The visual responses of single units in the lateral and dorsal terminal nuclei (LTN and DTN) of the accessory optic system (AOS) were studied in adult cats reared in total darkness. In the LTN of the normal cat equal numbers of cells prefer upward and downward vertical stimulus motion (previous results). While direction selectively continued to be a characteristic property of LTN and DTN units in dark-reared animals, the distribution of preferred and non-preferred directions of LTN cells was radically altered such that almost every LTN cell examined in the dark-reared cat preferred downward stimulus motion. In contrast, the distribution of preferred directions among DTN cells was largely unaffected by dark rearing. Both normal and dark-reared cat DTN cells responded best to stimuli moving horizontally toward the recorded hemisphere. The velocity preferences of DTN units of the dark-reared cat were, however, much slower than those of normal DTN units. LTN units responding to downward motion in dark-reared cats showed similar velocity preferences to those downward direction-selective LTN units in normal animals. Unlike the highly binocular responses of AOS cells encountered in the normal cat, the ocular dominance distribution obtained from units in the LTN and DTN of the dark-reared cat is completely monocular, favoring the contralateral eye. Thus, dark rearing renders the distribution of preferred directions most affected in the LTN, velocity preference most affected in the DTN and ocular dominance strongly affected in both nuclei. The physiological response properties of the dark-reared cat presented in this report bear a close resemblance to those we have described in the AOS of acutely decorticated animals (previous results). Data obtained from the dark-reared cat support our earlier suggestion that the visual cortex is a major source of upward direction selectively, high-velocity tuning and ipsilateral eye input for AOS cells. Some of the functional consequences of these findings are discussed in relation to frontal eye placement and optokinetic nystagmus.