Electron microscopy of Golgi-impregnated photoreceptors reveals connections between red and green cones in the turtle retina

Abstract

Red and green cones of two turtle species (Pseudemys scripta elegans and Chelydra serpentina) retina have been stained with Golgi procedures and examined by light microscopy of whole-mount tissue and by electron microscopy of serial thin sections. By light microscopy, red and green single cones appear indistinguishable, but double cones can be readily identified. All Golgi-stained photoreceptors in turtle retina have a spray of telodendria radiating from their synaptic pedicles. The telodendria of single cones are 10-20 micron long and end in clusters of terminals, whereas double cones have 30- to 50-micron long telodendria in addition to a very short bush of telodendria arising from one side of the pedicle. Electron microscopy of the Golgi-stained cones allows them to be distinguished into red or green spectral types by the appearance of their oil droplets. Furthermore, the spectral identity of cones contacted by the telodendria of identified Golgi-stained cones can similarly be determined. Red single cones make telodendrial contacts with other red singles, both members of the double cones, and with green single cones. Green single cones likewise connect to many surrounding red cones, both single and double types, and a few other green singles. Both members of the double cone connect to neighboring red and green singles and occasionally to double cones. The telodendria of stained cones end on spectrally homologous or heterologous cone types at basal junctions, central elements of ribbon synapses or, sometimes, as lateral elements of ribbon synapses. However, all these synaptic contacts appear to be of the same type, i.e., narrow-cleft basal junctions. Small gap junctions occur between neighboring cone pedicles, regardless of spectral type, in the visual streak area of the retina. Large gap junctions occur between unidentified cone telodendria in the neuropil of the outer plexiform layer. The telodendrial connections between red and green cones in the turtle retina have the appearance of chemical synapses and suggest an anatomical pathway responsible for the mixing of red and green signals in red or green cones of the turtle retina as reported in the accompanying physiological paper by Normann, Perlman, and Daly (27).