Head–eye interactions during vertical gaze shifts made by rhesus monkeys

Abstract

Changing the direction of the line of sight (gaze) can involve coordinated movements of the eyes and head. During gaze shifts directed along the horizontal meridian, the contribution of the eyes and head depends upon the position of the eyes in the orbits; the contribution of the head to accomplishing the overall shift in gaze declines as the eyes increasingly are deviated away from the direction of the ensuing gaze shift. Also during horizontal gaze shifts, changes in the metrics and kinematics of the saccadic (eye movement) portion of coordinated movements, are correlated with the amplitude and velocity of the concurrent head movement. With increasing head contributions, saccade peak velocities decline, durations increase and velocity profiles develop two peaks. It remains unknown whether the interaction between head and eyes observed during horizontal gaze shifts also occurs during vertical gaze shifts. Yet, a full understanding of the neural control of eye-head coordination will depend upon the correlation of neural activity and features of vertical as well as horizontal movements. This report describes the metrics and kinematics of vertical gaze shifts made by head-unrestrained rhesus monkeys. Key observations include: (1) during vertical gaze shifts of a particular amplitude, relative eye and head contributions depend upon the initial vertical positions of the eyes in the orbits; (2) as head contribution increases, peak eye velocities decline, durations increase and vertical velocity profiles develop two peaks; (3) head movement metrics and kinematics are accurately predictable given knowledge only of head movement amplitude. In these ways, vertical gaze shifts were found to be qualitatively similar to horizontal gaze shifts. It seems probable that similar mechanisms mediate head-eye interactions during both horizontal and vertical movements. These observations are consistent with the hypothesis that a signal proportional to vertical head velocity reduces the gain of the vertical saccade burst generator.