At most synapses, presynaptic Ca²⁺ channels are positioned near vesicle release sites, and increasing this distance reduces synaptic strength. We examined the lateral membrane mobility of presynaptic L-type Ca²⁺ channels at photoreceptor ribbon synapses of the tiger salamander (Ambystoma tigrinum) retina. Movements of individual Ca²⁺ channels were tracked by coupling quantum dots to an antibody against the extracellular α₂δ₄ Ca²⁺ channel subunit. α₂δ₄ antibodies labeled photoreceptor terminals and colocalized with antibodies to synaptic vesicle glycoprotein 2 and voltage-gated Ca²⁺ channel 1.4 (Ca_V1.4) α₁ subunits. The results show that Ca²⁺ channels are dynamic and move within a confined region beneath the synaptic ribbon. The size of this confinement area is regulated by actin and membrane cholesterol. Fusion of nearby synaptic vesicles caused jumps in Ca²⁺ channel position, propelling them toward the outer edge of the confinement domain. Channels rebounded rapidly toward the center. Thus, although Ca_V channels are mobile, molecular scaffolds confine them beneath the ribbon to maintain neurotransmission even at high release rates.