Light hyperpolarizes cone photoreceptors, causing synaptic voltage-gated Ca²⁺ channels to open infrequently. To understand neurotransmission under these conditions, we determined the number of L-type Ca²⁺ channel openings necessary for vesicle fusion at the cone ribbon synapse. Ca²⁺ currents ( I_Ca) were activated in voltage-clamped cones, and excitatory postsynaptic currents (EPSCs) were recorded from horizontal cells in the salamander retina slice preparation. Ca²⁺ channel number and single-channel current amplitude were calculated by mean-variance analysis of I_Ca. Two different comparisons—one comparing average numbers of release events to average I_Ca amplitude and the other involving deconvolution of both EPSCs and simultaneously recorded cone I_Ca—suggested that fewer than three Ca²⁺ channel openings accompanied fusion of each vesicle at the peak of release during the first few milliseconds of stimulation. Opening fewer Ca²⁺ channels did not enhance fusion efficiency, suggesting that few unnecessary channel openings occurred during strong depolarization. We simulated release at the cone synapse, using empirically determined synaptic dimensions, vesicle pool size, Ca²⁺ dependence of release, Ca²⁺ channel number, and Ca²⁺ channel properties. The model replicated observations when a barrier was added to slow Ca²⁺ diffusion. Consistent with the presence of a diffusion barrier, dialyzing cones with diffusible Ca²⁺ buffers did not affect release efficiency. The tight clustering of Ca²⁺ channels, along with a high-Ca²⁺ affinity release mechanism and diffusion barrier, promotes a linear coupling between Ca²⁺ influx and vesicle fusion. This may improve detection of small light decrements when cones are hyperpolarized by bright light.