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The Journal of Neurophysiology Vol. 81 No. 4 April 1999, pp. 1760-1782
Copyright ©1999 by the American Physiological Society
1Centre for Vision Research and Departments of Psychology and Biology, York University, Toronto, Ontario M3J 1P3; and 2Montreal Neurological Institute and Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec H3A 2B4, Canada
Crawford, J. Douglas,
Melike Z. Ceylan,
Eliana M. Klier, and
Daniel Guitton.
Three-dimensional eye-head coordination during gaze saccades in
the primate. The purpose of this investigation was to describe the neural constraints on three-dimensional (3-D) orientations of the
eye in space (Es), head in space (Hs), and eye in head (Eh) during
visual fixations in the monkey and the control strategies used to
implement these constraints during head-free gaze saccades. Dual
scleral search coil signals were used to compute 3-D orientation quaternions, two-dimensional (2-D) direction vectors, and 3-D angular
velocity vectors for both the eye and head in three monkeys during the
following visual tasks: radial to/from center, repetitive horizontal,
nonrepetitive oblique, random (wide 2-D range), and random with
pin-hole goggles. Although 2-D gaze direction (of Es) was controlled
more tightly than the contributing 2-D Hs and Eh components, the
torsional standard deviation of Es was greater (mean 3.55°) than Hs
(3.10°), which in turn was greater than Eh (1.87°) during random
fixations. Thus the 3-D Es range appeared to be the byproduct of Hs and
Eh constraints, resulting in a pseudoplanar Es range that was twisted
(in orthogonal coordinates) like the zero torsion range of Fick
coordinates. The Hs fixation range was similarly Fick-like, whereas the
Eh fixation range was quasiplanar. The latter Eh range was maintained
through exquisite saccade/slow phase coordination, i.e., during each
head movement, multiple anticipatory saccades drove the eye torsionally
out of the planar range such that subsequent slow phases drove the eye
back toward the fixation range. The Fick-like Hs constraint was
maintained by the following strategies: first, during purely
vertical/horizontal movements, the head rotated about constantly
oriented axes that closely resembled physical Fick gimbals, i.e., about
head-fixed horizontal axes and space-fixed vertical axes, respectively
(although in 1 animal, the latter constraint was relaxed during
repetitive horizontal movements, allowing for trajectory optimization).
However, during large oblique movements, head orientation
made transient but dramatic departures from the zero-torsion Fick
surface, taking the shortest path between two torsionally eccentric
fixation points on the surface. Moreover, in the pin-hole goggle task,
the head-orientation range flattened significantly, suggesting a
task-dependent default strategy similar to Listing's law. These and
previous observations suggest two quasi-independent brain stem
circuits: an oculomotor 2-D to 3-D transformation that coordinates
anticipatory saccades with slow phases to uphold Listing's law, and a
flexible "Fick operator" that selects head motor error; both
nested within a dynamic gaze feedback loop.
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