Express Saccades Research Articles

Effects of saccade training on express saccade proportions, saccade latencies, and peak velocities: an investigation of nasal/temporal differences.

Express saccades have very short latencies and are often considered a special population of saccadic eye movements. Recent evidence suggests that express saccade generation in humans increases with training, and that this training is independent of the actual saccade vector being trained. We assessed the time course of these training-induced increases in express saccade generation and how they differ between the nasal and temporal hemifields, and second whether they transfer from the trained to the untrained eye. We also measured the effects of training on saccade latencies more generally, and upon peak velocities. The training effect transferred between the nasal and temporal hemifields and between the trained and untrained eyes. More surprisingly, we found an asymmetric effect of training on express saccade proportions: Before training, express saccade proportions were higher for saccades made into the nasal hemifield but with training this reversed. This training-induced asymmetry was also observed in overall saccade latencies, showing how training can unmask nasal/temporal asymmetries in saccade latencies. Finally, we report for the first time that saccadic peak velocities increased with training, independently of changes in amplitude.

Saccade latency bias toward temporal hemifield: Evidence for role of retinotectal tract in mediating reflexive saccades

The superior colliculus (SC) plays a critical role in mediating reflexive eye movements. Under optimal conditions, for example including a temporal ‘gap’ of 200 ms after fixation offset and prior to target onset, it is possible to isolate a population of ‘express saccades' with very short latencies between 80 and 120 ms. Ablation of the SC abolishes express saccades in monkeys. However, it remains to be established whether express saccade generation is dependent upon visual afferents transmitting direct retinal projections to SC via the retinotectal tract (RTT). In nineteen healthy human participants, we used a gap paradigm to investigate whether express saccades demonstrate shorter latencies to targets in the temporal hemifield, a marker for RTT function. A population of predominantly reflexive saccades (with latencies between 70 and 150 ms) was isolated in which latencies toward temporal hemifield targets were shown to be shorter than toward nasal hemifield targets. The advantages for reflexive saccades toward temporal hemifield targets suggest that visual efferents from the retina to the superior colliculus contribute to generating reflexively triggered saccades.

Express saccades in distinct populations: east, west, and in-between

Express saccades are low latency (80–130 ms), visually guided saccades. While their occurrence is encouraged by the use of gap tasks (the fixation target is extinguished 200 ms prior to the saccade target appearing) and suppressed by the use of overlap tasks (the fixation target remains present when the saccade target appears), there are some healthy, adult participants, “express saccade makers” (ESMs), who persist in generating high proportions (> 30%) of express saccades in overlap conditions. These participants are encountered much more frequently in Chinese participant groups than amongst the Caucasian participants tested to date. What is not known is whether this high number of ESMs is only a feature of Chinese participant groups. More broadly, there are few comparative studies of saccade behaviour across large participant groups drawn from different populations. We, therefore, tested an independent group of 70 healthy adult Egyptian participants, using the same equipment and procedures as employed in the previous studies. Each participant was exposed to two blocks of 200 gap, and two blocks of 200 overlap trials, with block order counterbalanced. Results from the Schwartz Value Survey were used to confirm that this group of participants was culturally distinct from the Chinese and Caucasian (white British) groups tested previously. Fourteen percent (10/70) of this new group were ESMs, and the pattern of latency distribution in these ESMs was identical to that identified in the other participant groups, with a prominent peak in the express latency range in overlap conditions. Overall, we identified three modes in the distribution of saccade latency in overlap conditions, the timing of which (express peak at 110 ms, subsequent peaks at 160 and 210 ms) were strikingly consistent with our previous observations. That these behavioural patterns of saccade latency are observed consistently in large participant groups, drawn from geographically, ethnically, and culturally distinct populations, suggests that they relate to the underlying architecture of the saccade system.

Commentary: Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast.

Commentary: Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast.

