The functions of the diverse retinal ganglion cell types in primates and the parallel visual pathways they initiate remain poorly understood. Here, unusual physiological and computational properties of the ON and OFF smooth monostratified ganglion cells are explored. Large-scale multi-electrode recordings from 48 macaque retinas revealed that these cells exhibit irregular receptive field structure composed of spatially segregated hotspots, quite different from the classic center-surround model of retinal receptive fields. Surprisingly, visual stimulation of different hotspots in the same cell produced spikes with subtly different spatiotemporal voltage signatures, consistent with a dendritic contribution to hotspot structure. Targeted visual stimulation and computational inference demonstrated strong nonlinear subunit properties associated with each hotspot, supporting a model in which the hotspots apply nonlinearities at a larger spatial scale than bipolar cells. These findings reveal a previously unreported nonlinear mechanism in the output of the primate retina that contributes to signaling spatial information. • Smooth monostratified ganglion cells have hotspots in their receptive fields • Each hotspot does not originate from an individual presynaptic input • Stimulation of distinct hotspots produces subtly different spike waveforms • The hotspots form nonlinear computational subunits larger than bipolar cells Rhoades et al. find the smooth monostratified retinal ganglion cells in the primate retina have unusual receptive fields consisting of multiple hotspots. This differs from classic center-surround receptive field models and suggests a role in nonlinear visual computation. [ABSTRACT FROM AUTHOR]