Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat

The rod photoreceptor's synaptic terminal (or spherule) uses an elaborate synaptic structure to signal absorption of one or more photons to its postsynaptic targets. This structure includes one or two synaptic ribbons inside the terminal and a pouch‐like “invagination” outside the terminal, into which enter a widely variable number of incoming fibers and postsynaptic targets—central elements supplied by rod bipolar cells and lateral elements supplied by horizontal cells. Nonetheless, our three‐dimensional reconstructions of this synaptic structure in foveal retina of macaque monkey and peripheral retina of human and cat reveal several features that are highly conserved across species and with eccentricity: 1) every spherule has one invagination; 2) with rare exceptions, every spherule has two ribbon synaptic units with these features: a) on the presynaptic side, each ribbon synaptic unit has a ribbon or part of a ribbon and one trough‐shaped arciform density that demarcates its active zone; b) on the postsynaptic side, each ribbon synaptic unit has two apposed lateral elements and one or more central elements; 3) the volume of the extracellular space in the single invagination is small, ∼0.1 μm3; and 4) the largest distance from active zone to receptor regions on bipolar cells is small, less than ∼1.5 μm. With such small dimensions, release of one quantum of transmitter can pulse glutamate to a concentration comparable to the EC50 of the metabotropic glutamate receptors on the central elements associated with both synaptic units. We speculate that two ribbon synaptic units are required to sustain the high quantal release rate needed to signal a single photon. J. Comp. Neurol. 455:100–112, 2003. © 2002 Wiley‐Liss, Inc.