Interactions between natural and electrically evoked saccades. II. At what time is eye position sampled as a reference for the localization of a target?

Electrical microstimulation was applied at brain sites (thalamic internal medullary lamina complex and superficial layers of superior colliculus) of alert, trained monkeys to evoke fixed-vector saccades. When the stimulation was timed to occur during or after an eye movement, the evoked saccade had a modified trajectory, compensating for, at least, the last portion of the ongoing eye movement. The hypothesis proposed to explain this compensatory effect (Schlag-Rey et al. 1989) is that the electrical stimulation produces a saccade by generating a signal, equivalent to a retinal error, specifying the saccade goal at a fixed location with respect to some eye position (called reference eye position). If the eyes are moving at the time of stimulation, the reference eye position lies somewhere along the trajectory of the ongoing movement. In the present study, we tried to determine this reference eye position, and deduce from it the instant at which the goal was specified. A significant timing difference was observed between thalamic and collicular stimulations. The goal appeared to be referred to an eye position existing at stimulation onset in superior colliculus (SC), and 35-65 ms before stimulation onset in central thalamus. In the latter case, the results suggest that the evoked saccade was aimed at the spatial location that the brain computed by summing a retinal error signal (evoked by stimulation) with the eye position at the time such a signal would have been elicited by a real target. In contrast, the collicular results suggest that the evoked saccade was directed to the retinal location specified by the retinal error signal. The findings imply that if the eyes are not steady while the target position is calculated, signals conveyed in the superficial layers of SC (in contrast to the thalamus) cannot direct the eyes correctly to a visual target.