The effect of object-centered instructions in Cartesian and polar coordinates on saccade vector

Express saccades (ES) are the most reflexive saccadic eye movements, with very short reaction times of 70–110 ms. It is likely that ES have the shortest saccade reaction times (SRTs) possible given the known physiological and anatomical delays present in sensory and motor systems. Nevertheless, it has been demonstrated that a vector displacement of ES to spatially extended stimuli can be influenced by spatial cognition. Edelman, Kristjansson, and Nakayama (2007) found that when two horizontally separated visual stimuli appear at a random location, the spatial vector, but not the reaction time, of human ES is strongly influenced by an instruction to make a saccade to one side (either left or right) of a visual stimulus array. Presently, we attempt to extend these findings of cognitive effects on saccades in three ways: (a) determining whether ES could be affected by other types of spatial instructions: vertical, polar amplitude, and polar direction; (b) determining whether these spatial effects increased with practice; and (c) determining how these effects depended on SRTs. The results demonstrate that both types of Cartesian as well as polar amplitude instructions strongly affect ES vector, but only modestly affect SRTs. Polar direction instructions had sizable effects only on nonreflexive saccades where the visual stimuli could be viewed for several hundred milliseconds prior to saccade execution. Short- (trial order within a block) and long-term (experience across several sessions) practice had little effect, though the effect of instruction increased with SRT. Such findings suggest a generalized, innate ability of cognition to affect the most reflexive saccadic eye movements.

The influence of distractors on express saccades.

It is well known that regular target-driven saccades are affected by the presence of close and remote distractors. Distractors close to the target affect the saccade landing position (known as the global effect), while remote distractors prolong saccade latencies to the target (known as the remote-distractor effect). Little is known about whether a different population of saccades known as express saccades (saccades with very short latencies between 80 and 130 ms) is similarly affected by close and remote distractors, as these saccades are considered to be the result of advanced preparation of an oculomotor program toward the target. We designed a task in which we were able to generate a large number of express saccades, as evidenced by a separate and very early peak in the saccade-latency distribution-a distribution that was different from that of regular saccades. Our results show that irrelevant and unexpected visual input had a large effect on express saccades. We found a global and a remote-distractor effect which were similar to those seen in regular saccades. Even though our findings confirm the existence of very-short-latency saccades in humans, it is questionable whether they represent a different population of saccades, as they were equally affected by the presence of distractors as are regular saccades.

Direct gaze facilitates rapid orienting to faces: Evidence from express saccades and saccadic potentials

Direct gaze is a crucial signal in human social communication, which is known to attract visual attention and modulate a wide range of behaviours. The present study investigated whether direct gaze facilitates rapid orienting to faces, which is important for adaptive on-line communication, and its neural correlates. Fifteen participants performed a rapid orienting task, in which they were instructed to saccade to peripherally presented buildings or faces containing direct or averted gaze as quickly as possible. Electroencephalographic recordings were made during the task. Shorter express saccade latencies were found for faces with direct gaze, compared to averted gaze or buildings, while no significant difference was found between faces with averted gaze and buildings. Furthermore, saccade-locked event-related potential (ERP) amplitudes in parieto-occipital areas discriminated faces with direct gaze from buildings and faces with averted gaze corroborating behavioural results. These results show that detection of direct gaze facilitates rapid orienting to faces.

Two subdivisions of macaque LIP process visual-oculomotor information differently

Although the cerebral cortex is thought to be composed of functionally distinct areas, the actual parcellation of area and assignment of function are still highly controversial. An example is the much-studied lateral intraparietal cortex (LIP). Despite the general agreement that LIP plays an important role in visual-oculomotor transformation, it remains unclear whether the area is primary sensory- or motor-related (the attention-intention debate). Although LIP has been considered as a functionally unitary area, its dorsal (LIPd) and ventral (LIPv) parts differ in local morphology and long-distance connectivity. In particular, LIPv has much stronger connections with two oculomotor centers, the frontal eye field and the deep layers of the superior colliculus, than does LIPd. Such anatomical distinctions imply that compared with LIPd, LIPv might be more involved in oculomotor processing. We tested this hypothesis physiologically with a memory saccade task and a gap saccade task. We found that LIP neurons with persistent memory activities in memory saccade are primarily provoked either by visual stimulation (vision-related) or by both visual and saccadic events (vision-saccade-related) in gap saccade. The distribution changes from predominantly vision-related to predominantly vision-saccade-related as the recording depth increases along the dorsal-ventral dimension. Consistently, the simultaneously recorded local field potential also changes from visual evoked to saccade evoked. Finally, local injection of muscimol (GABA agonist) in LIPv, but not in LIPd, dramatically decreases the proportion of express saccades. With these results, we conclude that LIPd and LIPv are more involved in visual and visual-saccadic processing, respectively.

