Preparatory Gain Modulation of Visuomotor Transmission for Smooth Pursuit Eye Movements in Monkeys

Abstract

It has been reported that the visuomotor processing underlying the initiation of smooth pursuit eye movement is modulated in relation to the recent experience of eye movements: the initial pursuit eye velocity is larger after experiencing repeated pursuits than saccades. To assess which parameters of the previously executed pursuits play an essential role in modulating the gain of visuomotor transmission, we recorded the ocular responses of monkeys to a brief perturbing motion of the tracking target injected before the start of the eye movements. First, we compared the perturbation responses among the blocks in which the duration of executing pursuit was varied. We found that the response amplitude increased with the increase of the pursuit duration and it reached a plateau level at 100–200 ms of the duration. Second, a comparison of the perturbation responses in the blocks in which target velocity was different showed a gradual increase of the response as a function of the required pursuit velocity. Third, when the animals repeatedly performed pursuits, the response amplitude gradually increased with increasing interval between the appearance of the target and the onset of perturbation. On the other hand, such an increase was not observed when the animals repeatedly performed saccades. These results suggest that before initiating eye movements, the pursuit system modulates the gain of visuomotor transmission so as to be closely related to the properties of the repeatedly experienced eye movements and this gain modulation is triggered by the target’s appearance.

Trial-by-Trial Updating of the Gain in Preparation for Smooth Pursuit Eye Movement Based on Past Experience in Humans

“…Therefore neural activity in the sites that store event history data might be maintained even during the ITI. On the other hand, we have reported that the preparatory gain increase in monkeys is triggered by the appearance of the tracking target (Tabata et al 2006). After the appearance of the target, the amplitude of the perturbation response gradually increases and reaches its peak 300 -600 ms after the target appearance (in the current study, the time between target appearance and onset of the perturbation was always 300 ms).…”

“…Thus the initial response to the target motion is principally governed by the visual properties such as eccentricity, velocity, and acceleration (e.g., Carl and Gellman 1987;Krauzlis and Lisberger 1994;Lisberger and Westbrook 1985;Lisberger et al 1981;Morris and Lisberger 1987;Tychsen and Lisberger 1986). Since the amplitude of the perturbation response is correlated with the magnitude of the initial pursuit response (Tabata et al , 2006, our results suggest that the initial pursuit response is not only generated by a transformation of the visual signal into motor command, but also influenced by an internal cognitive process that dynamically modulates the gain based on recent experiences.…”

“…Recent evidences suggest that the gain of visuomotor transmission increases in preparation for pursuit in advance of actual target movement. Ocular responses to target perturbation during fixation become larger in monkeys or humans with repeated smooth pursuit compared with repeated performance of either fixation or saccade (Kodaka and Kawano 2003;Tabata et al 2004), and the amplitude of the perturbation response in monkeys is correlated with the magnitude of the initial pursuit response (Tabata et al , 2006.…”

The neuronal basis of on-line visual control in smooth pursuit eye movements

“…A sudden change in target motion induces a corresponding perturbation response of eye motion (Churchland & Lisberger, 2002; Ono, 2013; Schwartz & Lisberger, 1994; Tabata et al, 2006). This approach evaluates how the visual input associated with a given speed and direction of image motion on the retina affects the on-line visual control in smooth pursuit eye movements.…”

“…The visuomotor gain associated with the initial pursuit is variable, which depends on ongoing behavioral states or cognitive factors (Barnes, 2008; Keating & Pierre, 1996; Krauzlis & Miles, 1996; Tabata, Miura, & Kawano, 2005; Tabata et al, 2006). For example, the initial pursuit response evoked by visual target motion is enhanced when the subjects anticipated the tracking of a moving target.…”