Light produces a graded hyperpolarization in retinal photoreceptors that decreases their release of synaptic neurotransmitter. Cone photoreceptors use glutamate as a neurotransmitter with which to communicate with two types of bipolar cell. Activation of metabotropic glutamate receptors in 'On' bipolar cells initiates a second-messenger cascade that can amplify small synaptic inputs from cones. In contrast, it is not known how the ionotropic glutamate receptors that are activated in 'Off' bipolar cells are optimized for transmitting small, graded signals. Here we show, by recording from a cone and a synaptically connected 'Off' bipolar cell in slices of retina from the ground squirrel, that transmission is mediated by glutamate receptors of the kainate-preferring subtype. In the dark, a cone releases sufficient neurotransmitter to desensitize most postsynaptic kainate receptors. The small postsynaptic current that persists (<5% of maximum) is quickly modulated by changes in presynaptic voltage. Since recovery from desensitization is slow (the decay time constant is roughly 500 milliseconds), little recovery can occur during the brief (roughly 100-millisecond) hyperpolarization that is produced in cones by a flash of light. By limiting the postsynaptic current, receptor desensitization prevents saturation of the 'Off' bipolar cell's voltage response and allows the synapse to operate over the cone's entire physiological voltage range.