activation, requiring only the slow depolarization underlying complex spikes.