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