Bimodal latency distribution and distractor effects in Express Saccades in humans.

Bimodal latency distribution and distractor effects in Express Saccades in humans.

Saccadic Eye Movement Abnormalities in Children with Epilepsy.

Childhood onset epilepsy is associated with disrupted developmental integration of sensorimotor and cognitive functions that contribute to persistent neurobehavioural comorbidities. The role of epilepsy and its treatment on the development of functional integration of motor and cognitive domains is unclear. Oculomotor tasks can probe neurophysiological and neurocognitive mechanisms vulnerable to developmental disruptions by epilepsy-related factors. The study involved 26 patients and 48 typically developing children aged 8–18 years old who performed a prosaccade and an antisaccade task. Analyses compared medicated chronic epilepsy patients and unmedicated controlled epilepsy patients to healthy control children on saccade latency, accuracy and dynamics, errors and correction rate, and express saccades. Patients with medicated chronic epilepsy had impaired and more variable processing speed, reduced accuracy, increased peak velocity and a greater number of inhibitory errors, younger unmedicated patients also showed deficits in error monitoring. Deficits were related to reported behavioural problems in patients. Epilepsy factors were significant predictors of oculomotor functions. An earlier age at onset predicted reduced latency of prosaccades and increased express saccades, and the typical relationship between express saccades and inhibitory errors was absent in chronic patients, indicating a persistent reduction in tonic cortical inhibition and aberrant cortical connectivity. In contrast, onset in later childhood predicted altered antisaccade dynamics indicating disrupted neurotransmission in frontoparietal and oculomotor networks with greater demand on inhibitory control. The observed saccadic abnormalities are consistent with a dysmaturation of subcortical-cortical functional connectivity and aberrant neurotransmission. Eye movements could be used to monitor the impact of epilepsy on neurocognitive development and help assess the risk for poor neurobehavioural outcomes.

Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast

A key structure for directing saccadic eye movements is the superior colliculus (SC). The visual pathways that project to the SC have been reported to carry only luminance information and not color information. Short-wavelength-sensitive cones (S-cones) in the retina make little or no contribution to luminance signals, leading to the conclusion that S-cone stimuli should be invisible to SC neurons. The premise that S-cone stimuli are invisible to the SC has been used in numerous clinical and human psychophysical studies. The assumption that the SC cannot use S-cone stimuli to guide behavior has never been tested. We show here that express saccades, which depend on the SC, can be driven by S-cone input. Further, express saccade reaction times and changes in SC activity depend on the amount of S-cone contrast. These results demonstrate that the SC can use S-cone stimuli to guide behavior. We conclude that the use of S-cone stimuli is insufficient to isolate SC function in psychophysical and clinical studies of human subjects.

Linking express saccade occurance to stimulus properties and sensorimotor integration in the superior colliculus.

Express saccades represent the fastest possible eye movements to visual targets with reaction times that approach minimum sensory-motor conduction delays. Previous work in monkeys has identified two specific neural signals in the superior colliculus (SC: a midbrain sensorimotor integration structure involved in gaze control) that are required to execute express saccades: 1) previsual activity consisting of a low-frequency increase in action potentials in sensory-motor neurons immediately before the arrival of a visual response; and 2) a transient visual-sensory response consisting of a high-frequency burst of action potentials in visually responsive neurons resulting from the appearance of a visual target stimulus. To better understand how these two neural signals interact to produce express saccades, we manipulated the arrival time and magnitude of visual responses in the SC by altering target luminance and we examined the corresponding influences on SC activity and express saccade generation. We recorded from saccade neurons with visual-, motor-, and previsual-related activity in the SC of monkeys performing the gap saccade task while target luminance was systematically varied between 0.001 and 42.5 cd/m(2) against a black background (∼0.0001 cd/m(2)). Our results demonstrated that 1) express saccade latencies were linked directly to the arrival time in the SC of visual responses produced by abruptly appearing visual stimuli; 2) express saccades were generated toward both dim and bright targets whenever sufficient previsual activity was present; and 3) target luminance altered the likelihood of producing an express saccade. When an express saccade was generated, visuomotor neurons increased their activity immediately before the arrival of the visual response in the SC and saccade initiation. Furthermore, the visual and motor responses of visuomotor neurons merged into a single burst of action potentials, while the visual response of visual-only neurons was unaffected. A linear combination model was used to test which SC signals best predicted the likelihood of producing an express saccade. In addition to visual response magnitude and previsual activity of saccade neurons, the model identified presaccadic activity (activity occurring during the 30-ms epoch immediately before saccade initiation) as a third important signal for predicting express saccades. We conclude that express saccades can be predicted by visual, previsual, and presaccadic signals recorded from visuomotor neurons in the intermediate layers of the SC.

