Short-term adaptation of electrically induced saccades in monkey superior colliculus.

Abstract

1. This study focuses on the neural mechanisms underlying short-term adaptation of saccadic eye movements in the rhesus monkey. Involuntary saccades of various amplitudes and directions (E-saccades) were elicited in complete darkness by electrical stimulation (< or = 50 microA) in the deeper layers of the superior colliculus (SC) at 30 different sites in two monkeys. E-saccades at a given site could be adapted by presenting a visual target at a small distance from the expected end point immediately after their occurrence. The monkeys were trained to null the ensuing error signal by making the appropriate correction saccade to the visual target in many successive trials (E-adap paradigm). By properly adjusting the location of the visual target relative to the end point of the E-saccade, the latter could be modified in amplitude as well as in direction. 2. E-saccade modifications were highly significant, always in the intended direction, and occurred only if a postsaccadic visual error signal was created. These changes were plastic and required a subsequent E-adap series with an opposite error signal to cancel them. Their time course, both during the adaptation and the readaptation period, indicated that the modification was a slow and gradual process, as has been observed earlier in classical visual adaptation experiments. 3. Postadaptation tests, assessing whether the adaptation of E-saccades was also noticeable in normal visually guided saccades (V-saccades), showed incomplete adaptation transfer that was significant in most cases. A similar result, significant in all cases, was obtained with an extended version of the E-adap paradigm in which movement planning on the basis of target selection was possible. In this case, a presaccadic visual target was presented at the expected end point of the E-saccade, which was evoked just before the monkey would make a voluntary saccade itself (VE-adap). 4. In another series of experiments, V-saccades, which were matched to the optimal saccade vector of the particular collicular site under investigation, were adapted with the classical intrasaccadic target shift paradigm (V-adap). In agreement with earlier findings, this V-adaptation showed no transfer to the E-saccades. This result was obtained even in trials in which movement planning on the basis of target selection was possible (VE-test). 5. Our experiments have shown that saccades of collicular origin can be adapted and that presaccadic target selection is not crucial for this process. Both results are nicely in line with an existing model featuring a downstream adaptive corrector with access to SC inputs. This scheme, however, does not explain why the degree of saccadic adaptation, achieved by applying any of the three adaptation paradigms (E-adap, EV-adap, or V-adap), was never equally expressed in V- and E-saccades. Arguments for extending the model by adding a cortical input from the frontal eye fields to the adaptive corrector are discussed.