Hyperpolarization-activated cyclic nucleotide-gated (HCN) channels that generate Ih currents are widely distributed in the brain, and have been shown to contribute to various neuronal functions. In the present study, we investigated the functions of Ih in the motion sensitive projection neurons (WFV cells) of the superior colliculus, a pivotal visual center for detection of and orientating to salient objects. Combination of whole-cell recordings and immunohistochemical investigations suggested that HCN1 channels dominantly contribute to the I_h in WFV cells among HCN isoforms expressed in the sSC, and mainly located on their expansive dendritic trees. We found that blocking I_h suppressed the initiation of short- and fixed-latency dendritic spike responses, and led instead to long- and fluctuating-latency somatic spike responses to optic fiber stimulations. These results suggest that the dendritic I_h facilitates the dendritic initiation and/or propagation of action potentials and ensures that WFV cells generate spike responses to distal synaptic inputs in a sensitive and robustly time-locked manner, probably by acting as continuous depolarizing drive and fixing dendritic membrane potentials close to the spike threshold. These functions are different from known functions of dendritic I_h revealed in hippocampal and neocortical pyramidal cells, where they spatiotemporally limit the propagations of synaptic inputs along the apical dendrites by reducing dendritic membrane resistance. Thus, we have revealed new functional aspects of I_h, and these dendritic properties are likely critical for visual motion processing in these neurons.