1. The visual receptive field properties of neurons in the nucleus of the optic tract (NOT) in the pretectum and the dorsal terminal nucleus (DTN) of the accessory optic tract were analyzed quantitatively in anesthetized, paralyzed macaque monkeys. 2. Visual latencies to reversals in direction of stimulus movement ranged from 40 to 80 ms [61 +/- 13.5 (SD) ms]. 3. All neurons increased their discharge rate during ipsiversive movement and decreased their ongoing activity during contraversive movement of single stimuli or whole-field random dot patterns. The population of neurons in the left NOT-DTN was excited most strongly by leftward movement pointing 4 degrees down; neurons in the right NOT-DTN were excited most strongly by rightward movement pointing 6 degrees down. The mean angle between the directions yielding the highest and the lowest discharge rate in the two populations of NOT-DTN neurons was 177 degrees. 4. The deviation of the preferred excitatory directions from the horizon in individual neurons varied with recording depth. Within the first 500 microns below the midbrain surface, neurons preferred near-horizontal directions, whereas neurons recorded more deeply preferred more oblique directions of stimulus movement. 5. The tuning widths of NOT-DTN neurons in the preferred excitatory direction were very broad. The mean halfwidth defined as the range of directions eliciting responses greater than 50% of the maximum was 127 +/- 25 degrees. 6. Moving a random dot pattern and a single bar of light simultaneously but in opposite directions caused NOT-DTN neurons to increase their discharge rate as soon as one of the two stimuli moved in the ipsiversive direction. The reduction in overall discharge rates when two stimuli moved in opposite directions indicates mainly inhibitory interactions. 7. All NOT-DTN neurons could be activated from both eyes. Interactions between the two eyes were modest and unspecific. Misalignment of the visual axes of the two eyes had no influence on response strength. 8. Optimal speeds of stimulus movement varied widely for different NOT-DTN neurons. The effective range of speeds to elicit direction-selective responses in the total population was very broad (0.1400 degrees/s. With oscillating horizontal stimulation, NOT-DTN neurons followed repetition rates up to 4 Hz at excursions of 40 degrees. Speeds greater than 500 degrees/s were either not effective or resulted in a suppression of ongoing activity in all directions of movement.(ABSTRACT TRUNCATED AT 400 WORDS)