Effect of short-term saccadic adaptation on saccades evoked by electrical stimulation in the primate superior colliculus

The brain maintains the accuracy of visually guided movements by using visual feedback to correct for changes in the nervous system and musculature that would otherwise result in dysmetria. In monkeys, evidence suggests that an adaptive mechanism can compensate for weakness in an extraocular muscle by changing the gain of the neural signal to the weakened muscle. The visual effects of such neuromuscular changes have been simulated using a short-term saccade adaptation paradigm, in which the target spot jumps to a new location during the initial saccade. Under these circumstances, over several hundred trials, monkeys gradually change the amplitude of their saccades so that the eye lands closer to the final location of the target spot. There is considerable evidence from lesion and single-unit recording studies that the locus of such saccade adaptation is downstream of the superior colliculus in the cerebellum. Paradoxically, previous research has indicated that saccades evoked by electrical stimulation in the superior colliculus are not modified by short-term saccade adaptation, suggesting that adaptation occurs in the oculomotor system upstream of the superior colliculus or else in a pathway that bypasses the superior colliculus. We tested whether this result was due to using suprathreshold stimulation currents. Stimulating at 44 low-threshold sites in the superior colliculi of three monkeys revealed that using low current levels evoked saccades that were modified by adaptation. Adaptation for visually guided and electrically evoked saccades had similar time courses and tended to be accomplished by a reduction in saccade velocity rather than a decrease in duration. Moreover, the more similar the velocity of electrically evoked and visually guided saccades prior to the start of saccadic adaptation the greater the effect of adaptation on electrically evoked saccades. These results suggest that the superior colliculus is indeed upstream of the locus of adaptation, corroborating previous lesion and single-cell recording studies, but that the mechanism mediating saccade adaptation is sensitive to the parameters of electrical stimulation.