Midget and parasol ganglion cells (GCs) represent the major output channels from the primate eye to the brain. On-type midget and parasol GCs exhibit a higher background spike rate and thus can respond more linearly to contrast changes than their Off-type counterparts. Here, we show that a calcium-permeable AMPA receptor (CP-AMPAR) antagonist blocks background spiking and sustained light-evoked firing in On-type GCs while preserving transient light responses. These effects are selective for On-GCs and are occluded by a gap-junction blocker suggesting involvement of AII amacrine cells (AII-ACs). Direct recordings from AII-ACs, cobalt uptake experiments, and analyses of transcriptomic data confirm that CP-AMPARs are expressed by primate AII-ACs. Overall, our data demonstrate that under some background light levels, CP-AMPARs at the rod bipolar to AII-AC synapse drive sustained signaling in On-type GCs and thus contribute to the more linear contrast signaling of the primate On- versus Off-pathway. Display omitted •AII amacrine cells express calcium-permeable AMPA receptors (CP-AMPARs)•Blocking CP-AMPARs suppresses sustained, light-driven signals in On-ganglion cells•CP-AMPARs on AII-ACs may support the linear signaling specific to On-ganglion cells Percival et al. describe how a night vision circuit contributes to functional asymmetries in signaling of the On- and Off-type midget and parasol ganglion cells, the major output neurons of the primate retina.