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J Neurophysiol (May 1, 2003). 10.1152/jn.00763.2002
Submitted on Submitted 5 September 2002; accepted in final form 13 January 2003
Canadian Institutes of Health Research Group for Action and Perception, York Centre for Vision Research and Departments of Psychology, Biology and Kinesiology and Health Sciences, York University, Toronto, Ontario M3J 1P3, Canada
Klier, Eliana M.,
Hongying Wang, and
J. Douglas Crawford.
Three-Dimensional Eye-Head Coordination Is Implemented Downstream
From the Superior Colliculus. J. Neurophysiol. 89: 2839-2853, 2003. How the brain transforms
two-dimensional visual signals into multi-dimensional motor commands,
and subsequently how it constrains the redundant degrees of freedom,
are fundamental problems in sensorimotor control. During fixations
between gaze shifts, the redundant torsional degree of freedom is
determined by various neural constraints. For example, the eye- and
head-in-space are constrained by Donders' law, whereas the
eye-in-head obeys Listing's law. However, where and how the brain
implements these laws is not yet known. In this study, we show that eye
and head movements, elicited by unilateral microstimulations of the
superior colliculus (SC) in head-free monkeys, obey the same Donders'
strategies observed in normal behavior (i.e., Listing's law for final
eye positions and the Fick strategy for the head). Moreover, these
evoked movements showed a pattern of three-dimensional eye-head
coordination, consistent with normal behavior, where the eye is driven
purposely out of Listing's plane during the saccade portion of the
gaze shift in opposition to a subsequent torsional vestibuloocular
reflex slow phase, such that the final net torsion at the end of each
head-free gaze shift is zero. The required amount of saccade-related
torsion was highly variable, depending on the initial position of the eye and head prior to a gaze shift and the size of the gaze shift, pointing to a neural basis of torsional control. Because these variable, context-appropriate torsional saccades were correctly elicited by fixed SC commands during head-free stimulations, this shows
that the SC only encodes the horizontal and vertical components of
gaze, leaving the complexity of torsional organization to downstream control systems. Thus we conclude that Listing's and Donders' laws of
the eyes and head, and their three-dimensional coordination mechanisms,
must be implemented after the SC.
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