Kainate receptors mediate synaptic transmission between cones and "off" bipolar cells in a mammalian retina

Light produces a graded hyperpolarization in retinal photoreceptors(1,2) th at decreases their release of synaptic neurotransmitter(3,4). Cone photorec eptors use glutamate(5,6) as a neurotransmitter with which to communicate w ith two types of bipolar cell. Activation of metabotropic glutamate recepto rs in 'On' bipolar cells(7,8) 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 cel ls(9,10) 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 c one releases sufficient neurotransmitter to desensitize most postsynaptic k ainate receptors. The small postsynaptic current that persists (<5% of maxi mum) is quickly modulated by changes in presynaptic voltage. Since recovery from desensitization is slow (the decay time constant is roughly 500 milli seconds), little recovery can occur during the brief (roughly 100-milliseco nd) hyperpolarization that is produced in cones by a flash of light. By lim iting the postsynaptic current, receptor desensitization prevents saturatio n of the 'Off' bipolar cell's voltage response and allows the synapse to op erate over the cone's entire physiological voltage range.