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The Journal of Neurophysiology Vol. 85 No. 2 February 2001, pp. 804-815
Copyright ©2001 by the American Physiological Society
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435
Hanes, Doug P. and
Robert H. Wurtz.
Interaction of the Frontal Eye Field and Superior Colliculus for
Saccade Generation. J. Neurophysiol. 85: 804-815, 2001. Both the frontal eye field (FEF) in the
prefrontal cortex and the superior colliculus (SC) on the roof of the
midbrain participate in the generation of rapid or saccadic eye
movements and both have projections to the premotor circuits of the
brain stem where saccades are ultimately generated. In the present
experiments, we tested the contributions of the pathway from the FEF to
the premotor circuitry in the brain stem that bypasses the SC. We assayed the contribution of the FEF to saccade generation by evoking saccades with direct electrical stimulation of the FEF. To test the
role of the SC in conveying information to the brain stem, we
inactivated the SC, thereby removing the circuit through the SC to the
brain stem, and leaving only the direct FEF-brain stem pathway. If the
contributions of the direct pathway were substantial, removal of the SC
should have minimal effect on the FEF stimulation, whereas if the FEF
stimulation were dependent on the SC, removal of the SC should alter
the effect of FEF stimulation. By acutely inactivating the SC, instead
of ablating it, we were able to test the efficiency of the direct
FEF-brain stem pathway before substantial compensatory mechanisms
could mask the effect of removing the SC. We found two striking effects
of SC inactivation. In the first, we stimulated the FEF at a site that
evoked saccades with vectors that were very close to those evoked at
the site of the SC inactivation, and with such optimal alignment, we
found that SC inactivation eliminated the saccades evoked by FEF
stimulation. The second effect was evident when the FEF evoked saccades
were disparate from those evoked in the SC, and in this case we
observed a shift in the direction of the evoked saccade that was
consistent with the SC inactivation removing a component of a vector
average. Together these observations lead to the conclusion that in the nonablated monkey the direct FEF-brain stem pathway is not
functionally sufficient to generate accurate saccades in the absence of
the indirect pathway that courses from the FEF through the SC to the brain stem circuitry. We suggest that the recovery of function following SC ablation that has been seen in previous studies must result not from the use of an already functioning parallel pathway but
from neural plasticity within the saccadic system.
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