Foveal cones form basal as well as invaginating junctions with diffuse ON bipolar cells

The response of a mammalian bipolar cell is generally thought to be determined by the location and morphology of synapses from the cone terminal: ON bipolar cells are believed to be depolarized strictly at invaginating contacts and OFF bipolar cells hyperpolarized at basal contacts. This hypothesis was re-investigated in the macaque fovea (1 deg nasal) using electron micrographs of serial sections. We determined the number of invaginating sites available and then identified the contacts to bipolar cells with axons in the ON level of the inner plexiform layer. A cone terminal forms about 20 active zones marked by ribbons. A few active zones house two invaginating dendrites, so there are 22 invaginating sites per cone. A midget ON bipolar cell collects 18 invaginating contacts from one cone, thus only about four invaginating sites remain for diffuse ON bipolar cells. Two diffuse ON cells were reconstructed; each collects about 25 contacts from an estimated 10 cones. Only three or four of these contacts are invaginating; the rest are basal, adjacent to the triad. This suggests that basal contacts can be depolarizing. The distance from the vesicle release site at active zones to an invaginating contact is 140 +/- 40 nm; to a basal contact adjacent to the triad is 500 +/- 160 nm, and to the next nearest basal contact is 950 +/- 370 nm.