RAPID HORIZONTAL GAZE MOVEMENT IN THE MONKEY

1. We studied horizontal eye and head movements in three monkeys that were trained to direct their gaze (eye position in space) toward jumping targets while their heads were both fixed and free to rotate about a vertical axis. We considered all gaze movements that traveled greater than or equal to 80% of the distance to the new visual target. 2. The relative contributions and metrics of eye and head movements to the gaze shift varied considerably from animal to animal and even within animals. Head movements could be initiated early or late and could be large or small. The eye movements of some monkeys showed a consistent decrease in velocity as the head accelerated, whereas others did not. Although all gaze shifts were hypometric, they were more hypometric in some monkeys than in others. Nevertheless, certain features of the gaze shift were identifiable in all monkeys. To identify those we analyzed gaze, eye in head position, and head position, and their velocities at three points in time during the gaze shift: 1) when the eye had completed its initial rotation toward the target, 2) when the initial gaze shift had landed, and 3) when the head movement was finished. 3. For small gaze shifts (<20 degrees) the initial gaze movement consisted entirely of an eye movement because the head did not move. As gaze shifts became larger, the eye movement contribution saturated at similar to 300 and the head movement contributed increasingly to the initial gaze movement. For the largest gaze shifts, the eye usually began counterrolling or remained stable in the orbit before gaze landed. During the interval between eye and gaze end, the head alone carried gaze to completion. Finally, when the head movement landed, it was almost aimed at the target and the eye had returned to within 10 +/- 7 degrees, mean +/- SD, of straight ahead. Between the end of the gaze shift and the end of the head movement, gaze remained stable in space or a small correction saccade occurred. 4. Gaze movements <20 degrees landed accurately on target whether the head was fixed or free. For larger target movements, both head-free and head-fixed gaze shifts became increasingly hypometric. Head-free gaze shifts were more accurate, on average, but also more variable. This suggests that gaze is controlled in a different way with the head free. For target amplitudes <60 degrees, head position was hypometric but the error was rather constant at similar to 10 degrees. Because, in addition, the scatter of head position was less when it landed than at other times in its trajectory, these data suggest that final head position is a controlled variable. 5. Head-free gaze shifts were accompanied by crossing or centrifugal saccades. When the velocity characteristics of head-fixed centrifugal saccades were compared with those of head-free saccades, their velocity profiles were very similar, suggesting that eye movement is controlled similarly whether the head is fixed or free. For the largest gaze shifts, gaze velocity was greater than eye velocity because the head carried the eye after the saccadic system could drive it no farther. After the eye had stopped or begun to counterrotate, gaze continued to slide onward to completion, presumably because of a decrease in the efficacy of the vestibuloocular reflex. 6. Several details of the gaze and head movement trajectories were not reflected in each other. First, when head movement preceded gaze movement during larger gaze shifts, the head often did not reaccelerate when the gaze shift was initiated. Second, gaze shifts with bell-shaped velocity profiles could be accompanied by head velocity profiles of widely assorted shapes. Third, the peak velocities, onset times, and times to peak velocity for the two movements were poorly correlated. Fourth, gaze and head durations were poorly correlated. Fifth, the timing and magnitudes of peak eye and head movements were poorly correlated. Finally, correction eye saccades that occurred during the later portions of the head movement did not consistently produce a change in the head trajectory. These data suggest that gaze and head movements are not driven by a common signal that is filtered by the characteristics of the different loads presented by the eye and head. 7. Taken together, our data suggest that head and eye movements are driven independently during gaze shifts in monkeys. Because final gaze position is strongly dependent on-and final head position is roughly dependent on-final target position, both seem to be driven to attain the target. Because the relations between eye, head, and gaze movement are quite variable, a single command does not drive both the eye and the head. Therefore we propose a model in which the eye and head are controlled independently and gaze is coordinated by titration of the vestibuloocular reflex.