The excitatory amino acid receptor (EAAR) types involved in the generation of light-evoked excitatory postsynaptic currents (EPSCs) were examined in X-type retinal ganglion cells. Using isolated and sliced preparations of cat and ferret retina, the light-evoked EPSCs of X cells were isolated by adding picrotoxin and strychnine to the bath to remove synaptic inhibition. N-methyl-D-aspartate (NMDA) receptors contribute significantly to the light-evoked EPSCs of ON- and OFF-X cells at many different holding potentials. An NMDA receptor contribution to the EPSCs was observable when retinal synaptic inhibition was either normally present or pharmacologically blocked. NMDA receptors formed 80% of the peak light-evoked EPSC at a holding potential of -40 mV; however, even at -80 mV, 20% of the light-evoked EPSC was NMDA-mediated. An alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptor-mediated component to the light-evoked EPSCs predominated at a holding potential of -80 mV. The light-evoked EPSC was blocked by the AMPA receptor-selective antagonist GYKI52466 (50-100 microM). The AMPA receptor-mediated EPSC component had a linear current-voltage relation. AMPA receptors form the main non-NMDA EAAR current on both ON- and OFF- X ganglion cell dendrites. When synaptic transmission was blocked by the addition of Cd(2+) to the Ringer, application of kainate directly to ganglion cells evoked excitatory currents that were strongly blocked by GYKI52466. Experiments using selective EAAR modulators showed the AMPA receptor-selective modulator cyclothiazide potentiated glutamate-evoked currents on X cells, while the kainate receptor-selective modulator concanavalin A (ConA) had no effect on kainate-evoked currents. Whereas the present study confirms the general notion that AMPA EAAR-mediated currents are transient and NMDA receptor-mediated currents are sustained, current-voltage relations of the light-evoked EPSC at different time points showed the contributions of these two receptor types significantly overlap. Both NMDA and AMPA EAARs can transmit transient and sustained visual signals in X ganglion cells, suggesting that much signal shaping occurs presynaptically in bipolar cells.