COMBINED EYE-HEAD GAZE SHIFTS PRODUCED BY ELECTRICAL STIMULATION OF THE SUPERIOR COLLICULUS IN RHESUS MONKEYS. Edward G. Freedman, Terrence R. Stanford, David L. Sparks. Institute of Neurological Sciences and the Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104-6196.
APStracts 3:0064N, 1996.
SUMMARY AND CONCLUSIONS
1. We electrically stimulated the intermediate and deep layers of the superior colliculus (SC) in two rhesus macaques free to move their heads both vertically and horizontally (head unrestrained). Stimulation of the primate SC can elicit high velocity, combined, eye-head gaze shifts that are similar to visually-guided gaze shifts of comparable amplitude and direction. The amplitude of gaze shifts produced by collicular stimulation depends on the site of stimulation and on the parameters of stimulation (frequency, current, and duration of the stimulation train). 2. The maximal amplitude gaze shifts, produced by electrical stimulation at 56 sites in the superior colliculi of two rhesus monkeys, ranged in amplitude from 7 to 80. Because the head was unrestrained, stimulation-induced gaze shifts often included movements of the head. Head movements produced at the 56 stimulation sites ranged in amplitude from 0 to 70. 3. The relationships between peak velocity and amplitude, and between duration and amplitude of stimulation-induced head movements and gaze shifts were comparable to the relationships observed during visually-guided gaze shifts. The relative contributions of the eyes and head to visually- guided and stimulation-induced gaze shifts were also similar. 4. As was true for visually-guided gaze shifts, the head contribution to stimulation-induced gaze shifts depended on the position of the eyes relative to the head at the onset of stimulation. When the eyes were deviated in the direction of the ensuing gaze shift the head contribution increased and the latency to head movement onset was decreased. 5. We systematically altered the duration of stimulation trains (10 - 400 ms) while stimulation frequency and current remained constant. Increases in stimulation duration systematically increased the amplitude of the evoked gaze shift until a site specific maximal amplitude was reached. Further increases in stimulation duration did not increase gaze amplitude. There was a high correlation between the end of the stimulation train and the end of the evoked gaze shift for movements smaller than the site specific maximal amplitude. 6. Unlike the effects of stimulation duration on gaze amplitude, the amplitude and duration of evoked head movements did not saturate for the range of durations tested (10 - 400 ms), but continued to increase linearly with increases in stimulation duration. 7. The frequency of stimulation was systematically varied (range: 63 Hz - 1000 Hz) while other stimulation parameters remained constant. The velocity of evoked gaze shifts was related to the frequency of stimulation; higher stimulation frequencies resulted in higher peak velocities. The maximal, site specific amplitude was independent of stimulation frequency. 8. When stimulating a single collicular site using identical stimulation parameters, the amplitude and direction of stimulation-induced gaze shifts initiated from different initial positions, were relatively constant. In contrast, the amplitude and direction of the eye component of these fixed vector gaze shifts depended upon the initial position of the eyes in the orbits; the endpoints of the eye movements converged on an orbital region, or "goal", that depended on the site of collicular stimulation. 9. The gaze shifts produced by caudal collicular stimulation when the head was restrained were typically smaller than those evoked from the same site when the head was unrestrained when identical stimulation parameters were used and when the eyes were initially centered in the orbits. This attenuation occurred because stimulation drove the eyes to approximately the same orbital position when the head was restrained or unrestrained. Thus, movements produced when the head was restrained were reduced in amplitude by approximately the amount that the head would have contributed if free to move. 10. When the head was restrained, only the eye component of the intended gaze shift was observed. This resulted in a dissociation of the "desired" gaze amplitude specified by the locus of collicular activity and the observed movement. Because, during head restrained stimulation, the observed movement is only a portion of the movement encoded by the locus of collicular activity, the collicular "motor map" defined using microstimulation in head restrained subjects may be distorted. 11. The directions of the eye, head, and gaze components of stimulation-induced movements, evoked from different initial positions, were different. For example, during an oblique gaze shift directed 45 above the horizontal meridian, the eye component of the gaze shift could be almost purely vertical and the head component almost purely horizontal. This produced a dissociation of the eye, head and gaze movement directions. 12. Collectively, these data are inconsistent with the hypothesis that the SC generates separate eye and head displacement commands. Instead, the findings are interpreted as support for the hypothesis that a signal of desired gaze displacement is derived from the locus of collicular activity. The level of collicular activity can influence the velocity of gaze shifts without affecting the gaze displacement signal. 

Received 2 October 1995; accepted in final form 12 March 1996.
APS Manuscript Number J653-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 1 April 96