Voluntary Control of Multisaccade Gaze Shifts During Movement Preparation and Execution

Abstract

Although the nature of gaze control regulating single saccades is relatively well documented, how such control is implemented to regulate multisaccade gaze shifts is not known. We used highly eccentric targets to elicit multisaccade gaze shifts and tested the ability of subjects to control the saccade sequence by presenting a second target on random trials. Their response allowed us to test the nature of control at many levels: before, during, and between saccades. Although the saccade sequence could be inhibited before it began, we observed clear signs of truncation of the first saccade, which confirmed that it could be inhibited in midflight as well. Using a race model that explains the control of single saccades, we estimated that it took about 100 ms to inhibit a planned saccade but took about 150 ms to inhibit a saccade during its execution. Although the time taken to inhibit was different, the high subject-wise correlation suggests a unitary inhibitory control acting at different levels in the oculomotor system. We also frequently observed responses that consisted of hypometric initial saccades, followed by secondary saccades to the initial target. Given the estimates of the inhibitory process provided by the model that also took into account the variances of the processes as well, the secondary saccades (average latency approximately 215 ms) should have been inhibited. Failure to inhibit the secondary saccade suggests that the intersaccadic interval in a multisaccade response is a ballistic stage. Collectively, these data indicate that the oculomotor system can control a response until a very late stage in its execution. However, if the response consists of multiple movements then the preparation of the second movement becomes refractory to new visual input, either because it is part of a preprogrammed sequence or as a consequence of being a corrective response to a motor error.

A Within Trial Measure of the Stop Signal Reaction Time in a Head-Unrestrained Oculomotor Countermanding Task

“…Although we chose not to include such trials in our comparative analysis of antagonist neck muscle latency with SSRTs, because the GO process technically wins the race on such trials, the STOP process is still engaged to arrest the trial in mid-flight. While we note that other studies have reported truncated movements previously in other tasks (Boucher et al 2007b;Ramakrishnan et al 2010), we observed a much higher incidence in this study. Presumably, the use of larger amplitude gaze shifts (which last longer) provides more opportunity for mid-flight movement cancellation.…”

“…This prolonged duration provides an interval in which subjects can cancel an on-going gaze shift in mid-flight. The presence of truncated gaze shifts suggest that gaze shifts are not completely ballistic (e.g., Ramakrishnan et al 2010) and that the processing of the stop signal continues after the initiation of the gaze shift. However, because we are explicitly interested in neck muscle recruitment as a function of the control of the gaze axis, we have derived our measures of antagonist muscle recruitment exclusively from trials with head-only errors to avoid confounds associated with gaze shift initiation.…”

Understanding How the Brain Changes Its Mind: Microstimulation in the Macaque Frontal Eye Field Reveals How Saccade Plans Are Changed

“…Behavioral data were collected from 56 sessions (31 sessions from Monkey C and 25 sessions from Monkey D) while monkeys performed the redirect task (Ray et al, 2004;Ramakrishnan et al, 2010). In this task, monkeys made a quick saccade to the initial target as soon as it appeared (no-step trials; see Fig.…”

“…Monkeys were trained on the redirect task (Ray et al, 2004;Ramakrishnan et al, 2010), which is a modified version of the classic double-step task (Westheimer, 1954;Wheeless et al, 1966;Komoda et al, 1973;Lisberger et al, 1975;Becker and Jürgens, 1979;Aslin and Shea, 1987;Ray et al, 2004). The task consists of two kinds of trials: no-step trials, in which a single target is presented; and step trials, in which two targets are presented in succession.…”

“…To understand how the weaker motor program can supersede the stronger one, allowing for successful changes of mind, we used a redirect task. In this task, a second stimulus that appeared on infrequent trials required monkeys to withhold the saccade to the first stimulus and instead make a saccade to the second one (Ray et al, 2004;Ramakrishnan et al, 2010). Following up on earlier work (Gold and Shadlen, 2000), we stimulated the FEF during redirect behavior to track the time course of the changing saccade plan and examined the underlying computational mechanisms that entail a change of plan.…”