Visual responses were examined quantitatively in 96 units in the lateral (LTN) and dorsal (DTN) terminal nuclei of the cat accessory optic system (AOS). The receptive fields of LTN and DTN cells were quite large, with an average diameter of approximately 60 degrees. Individual cell receptive fields, which could be as small as 30 degrees vertically by 15 degrees horizontally or as large as 100 by 100 degrees, always included the area centralis. Large, moving textured stimuli provoked optimal modulation in these cells. In response to a 100 by 80 degrees random-dot pattern moving at a constant velocity, nearly all cells in both the LTN and DTN displayed a high degree of direction selectivity. Directional response profiles were subjected to a vector analysis that generated two quantities proportional to the direction and magnitude of the major excitatory (E vectors) and inhibitory (I vectors) responses of individual cells. Directional vectors of the LTN displayed a strikingly bimodal distribution: E vectors of individual LTN cells pointed either upward (25 of 49) or downward (23 of 49). I vectors also pointed either up or down in a direction opposite to that of the E vector for the same cell. E and I vectors in both LTN and DTN units were separated by approximately 180 degrees. With few exceptions, E vectors of DTN cells pointed in a horizontal-medial direction, while DTN I vectors pointed in a horizontal-lateral direction. A relatively broad range of stimulus velocities (0.8-102.4 degrees/s) evoked maximal excitation in individual LTN units. The majority of LTN cells, however, achieved maximal excitation at velocities between 0.8 and 12.8 degrees/s. The deepest inhibition was elicited over a range of velocities from 0.2 to 102.4 degrees/s, with two major peaks at 0.8 and 12.8 degrees/s. A similar range of velocity sensitivity was observed in DTN cells: maximal excitation was obtained for stimulus velocities from 1.6 to 102.4 degrees/s, with most DTN cells showing the greatest excitatory response between 6.4 and 12.8 degrees/s. A broad range of inhibitory velocity tuning was also observed in DTN units, with most cells exhibiting the deepest inhibitory modulation at 25.6 degrees/s. The majority of LTN and DTN units were driven most effectively through the eye contralateral to the recording site. Nonetheless, a large percentage of LTN (78%) and DTN (93%) cells could be driven to some extent through both eyes. Despite this conspicuous ipsilateral eye influence, no units were found in either the LTN or the DTN that were driven solely through the ipsilateral eye.(ABSTRACT TRUNCATED AT 400 WORDS)