Deprivation and Recovery of Sleep in Succession Enhances Reflexive Motor Behavior.

Sleep deprivation impairs inhibitory control over reflexive behavior, and this impairment is commonly assumed to dissipate after recovery sleep. Contrary to this belief, here we show that fast reflexive behaviors, when practiced during sleep deprivation, is consolidated across recovery sleep and, thereby, becomes preserved. As a model for the study of sleep effects on prefrontal cortex-mediated inhibitory control in humans, we examined reflexive saccadic eye movements (express saccades), as well as speeded 2-choice finger motor responses. Different groups of subjects were trained on a standard prosaccade gap paradigm before periods of nocturnal sleep and sleep deprivation. Saccade performance was retested in the next morning and again 24 h later. The rate of express saccades was not affected by sleep after training, but slightly increased after sleep deprivation. Surprisingly, this increase augmented even further after recovery sleep and was still present 4 weeks later. Additional experiments revealed that the short testing after sleep deprivation was sufficient to increase express saccades across recovery sleep. An increase in speeded responses across recovery sleep was likewise found for finger motor responses. Our findings indicate that recovery sleep can consolidate motor disinhibition for behaviors practiced during prior sleep deprivation, thereby persistently enhancing response automatization.

Oculomotor inhibitory control in express saccade makers.

Express saccade makers (ESMs) produce high proportions (>30 %) of low-latency (80-130 ms) express saccades in tasks in which such responses are usually suppressed. In addition, high directional error rates on the antisaccade (AS) task suggest a failure of oculomotor inhibitory mechanisms in ESMs. However, the AS task is complex and does not provide a measure of inhibitory processes in isolation. We therefore examined inhibitory control in 25 ESM and 28 non-ESM ('Norm') participants, using a minimally delayed oculomotor response (MDOR) task. After a randomised fixation period, a pro-saccade target appeared for 200 or 1,000 ms. Participants were instructed to maintain fixation and saccade to the target position upon target offset. In a control task, they saccaded on target onset. Overall, saccade latency was considerably increased in the MDOR task compared to the control task (354 vs. 170 ms; p < 0.001), and we also observed a latency modulation with display time (200: 399, 1,000: 302 ms; p < 0.001). However, there was no evidence of a difference between groups (p = 0.29). Errors consisted primarily of responses to target onsets and error rates were comparable between the groups (p = 0.33). The overproduction of fast, reflexive responses was still observed in ESMs who generated a higher proportion of their errors within the express latency range (p < 0.001). We confirmed that in the AS task, the ESMs exhibited a higher directional error rate (p = 0.03). These results suggest that the performance 'deficit' observed on the AS task in ESMs cannot be attributed to generally weaker inhibitory control.

Saccade learning with concurrent cortical and subcortical basal ganglia loops.

The Basal Ganglia (BG) is a central structure involved in multiple cortical and subcortical loops. Some of these loops are believed to be responsible for saccade target selection. We study here how the very specific structural relationships of these saccadic loops can affect the ability of learning spatial and feature-based tasks. We propose a model of saccade generation with reinforcement learning capabilities based on our previous BG and superior colliculus models. It is structured around the interactions of two parallel cortico-basal loops and one tecto-basal loop. The two cortical loops separately deal with spatial and non-spatial information to select targets in a concurrent way. The subcortical loop is used to make the final target selection leading to the production of the saccade. These different loops may work in concert or disturb each other regarding reward maximization. Interactions between these loops and their learning capabilities are tested on different saccade tasks. The results show the ability of this model to correctly learn basic target selection based on different criteria (spatial or not). Moreover the model reproduces and explains training dependent express saccades toward targets based on a spatial criterion. Finally, the model predicts that in absence of prefrontal control, the spatial loop should dominate.

