The network properties of bipolar–bipolar cell coupling in the retina of teleost fishes

Abstract

AbstractRetinal bipolar cells exhibit a center-surround antagonistic receptive field to a light stimulus (Werblin & Dowling, 1969; Kaneko, 1970), and thus constitute an early stage of spatial information processing. We injected Lucifer Yellow and a small biotinylated tracer, biocytin, into bipolar cells of the teleost retina to examine electrical coupling in these cells. Lucifer-Yellow coupling was observed in one of 55 stained bipolar cells; the coupling pattern was one injected bipolar cell and three surrounding cells. Biocytin coupling was observed in 16 of 55 stained bipolar cells, six of which were ON center and ten OFF center. Although biocytin usually coupled to three to six bipolar cells, some OFF-center bipolar cells showed strong coupling to more than 20 cells. The biocytin-coupled bipolar cells were morphologically homologous. Membrane appositions resembling gap junctions were found between dendrites and between axon terminals of neighboring bipolar cells.In the strongest biocytin-coupled bipolar cells, the contacts between bipolar cells and cone photoreceptor cells were examined after reconstruction of the dendritic trees of five well-stained, serially sectioned OFF-center bipolar cells. Each of these bipolar cells was in contact with different numbers of cones: 11 to 20 for twin cones and two to four for single cones. This implies that, although these bipolar cells belong to the same category, the signal inputs differ among bipolar cells. Numerical simulation conducted on a hexagonal array network model demonstrated that the electrical coupling of bipolar cells can decrease the difference in input (≈80%) without causing significant loss of spatial resolution. Our results suggest that electrical coupling of bipolar cells has the advantage of decreasing the dispersion of input signals from cones, and permits bipolar cells of the same class to respond to light with similar properties.