Ground-feeding birds such as pigeons possess the most developed isthmo-optic nucleus in all classes of vertebrates. A previous study showed that this centrifugal or retinopetal nucleus modulates visual activity in tectal cells of pigeons; the present study aimed at revealing the morphology and possible dye-coupling of neurons in the isthmo-optic nucleus and in the ectopic cell region by intracellular injections of Lucifer yellow into neurons in slices. One hundred and twelve successfully labeled cells of the isthmo-optic nucleus were classified into bipolar (83%) and multipolar (17%) types, each of which was further divided into two subtypes, B and P and M and N, respectively. Neurons of B- and P-types are similar in that they have apical dendrites and axons usually arising from the opposite pole of piriform perikarya, but they differ in the length (20–120 vs. 10–20 μm) of their dendritic stems; M- and N-types possess polygonal perikarya giving rise to two to five primary dendrites either in the same orientation (M) or in a radiation fashion (N), and their axons originate from perikarya or occasionally from dendritic stems. Twelve single-injections resulted in the labeling of 26 cells, including 11 pairs and 1 quadruple labeling. About half of these are closely apposed ‘twin-cells’. Dye-coupling was found only between neighboring cells in the cell lamina. Thirteen cells in the ECR rostroventral to the ION were labeled and could be grouped into large or L- (46%) and small or S- (54%) types, mainly depending on the dendritic field size and the number of primary dendrites. No dye-coupling was observed between the presumptive ECR cells. The functional role of the ION and the significance of dye-coupling between neurons are discussed.