Erratum to: Visual priming through a boost of the target signal: Evidence from saccadic landing positions

Searching for a target is slower when target features change from trial to trial than when they are repeated. Although heavily studied, it is still not wholly clear what process is influenced by such visual priming. Here, we introduce a new measure to study priming. When a target and distractor are in close proximity, fast saccades generally fall in between the two, a finding known as the global effect. We elicited global effect saccades to study the effects of repeating target or distractor colors on overt attention. Saccades landed closer to a target or distractor in the color of a previous target, suggesting that priming enhances target color signals. This was true even for the fastest eye movements, in the range of express saccades. Distractor color repetition, on the other hand, had no effect, at least in isolation. Visual priming is, we conclude, at least partly the result of boosting perceptual target signals.

Control of the superior colliculus by the lateral prefrontal cortex

Several decades of patient, functional imaging and neurophysiological studies have supported a model in which the lateral prefrontal cortex (PFC) acts to suppress unwanted saccades by inhibiting activity in the oculomotor system. However, recent results from combined PFC deactivation and neural recordings of the superior colliculus in monkeys demonstrate that the primary influence of the PFC on the oculomotor system is excitatory, and stands in direct contradiction to the inhibitory model of PFC function. Although erroneous saccades towards a visual stimulus are commonly labelled reflexive in patients with PFC damage or dysfunction, the latencies of most of these saccades are outside of the range of express saccades, which are triggered directly by the visual stimulus. Deactivation and pharmacological manipulation studies in monkeys suggest that response errors following PFC damage or dysfunction are not the result of a failure in response suppression but can best be understood in the context of a failure to maintain and implement the proper task set.

Visual priming through a boost of the target signal: Evidence from saccadic landing positions

Searching for a target is slower when target features change from trial to trial than when they are repeated. Although heavily studied, it is still not wholly clear what process is influenced by such visual priming. Here, we introduce anew measure to study priming. When a target and distractor are in close proximity, fast saccades generally fall in between the two, a finding known as the global effect. We elicited global effect saccades to study the effects of repeating target or distractor colors on overt attention. Saccades landed closer to a target or distractor in the color of a previous target, suggesting that priming enhances target color signals. This was true even for the fastest eye movements, in the range of express saccades. Distractor color repetition, on the other hand, had no effect, at least in isolation. Visual priming is, we conclude, at least partly the result of boosting perceptual target signals [corrected].

Parietal Cortical Neuronal Activity Is Selective for Express Saccades

Saccadic eye movements are central to primate behavior and serve to move the eyes to visual objects of interest. Express saccades, unlike regular saccades, occur with very short reaction times, a behavior necessary for speeded reactions in goal-directed behavior. Previous studies have shown that introduction of a blank interval (gap) between the fixation point offset and the saccadic target onset leads to an increase in the number of express saccades and that the superior colliculus plays a crucial role in the generation of express saccades. A longstanding hypothesis asserted that express saccades are mediated largely by a subcortical circuit, circumventing extrastriate visual cortex. An alternative "posterior pathway" hypothesis proposed the involvement of posterior parietal cortex. In the present study, using a gap saccade task, we investigated the role of nonhuman primate's lateral intraparietal cortex (LIP) in generation of express saccades. We show that roughly half of recorded LIP neurons were modulated during the gap interval. Moreover, a group of neurons with persistent activity in a memory-guided saccade task enhanced their activity during express saccades relative to that during regular saccades. After reducing the target's certainty by increasing the potential target locations, neuronal activity remained in the similar level during express saccades but markedly reduced during regular saccades that correlated with the increase of saccadic reaction time in the regular saccade. Our results suggest that area LIP is directly involved in generating saccades in express mode.

Correction: Performance Deficits in a Voluntary Saccade Task in Chinese “Express Saccade Makers”

Correction: Performance Deficits in a Voluntary Saccade Task in Chinese “Express Saccade Makers”