COMBINED EYE-HEAD GAZE SHIFTS IN THE PRIMATE .3. CONTRIBUTIONS TO THE ACCURACY OF GAZE SACCADES

1. The behavior of the combined eye-head gaze saccade mechanism was investigated in the rhesus monkey under both normal circumstances and in the presence of perturbations delivered to the head by a torque motor. Animals were trained to follow a target light that stepped at regular intervals through an angle of 68-degrees (+/- 34-degrees with respect to the midsagittal plane). Thus all primary saccades were center crossing. On randomly occurring trials the torque motor was pulsed so as to perturb the trajectory of the head, thus allowing us to assess both the functional state of the vestibuloocular reflex (VOR) and the effects of such perturbations on gaze saccade accuracy (gaze is defined as the sum of eye-in-head plus head-in-space, and a gaze saccade as a combined eye-head saccadic gaze shift). 2. Gaze shifts can be divided into two discrete sections: the portion during which the gaze angle is changing (the saccadic portion), and the portion during which the gaze is stationary but the head continues to move (the terminal head-movement portion). For the system to accurately acquire eccentric targets, at least two criteria must be met: 1) the saccadic portion must be accurate, 2) the compensatory eye movement that occurs during the terminal head-movement portion must be equal and opposite to the head movement, thereby maintaining gaze stability. Perturbations delivered during the terminal head-movement portion of the gaze shift indicated that VOR was functioning normally, and thus we concluded that the compensatory eye movements that accompany head movements were vestibular in origin. 3. As reported previously, during the saccadic portion of large-amplitude gaze saccades, the VOR ceases to function. In spite of this observation, the accuracy of the gaze saccade is not affected by perturbations delivered to the head. Gaze accuracy is maintained both by changing the duration of the saccadic portion and by altering the head trajectory. 4. Because rhesus monkeys often make very rapid head movements (1,200-degrees/s), we wished to discover the velocity range over which the monkey VOR might be expected to operate. Accordingly, in a second series of experiments, VOR function was assessed during passive whole-body rotations with the head fixed. By the use of spring-assisted manual rotations, peak velocities up to 850-degrees/s were achieved. When VOR gain was measured during such rotations, it was found to be equal to 0.9 up to the maximum velocities used. As the maximum vestibularly induced eye velocities approached the maximal velocities seen during saccades in the same animals, it seems likely that the rhesus monkey VOR is limited only by the characteristics of the plant rather than by any failure of the peripheral vestibular system to accurately transduce the head velocity. 5. The eye movements that accompanied gaze saccades that occurred during periods of high passive-head velocity were often extremely slow. Eye-in-head velocities were often close to 0, and the eye was even seen to reverse direction during the course of a single gaze saccade. As a result of this behavior, it was often impossible to distinguish between slow phases and saccades based solely on the eye-position record. Instead, gaze saccades were defined as periods when gaze was changing rapidly, whereas slow phases were characterized by gaze stability; these two different states were clearly distinguishable in the gaze records. 6. VOR gain was assessed during active head movements by making the measurements during the terminal head-movement portion of gaze saccades. When this was done, no evidence of saturation was ever seen. Although head velocities during large gaze shifts were occasionally seen > 1,200-degrees/s, such high velocities were only attained during the saccadic portion of the gaze shift when the VOR was off; during the terminal head movement, a time when the VOR is on, head velocities were only rarely seen > 500-degrees/s. VOR gain was found to be almost-equal-to 0.9 during this period. 7. The maintenance of gaze accuracy in the presence of perturbations delivered during a period when the VOR was turned off implies that some other mechanism is providing information about the perturbation. Furthermore, the observation that accurracy is maintained by changing the duration of the saccadic portion suports the concept that gaze saccades were controlled by a local feedback mechanism similar to the one proposed by Zee et al. for head-fixed eye saccades.