Frontal Eye Field Contributions to Rapid Corrective Saccades

Abstract

. Visually guided movements can be inaccurate, especially if unexpected events occur while the movement is programmed. Often errors of gaze are corrected before external feedback can be processed. Evidence is presented from macaque monkey frontal eye field (FEF), a cortical area that selects visual targets, allocates attention, and programs saccadic eye movements, for a neural mechanism that can correct saccade errors before visual afferent or performance monitoring signals can register the error. Macaques performed visual search for a color singleton that unpredictably changed position in a circular array as in classic double-step experiments. Consequently, some saccades were directed in error to the original target location. These were followed frequently by unrewarded, corrective saccades to the final target location. We previously showed that visually responsive neurons represent the new target location even if gaze shifted errantly to the original target location. Now we show that the latency of corrective saccades is predicted by the timing of movement-related activity in the FEF. Preceding rapid corrective saccades, the movement-related activity of all neurons began before explicit error signals arise in the medial frontal cortex. The movement-related activity of many neurons began before visual feedback of the error was registered and that of a few neurons began before the error saccade was completed. Thus movement-related activity leading to rapid corrective saccades can be guided by an internal representation of the environment updated with a forward model of the error.

Optimal and Suboptimal Use of Postsaccadic Vision in Sequences of Saccades

“…These cells would be ideally suited to compute the postsaccadic correction, as they would directly encode the visual prediction error. In accordance with this view, Murthy et al (2007) found with a double-step task a link between FEF activity and the latency of "corrective saccades"-actually large (Ͼ10°) saccades that resemble our S2 saccades. Overall, it is likely that FEF plays a major role in the postsaccadic updating.…”

Proactive control of sequential saccades in the human supplementary eye field

“…The slope of the ISI vs. RPT is often used as an explicit measure of concurrent planning of sequential saccades (14)(15)(16)(17)(18). Such a measure of RPT, however, is absent in the context of a delayed saccade task in which the second saccade may be concurrently planned along with the first saccade at any point during the hold-time (i.e., the time between the presentation of the initial target and the disappearance of fixation spot).…”

“…Proactive control is defined as the modification of a plan or a decision based on previous experience and in anticipation of forthcoming task demands (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11). It is distinct from reactive control, where an externally presented signal explicitly indicates the required change in plan (16)(17)(18). Evidence for the existence of proactive control largely derives from studies using the countermanding task, where performance has been found to be modulated on a trial-to-trial basis depending on the likely occurrence of a stop signal, independent of its actual presence (9).…”

“…Intersaccadic interval (ISI), defined as the time between the end of the first saccade and the beginning of the second saccade, has been shown to decrease with increasing concurrent preparation of two saccades (14)(15)(16)(17)(18). Thus, we hypothesized that if concurrent planning of sequential saccades is indeed affected by previous trial type, the ISI of a given no-shift trial should be shorter when preceded by a no-shift trial compared with when preceded by a target-shift trial.…”

“…Performance in a given trial was examined as a function of previous trial type using a parameter that has previously been shown to vary systematically with the reprocessing time (RPT), which is the time available for concurrent preparation of two saccades (14)(15)(16)(17)(18). Intersaccadic interval (ISI), defined as the time between the end of the first saccade and the beginning of the second saccade, has been shown to decrease with increasing concurrent preparation of two saccades (14)(15)(16)(17)(18).…”