Visual feature tuning properties of stimulus-driven saccadic inhibition in macaque monkeys.

Saccadic inhibition refers to a short-latency transient cessation of saccade generation after visual sensory transients. This oculomotor phenomenon occurs with a latency that is consistent with a rapid influence of sensory responses, such as stimulus-induced visual bursts, on oculomotor control circuitry. However, the neural mechanisms underlying saccadic inhibition are not well understood. Here, we exploited the fact that macaque monkeys experience robust saccadic inhibition to test the hypothesis that inhibition time and strength exhibit systematic visual feature tuning properties to a multitude of visual feature dimensions commonly used in vision science. We measured saccades in three monkeys actively controlling their gaze on a target, and we presented visual onset events at random times. Across seven experiments, the visual onsets tested size, spatial frequency, contrast, orientation, motion direction, and motion speed dependencies of saccadic inhibition. We also investigated how inhibition might depend on the behavioral relevance of the appearing stimuli. We found that saccadic inhibition starts earlier, and is stronger, for large stimuli of low spatial frequencies and high contrasts. Moreover, saccadic inhibition timing depends on motion direction and orientation, with earlier inhibition systematically occurring for horizontally drifting vertical gratings. On the other hand, saccadic inhibition is stronger for faster motions and when the appearing stimuli are subsequently foveated. Besides documenting a range of feature tuning dimensions of saccadic inhibition to the properties of exogenous visual stimuli, our results establish macaque monkeys as an ideal model system for unraveling the neural mechanisms underlying a ubiquitous oculomotor phenomenon in visual neuroscience.NEW & NOTEWORTHY Visual onsets dramatically reduce saccade generation likelihood with very short latencies. Such latencies suggest that stimulus-induced visual responses, normally jump-starting perceptual and scene analysis processes, can also directly impact the decision of whether to generate saccades or not, causing saccadic inhibition. Consistent with this, we found that changing the appearance of the visual onsets systematically alters the properties of saccadic inhibition. These results constrain neurally inspired models of coordination between saccade generation and exogenous sensory stimulation.

Pictorial depth cues always influence reaching distance.

We report five experiments to test the influence of pictorial depth on reaching. Our core method is to project a wide-field background of linear perspective and/or texture gradient onto a tabletop, and to measure the amplitude of reaches made to targets within it. In 63 healthy participants performing immediate open-loop reaches across Experiments 1-4, we observed a clear effect of pictorial depth. This effect was driven specifically by the convergence of the background pattern at the target position: for each additional degree of pictorial convergence, reaching distance increased by half a millimetre. In the individual experiments, we applied manipulations that might be expected to modify the influence of pictorial depth. We found no evidence that the effect was modified with monocular viewing, or when participants responded with the left hand, or if a memory delay was inserted before the response. Nor did participants become less susceptible to pictorial depth when visual feedback of terminal reaching errors was provided, although visual feedback during the reach did mitigate the influence of pictorial depth. Finally, the visual form agnosic patient DF showed an entirely normal effect of pictorial depth cues, which leads us to question the idea that this effect emanates from visual analyses of size and shape in the ventral stream, rather than from the dorsal stream, or from earlier stages of visual processing.

Peri-Saccadic Orientation Identification Performance and Visual Neural Sensitivity Are Higher in the Upper Visual Field.

Visual neural processing is distributed among a multitude of sensory and sensory-motor brain areas exhibiting varying degrees of functional specializations and spatial representational anisotropies. Such diversity raises the question of how perceptual performance is determined, at any one moment in time, during natural active visual behavior. Here, exploiting a known dichotomy between the primary visual cortex (V1) and superior colliculus (SC) in representing either the upper or lower visual fields, we asked whether peri-saccadic orientation identification performance is dominated by one or the other spatial anisotropy. Humans (48 participants, 29 females) reported the orientation of peri-saccadic upper visual field stimuli significantly better than lower visual field stimuli, unlike their performance during steady-state gaze fixation, and contrary to expected perceptual superiority in the lower visual field in the absence of saccades. Consistent with this, peri-saccadic superior colliculus visual neural responses in two male rhesus macaque monkeys were also significantly stronger in the upper visual field than in the lower visual field. Thus, peri-saccadic orientation identification performance is more in line with oculomotor, rather than visual, map spatial anisotropies.SIGNIFICANCE STATEMENT Different brain areas respond to visual stimulation, but they differ in the degrees of functional specializations and spatial anisotropies that they exhibit. For example, the superior colliculus (SC) both responds to visual stimulation, like the primary visual cortex (V1), and controls oculomotor behavior. Compared with the primary visual cortex, the superior colliculus exhibits an opposite pattern of upper/lower visual field anisotropy, being more sensitive to the upper visual field. Here, we show that human peri-saccadic orientation identification performance is better in the upper compared with the lower visual field. Consistent with this, monkey superior colliculus visual neural responses to peri-saccadic stimuli follow a similar pattern. Our results indicate that peri-saccadic perceptual performance reflects oculomotor, rather than visual, map spatial anisotropies.

