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The Journal of Neurophysiology Vol. 82 No. 6 December 1999, pp. 3236-3253
Copyright ©1999 by the American Physiological Society
1Graduate Group in Bioengineering, University of California, San Francisco 94143; 2Graduate Group in Bioengineering, University of California, Berkeley 94720; and 3The Smith-Kettlewell Eye Research Institute, San Francisco, California 94115
Gandhi, Neeraj J. and
Edward L. Keller.
Comparison of Saccades Perturbed by Stimulation of the Rostral
Superior Colliculus, the Caudal Superior Colliculus, and the Omnipause
Neuron Region. J. Neurophysiol. 82: 3236-3253, 1999. Over the past decade, considerable
research efforts have been focused on the role of the rostral superior
colliculus (SC) in control of saccades. The most recent theory
separates the deeper intermediate layers of the SC into two functional
regions: the rostral pole of these layers constitutes a fixation zone
and the caudal region comprises the saccade zone. Sustained activity of fixation neurons in the fixation zone is argued to maintain fixation and help prevent saccade generation by exciting the omnipause neurons (OPNs) in the brain stem. This hypothesis is in contrast to the
traditional view that the SC contains a topographic representation of
the saccade motor map on which the rostral pole of the SC encodes signals for generating small saccades (<2°) instead of preventing them. There is therefore an unresolved controversy about the specific role on the most rostral region of the SC, and we reexamined its functional contribution by quantifying and comparing spatial and temporal trajectories of 30° saccades perturbed by electrical stimulation of the rostral pole and more caudal regions in the SC and
of the OPN region. If the rostral pole serves to preserve fixation,
then saccades perturbed by stimulation should closely resemble
interrupted saccades produced by stimulation of the OPN region. If it also contributes to saccade generation, then the disrupted movements would better compare with redirected
saccades observed after stimulation of the caudal SC. Our
experiments revealed two significant findings: 1) the
locus of stimulation was the primary factor determining the
perturbation effect. If the directions of the target-directed saccade
and stimulation-evoked saccade were aligned and if the stimulation was
delivered within approximately the rostral 2 mm (<10° amplitude) of
SC, the ongoing saccade stopped in midflight but then resumed after
stimulation end to reach the original visually specified goal with
close to normal accuracy. When stimulation was applied at more caudal
sites, the ongoing saccade directly reached the target location without
stopping at an intermediate position. If the directions differed
considerably, both initial and resumed components were typically
observed for all stimulation sites. 2) A quantitative
analysis of the saccades perturbed from the fixation zone showed
significant deviations from their control spatial trajectories. Thus
they resembled redirected saccades induced by caudal SC stimulation and
differed significantly from interrupted saccades produced by OPN
stimulation. The amplitude of the initial saccade, latency of
perturbation, and spatial redirection were greatest for the most caudal
sites and decreased gradually for rostral sites. For stimulation sites
within the rostral pole of SC, the measures formed a smooth
continuation of the trends observed in the saccade zone. As these
results argue for the saccade zone concept, we offer reinterpretations
of the data used to support the fixation zone model. However, we also
discuss scenarios that do not allow an outright rejection of the
fixation zone hypothesis.
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