Abstract: Many common activities, like reading, scanning scenes, or searching for an inconspicuous item in a cluttered environment, entail serial movements of the eyes that shift the gaze from one object to another. Previous studies have shown that the primate brain is capable of programming sequential saccadic eye movements in parallel. Given that the onset of saccades directed to a target are unpredictable in individual trials, what prevents a saccade during parallel programming from being executed in the direction of the second target before execution of another saccade in the direction of the first target remains unclear. Using a computational model, here we demonstrate that sequential saccades inhibit each other and share the brain's limited processing resources (capacity) so that the planning of a saccade in the direction of the first target always finishes first. In this framework, the latency of a saccade increases linearly with the fraction of capacity allocated to the other saccade in the sequence, and exponentially with the duration of capacity sharing. Our study establishes a link between the dual-task paradigm and the ramp-to-threshold model of response time to identify a physiologically viable mechanism that preserves the serial order of saccades without compromising the speed of performance.
Abstract: How the brain maintains perceptual continuity across eye movements that yield discontinuous snapshots of the world is still poorly understood. In this study we adapted a framework from the dual task paradigm, well suited to reveal bottlenecks in mental processing, to study how information is processed across sequential saccades. The pattern of RTs allowed us to distinguish among three forms of transsaccadic processing (no trans-saccadic processing, trans-saccadic visual processing, and trans-saccadic visual processing and saccade planning models). Using a cued double-step saccade task we show that even though saccade execution is a processing bottleneck, limiting access to incoming visual information, partial visual and motor processing that occur prior to saccade execution are used to guide the next eye movement. These results provide insights into how the oculomotor system is designed to process information across multiple fixations that occur during natural scanning.
Abstract: The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process-target-step reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys' response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation.
Abstract: In the previous studies on the neural control of saccade initiation using the countermanding paradigm, movement and visuomovement neurons in the frontal eye field were grouped as movement-related neurons. The activity of both types of neurons was modulated when a saccade was inhibited in response to a stop signal, and this modulation occurred early enough to contribute to the control of the saccade initiation. We now report a functional difference between these two classes of neurons when saccades are produced. Movement neurons exhibited a progressive accumulation of discharge rate following target presentation that triggered a saccade when it reached a threshold. When saccades were inhibited with lower probability in response to a stop signal appearing at longer delays, this accumulating activity was interrupted at levels progressively closer to the threshold. In contrast, visuomovement neurons exhibited a maintained elevated discharge rate following target presentation that was followed by a further enhancement immediately before saccade initiation. When saccades were inhibited in response to a stop signal, the late enhancement was absent and the maintained activity decayed regardless of stop signal delay. These results demonstrate that the activity of movement neurons realizes the progressive commitment to saccade initiation modeled by the activation of the GO unit in computational models of countermanding performance. The lack of correspondence of the activity of visuomovement neurons with any elements of these models indicates that visuomovement neurons perform a function other than saccade preparation such as a corollary discharge to update visual processing.
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.
Abstract: The capacity to detect and correct errors is thought to engage cognitive control. To probe the nature of such control in relation to eye movements, subjects performed a double-step task under different instructions: to FOLLOW the appearance of successive targets; or to cancel the initial saccade and REDIRECT gaze to the final target location. Saccade sequences occurred in the FOLLOW and REDIRECT conditions where they represented correct and corrective behaviour, respectively. We observed that corrective responses were faster than correct responses, and concurrent preparation of saccades was facilitated during error correction. These results are consistent with psychological theories that posit supervisory cognitive control over action during error correction.
Abstract: While the role of attention in selecting visual attributes is well acknowledged, relatively less is known about the mechanisms that facilitate the selection of actions during goal-directed behaviors. The notion of an executive attention has provided a particularly fruitful framework to understand how the brain coordinates the selection of appropriate modules in a sequence that optimizes behavior. However, to do this, theorists have recognized the need to parcel out this unitary system into subcomponents. Two modules that have been commonly invoked are performance monitoring and response inhibition. Visuomotor control of eye movements provides an elegant model system to investigate these mechanisms of selection and control specially occurring during "double-step" tasks in which goals are suddenly changed, demanding inhibition and error detection/correction. Here, we describe our work that has focused on the executive mechanisms that regulate the production of saccadic movements during double-step tasks in different cognitive contexts and target-shift double-step tasks. By examining the pattern of response in the context of quantitative models of saccadic reaction times, we provide behavioral evidence of predictive error correction that produces fast, corrective responses. The predictions from these behavioral experiments were also tested and supported by analyzing neural data from the frontal cortex of monkeys performing similar tasks. Finally, we present data that tested the possibility of an interaction between the inhibitory control and error correction and suggest a model in which predictive error correction may be engaged when the likelihood of error is high. We propose that these results when used in conjunction with electrophysiological recordings, may provide an important approach to understand how error detection/correction and inhibition, two vital cogs in the functioning of executive control, may interact to govern goal-directed behaviors.
