Patterns of excitation in populations of retinal bipolar, amacrine, and ganglion cells were mapped by activating alpha-amino-3-hydroxyl-5-methylisoxazole-4-propionic acid (AMPA) and kainate (KA) receptors with KA in the presence of the channel-permeant guanidinium analogue 1-amino-4-guanidobutane (AGB). Registered serial thin sections were probed with immunoglobulins targeting AGB, glutamate, glycine, and gamma-aminobutyric acid (GABA) to visualize KA-evoked responses and the neurochemical signatures of distinct cell types. OFF-center cone bipolar cells and both type A and type B horizontal cells were strongly activated by KA. ON-center cone bipolar cells displayed weak AGB signals that arose at least partially, if not entirely, from coupling with KA-responsive glycinergic amacrine cells, whereas rod bipolar cells exhibited no detectable AGB permeation after KA activation. GABA-positive amacrine cells displayed a range of KA responses, some possessing little AGB signal even after strong KA activation, whereas all identifiable glycine-positive amacrine cells were driven by KA. Quantitative agonist responsivities of cells in the ganglion cell layer revealed that starburst amacrine cells are the most KA-responsive cell type in that layer. Ganglion cells varied in KA responsivity across morphologic subtypes, with a large alpha-like ganglion cell group the being the most KA responsive. Some ganglion cells displayed weak KA responses, even with saturating doses, that may have been be due to an absence of AMPA/KA receptors or to the existence of AGB-impermeant AMPA/KA receptor complexes.