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.