Properties of visually-guided saccadic behavior and bottom-up attention in marmoset, macaque, and human

Saccades are stereotypic behaviors whose investigation improves our understanding of how primate brains implement precise motor control. Furthermore, saccades offer an important window into the cognitive and attentional state of the brain. Historically, saccade studies have largely relied on macaque. However, the cortical network giving rise to the saccadic command is difficult to study in macaque because relevant cortical areas lie in deep sulci and are difficult to access. Recently, a New World monkey -the marmoset- has garnered attention as an alternative to macaque because of advantages including its smooth cortical surface. However, adoption of marmoset for oculomotor research has been limited due to a lack of in-depth descriptions of marmoset saccade kinematics and their ability to perform psychophysical tasks. Here, we directly compare free-viewing and visually-guided behavior of marmoset, macaque, and human engaged in identical tasks under similar conditions. In video free-viewing task, all species exhibited qualitatively similar saccade kinematics up to 25º in amplitude although with different parameters. Furthermore, the conventional bottom-up saliency model predicted gaze targets at similar rates for all species. We further verified their visually-guided behavior by training them with step and gap saccade tasks. In the step paradigm, marmoset did not show shorter saccade reaction time for upward saccades whereas macaque and human did. In the gap paradigm, all species showed similar gap effect and express saccades. Our results suggest that the marmoset can serve as a model for oculomotor, attentional, and cognitive research while being aware of their difference from macaque or human.

Sensitivity of express saccades to the expected value of the target

Express saccades, a distinct fast mode of visually guided saccades, are probably underpinned by a specific pathway that is at least partially different from the one underlying regular saccades. Whether and how this pathway deals with information on the subjective value of a saccade target is unknown. We studied the influence of varying reward expectancies and compared it with the impact of a temporal gap between the disappearance of the fixation dot and the appearance of the target on the visually guided saccades of two rhesus macaques (Macaca mulatta). We found that increasing reward expectancy increased the probability and decreased the reaction time of express saccades. The latter influence was stronger in the later parts of the reaction time distribution of express saccades, satisfactorily captured by a linear shift model of change in the saccadic reaction time distribution. Although different in strength, increasing reward expectancy and inserting a temporal gap resulted in similar effects on saccadic reaction times, suggesting that these two factors summon the same mechanism to facilitate saccadic reaction times.

Express saccades during a countermanding task

A serendipitous discovery that macaque monkeys produce express saccades under conditions that should discourage them reveals how cognitive control can adapt behavior to maximize reward.

Impairment but not abolishment of express saccades after unilateral or bilateral inactivation of the frontal eye fields

Express saccades are the shortest-latency saccade. The frontal eye fields (FEF) are thought to promote express saccades by presetting the superior colliculus. Here, by reversibly inactivating the FEF either unilaterally or bilaterally via cortical cooling, we support this by showing that the FEF plays a facilitative but not critical role in express saccade generation. We also found that FEF inactivation lowered express saccade peak velocity, emphasizing a contribution of the FEF to express saccade kinematics.

Differential effect of value and salience on saccadic reaction times

ABSTRACTExpress saccades, a mode of visually guided saccades, distinguished from regular saccades by extremely short reaction times, are triggered by inserting a temporal gap between the fixation dot and the saccade target. It is usually assumed that they are produced by a specific pathway in which the superior colliculus plays a key role. Whether and how this pathway deals with information on the subjective value of a saccade target is unknown. We, therefore, studied the influence of varying reward expectancies and compared it with the impact of the presence and absence of a temporal gap between the disappearance of the fixation dot and the appearance of the target on the visually guided saccades of two rhesus macaques (Macaca mulatta). We observed that the introduction of a gap shifted the entire saccadic reaction time distribution to shorter latencies while increasing the probability of express saccades. On the other hand, promoting the monkey’s reward expectancy shortened reaction times and increased peak velocities of regular saccades, and increased the probability of express saccades. Importantly, we observed that the reaction time and peak velocity of express saccades were not sensitive to the value of the saccade target, suggesting that the express pathway does not have access to information on value. We propose a new model on express saccades that treats the salience of visual objects in the scene differently from the subjective value assigned to them.

Express saccades during a countermanding task

ABSTRACTExpress saccades are unusually short latency, visually guided saccadic eye movements. They are most commonly observed when the fixation spot disappears at a consistent, short interval before a target spot appears at a repeated location. The saccade countermanding task includes no fixation-target gap, variable target presentation times, and the requirement to withhold saccades on some trials. These testing conditions should discourage production of express saccades. However, two macaque monkeys performing the saccade countermanding task produced consistent, multimodal distributions of saccadic latencies. These distributions consisted of a longer mode extending from 200 ms to as much as 600 ms after target presentation and another consistently less than 100 ms after target presentation. Simulations revealed that by varying express saccade production, monkeys could earn more reward. If express saccades were not rewarded, they were rarely produced. The distinct mechanisms producing express and longer saccade latencies were revealed further by the influence of regularities in the duration of the fixation interval preceding target presentation on saccade latency. Temporal expectancy systematically affected the latencies of regular but not of express saccades. This study highlights that cognitive control can integrate information across trials and strategically elicit intermittent very short latency saccades to acquire more reward.

Impairment but not abolishment of express saccades after unilateral- or bilateral cryogenic FEF inactivation

Express saccades (ESs) are a manifestation of a visual grasp reflex triggered when visual information arrives in the intermediate layers of the superior colliculus (SCi), which in turn orchestrates the lower level brainstem saccade generator to evoke a saccade with a very short latency (∼100ms). A prominent theory regarding express saccades generation is that they are facilitated by preparatory signals, presumably from cortical areas, which prime the SCi prior to the arrival of visual information. Here, we test this theory by reversibly inactivating a key cortical input to the SCi, the frontal eye fields (FEF), while monkeys perform an oculomotor task that promotes ES generation. Across three tasks with a different combination of potential target locations and uni- or bilateral FEF inactivation, we found a spared ability for monkeys to generate ESs, despite decreases in ES frequency during FEF inactivation. This result is consistent with the FEF having a facilitatory but not critical role in ES generation, likely because other cortical areas compensate for the loss of preparatory input to the SCi. However, we did find decreases in the accuracy and peak velocity of ESs generated during FEF inactivation, which argues for an influence of the FEF on the saccadic burst generator even during ESs. Overall, our results shed further light on the role of the FEF in the shortest-latency visually-guided eye movements.New & NoteworthyExpress saccades (ESs) are the shortest-latency visually-guided saccade. The frontal eye fields (FEF) is thought to promote ES by establishing the necessary preconditions in the superior colliculus. Here, by reversibly inactivate the FEF either unilaterally or bilaterally, we support this view by showing that the FEF plays an assistive but not critical role in ES generation. We also found that FEF inactivation lowered ES peak velocity, emphasizing a contribution of the FEF to ES kinematics.