The inevitability of visual interruption.

For successful adaptive behavior, exogenous environmental events must be sensed and reacted to as efficiently as possible. In the lab, the mechanisms underlying such efficiency are often studied with eye movements. Using controlled trials, careful measures of eye movement reaction times, directions, and kinematics suggest a form of "exogenous" oculomotor capture by external events. However, even in controlled trials, exogenous onsets necessarily come asynchronously to internal brain state. We argue that variability in the effectiveness of "exogenous" capture is inevitable. We review an extensive set of evidence demonstrating that before orienting must come interruption, a process that partially explains such variability. More importantly, we present a novel neural mechanistic account of interruption, leveraging the presence of early sensory processing capabilities in the very final stages of oculomotor control brain circuitry.

The extrafoveal preview paradigm as a measure of predictive, active sampling in visual perception.

A key feature of visual processing in humans is the use of saccadic eye movements to look around the environment. Saccades are typically used to bring relevant information, which is glimpsed with extrafoveal vision, into the high-resolution fovea for further processing. With the exception of some unusual circumstances, such as the first fixation when walking into a room, our saccades are mainly guided based on this extrafoveal preview. In contrast, the majority of experimental studies in vision science have investigated "passive" behavioral and neural responses to suddenly appearing and often temporally or spatially unpredictable stimuli. As reviewed here, a growing number of studies have investigated visual processing of objects under more natural viewing conditions in which observers move their eyes to a stationary stimulus, visible previously in extrafoveal vision, during each trial. These studies demonstrate that the extrafoveal preview has a profound influence on visual processing of objects, both for behavior and neural activity. Starting from the preview effect in reading research we follow subsequent developments in vision research more generally and finally argue that taking such evidence seriously leads to a reconceptualization of the nature of human visual perception that incorporates the strong influence of prediction and action on sensory processing. We review theoretical perspectives on visual perception under naturalistic viewing conditions, including theories of active vision, active sensing, and sampling. Although the extrafoveal preview paradigm has already provided useful information about the timing of, and potential mechanisms for, the close interaction of the oculomotor and visual systems while reading and in natural scenes, the findings thus far also raise many new questions for future research.

Time-dependent inhibition of covert shifts of attention.

Visual transients can interrupt overt orienting by abolishing the execution of a planned eye movement due about 90 ms later, a phenomenon known as saccadic inhibition (SI). It is not known if the same inhibitory process might influence covert orienting in the absence of saccades, and consequently alter visual perception. In Experiment 1 (n = 14), we measured orientation discrimination during a covert orienting task in which an uninformative exogenous visual cue preceded the onset of an oriented probe by 140-290 ms. In half of the trials, the onset of the probe was accompanied by a brief irrelevant flash, a visual transient that would normally induce SI. We report a time-dependent inhibition of covert orienting in which the irrelevant flash impaired orientation discrimination accuracy when the probe followed the cue by 190 and 240 ms. The interference was more pronounced when the cue was incongruent with the probe location, suggesting an impact on the reorienting component of the attentional shift. In Experiment 2 (n = 12), we tested whether the inhibitory effect of the flash could occur within an earlier time range, or only within the later, reorienting range. We presented probes at congruent cue locations in a time window between 50 and 200 ms. Similar to Experiment 1, discrimination performance was altered at 200 ms after the cue. We suggest that covert attention may be susceptible to similar inhibitory mechanisms that generate SI, especially in later stages of attentional shifting (> 200 ms after a cue), typically associated with reorienting.

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements.

