Localization of kainate receptors to the presynaptic active zone of the rod photoreceptor in primate retina

Abstract

Visual information is encoded at the photoreceptor synapse by modulation of the tonic release of glutamate from one or more electron-dense ribbons. This release is highest in the dark, when photoreceptors are depolarized, and decreases in grades when photoreceptors hyperpolarize with increasing light. Functional diversity between neurons postsynaptic at the synaptic ribbon arises in part from differential expression of both metabotropic (G-protein-gated) and ionotropic (ligand-gated) glutamate receptor. In the brain, different subunits also modulate the presynaptic active zone. In hippocampus, ionotropic kainate receptors localize to the presynaptic membrane of glutamatergic axon terminals and facilitate depolarization of the synapse (e.g. Lauri et al., 2001). Such facilitation may be helpful in the retina, where consistent depolarization of the photoreceptor axon terminal is necessary to maintain glutamate release in the dark. We investigated whether such a mechanism could be present in primate retina by using electron microscopy to examine the localization of the kainate subunits GluR6/7 at the rod axon terminal, where only a single ribbon synapse mediates glutamate release. We scored 54 rod axon terminals whose postsynaptic space contained one or more GluR6/7-labeled processes and traced these processes through serial sections to determine their identity. Of 68 labeled processes, 63% originated from narrow “fingers” of cytoplasm extending from the presynaptic axon terminal into the postsynaptic cleft. Each rod terminal typically inserts 4–6 presynaptic fingers, and we scored several instances where multiple fingers contained label. Such consistency suggests that each presynaptic finger expresses GluR6/7. The physiological properties of kainate receptors and the geometry of the rod axon terminal suggest that presynaptic GluR6/7 could provide a steady inward current to maintain consistent depolarization of the rod synapse in the long intervals between photons in the dark.