Neurons in turtle accessory optic system [basal optic nucleus (BON)] were recorded to study convergence of retinal afferents, using whole-cell patch electrodes in a reduced in vitro brainstem preparation with the eyes attached. BON cells primarily exhibit EPSPs from a contralateral retinal ganglion cell input and generate an output of action potentials. Visual responses were evoked by different directions of either full-field or local moving patterns. Direction tuning of action potentials was compared with that of EPSPs detected by passing the membrane voltage through an AC amplifier and window discriminator. This rough measure of retinal input indicated that the direction tuning of the full-field excitatory input from the retina matched that of the spike output for the same BON cell. Using local patterns within the receptive fields of the BON cells, it was estimated that one to four adjacent retinal inputs were being stimulated. The direction tuning of these inputs had preferred directions that were similar to that of the full-field spike output of the cell, irrespective of where the small window was placed within the receptive field. Because more than one retinal input may have been stimulated by the small stimulus window, subsets of those EPSPs that may represent responses of a single retinal afferent were identified based on their amplitude and rise time. Again, the preferred direction of those putative single retinal afferents matched the direction tuning of the spike output of the BON cell. These findings are discussed in terms of the formation of the retinal slip signal by the BON.