The activity of 53 antidromically identified abducens motoneurons was analyzed in alert cats during spontaneous and vestibular induced eye movements. Conduction velocities ranged from 13 to 70 m/s and all motoneurons increased their discharge rates with successive eye positions in the abducting direction. Motoneurons were recruited from -19 degrees to +7 degrees. Within the oculomotor range frequency saturation was never observed for any cell. The slope of rate-position (k) relationships ranged from 2 to 17.7 spikes/s/deg (n = 40, mean 8.7 +/- 2.5). Regression analysis showed that the rate-position plots could be fit by straight lines but in most cases exponential curves produced slightly better statistical fits. Steeper slopes suggest that successively larger increases in k are required for the lateral rectus muscle to maintain more eccentric fixations in the on direction. Interspike intervals for a constant eye position exhibited low variability (less than 3.5%) for fixations shorter than 1 s. Over longer periods, variability increased in proportion to the duration of the fixation in exponential-like fashion up to 14%. Abducens motoneurons showed considerable variability in frequency during repeated fixations of the same eye position. Discharge rates were found to depend upon both the direction of the previous eye movement and, more importantly, the animal's level of alertness. The rate-position regression lines for fixation periods after saccades in the on direction significantly differed in slopes (100%) and thresholds (20%) from those in the off direction. The observed static hysteresis in abducens motoneuron behavior was in opposite direction to that previously described for the mechanical properties of the lateral rectus. This suggests both neural and mechanical factors are significantly involved in determining final eye position. The animal's level of alertness was evaluated in this study by counting the number of saccadic movements/s occurring in "alert" (1 +/- 0.2 saccades/s), and "drowsy" (0.5 +/- 0.2 saccades/s) circumstances. Comparison of the rate-position regression lines between the two conditions showed a significant decrease in slopes (100%) and elevation of thresholds (70%). Discharge rate of abducens motoneurons increased abruptly 8.9 +/- 2.8 ms prior to saccades in the horizontal on direction, and decreased 14.8 +/- 4.05 m before saccades in the off direction. During purely vertical saccades the firing frequency of abducens motoneurons did not change. Burst frequency did not saturate during saccades, but increased with saccadic velocity in a linear fashion.(ABSTRACT TRUNCATED AT 400 WORDS)