At any moment in time, new information is sampled from the environment and interacts with ongoing brain state. Often, such interaction takes place within individual circuits that are capable of both mediating the internally ongoing plan as well as representing exogenous sensory events. Here, we investigated how sensory-driven neural activity can be integrated, very often in the same neuron types, into ongoing saccade motor commands. Despite the ballistic nature of saccades, visually induced action potentials in the rhesus macaque superior colliculus (SC), a structure known to drive eye movements, not only occurred intra-saccadically, but they were also associated with highly predictable modifications of ongoing eye movements. Such predictable modifications reflected a simultaneity of movement-related discharge at one SC site and visually induced activity at another. Our results suggest instantaneous readout of the SC during movement generation, irrespective of activity source, and they explain a significant component of kinematic variability of motor outputs.

Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements.

Visual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called microsaccades, is still involved. Microsaccades are small saccades that occur when maintaining precise gaze fixation on a stationary point, and they exhibit robust modulations in peripheral cueing paradigms used to investigate covert visual selection mechanisms. These modulations consist of changes in both microsaccade directions and frequencies after cue onsets. Over the past two decades, the properties and functional implications of these modulations have been heavily studied, revealing a potentially important role for microsaccades in mediating covert visual selection effects. However, the neural mechanisms underlying cueing effects on microsaccades are only beginning to be investigated. Here we review the available causal manipulation evidence for these effects' cortical and subcortical substrates. In the superior colliculus (SC), activity representing peripheral visual cues strongly influences microsaccade direction, but not frequency, modulations. In the cortical frontal eye fields (FEF), activity only compensates for early reflexive effects of cues on microsaccades. Using evidence from behavior, theoretical modeling, and preliminary lesion data from the primary visual cortex and microstimulation data from the lower brainstem, we argue that the early reflexive microsaccade effects arise subcortically, downstream of the SC. Overall, studying cueing effects on microsaccades in primates represents an important opportunity to link perception, cognition, and action through unaddressed cortical-subcortical neural interactions. These interactions are also likely relevant in other sensory and motor modalities during other active behaviors.

Dependence of the stimulus-driven microsaccade rate signature in rhesus macaque monkeys on visual stimulus size and polarity.

Microsaccades have a steady rate of occurrence during maintained gaze fixation, which gets transiently modulated by abrupt sensory stimuli. Such modulation, characterized by a rapid reduction in microsaccade frequency followed by a stronger rebound phase of high microsaccade rate, is often described as the microsaccadic rate signature, owing to its stereotyped nature. Here, we investigated the impacts of stimulus polarity (luminance increments or luminance decrements relative to background luminance) and size on the microsaccadic rate signature. We presented brief, behaviorally irrelevant visual flashes consisting of large or small, white or black stimuli over an otherwise gray image background. Both large and small stimuli caused robust early microsaccadic inhibition, but postinhibition microsaccade rate rebound was significantly delayed and weakened for large stimuli when compared with small ones. Critically, small black stimuli were associated with stronger modulations in the microsaccade rate signature than small white stimuli, particularly in the postinhibition rebound phase, and black stimuli also amplified the incidence of early stimulus-directed microsaccades. Our results demonstrate that the microsaccadic rate signature is sensitive to stimulus size and polarity, and they point to dissociable neural mechanisms underlying early microsaccadic inhibition after stimulus onset and later microsaccadic rate rebound at longer times thereafter. These results also demonstrate early access of oculomotor control circuitry to diverse sensory representations, particularly for momentarily inhibiting saccade generation with short latencies.NEW & NOTEWORTHY Microsaccade rate is transiently reduced after sudden stimulus onsets, and then strongly rebounds before returning to baseline. We explored the influence of stimulus polarity (black vs. white) and size on this "rate signature." Large stimuli caused more muted microsaccadic rebound than small ones, and microsaccadic rebound was also differentially affected by black versus white stimuli, particularly with small stimuli. These results suggest dissociated neural mechanisms for microsaccadic inhibition and rebound in the microsaccadic rate signature.

Task-Irrelevant Visual Forms Facilitate Covert and Overt Spatial Selection.

Covert and overt spatial selection behaviors are guided by both visual saliency maps derived from early visual features as well as priority maps reflecting high-level cognitive factors. However, whether mid-level perceptual processes associated with visual form recognition contribute to covert and overt spatial selection behaviors remains unclear. We hypothesized that if peripheral visual forms contribute to spatial selection behaviors, then they should do so even when the visual forms are task-irrelevant. We tested this hypothesis in male and female human subjects as well as in male macaque monkeys performing a visual detection task. In this task, subjects reported the detection of a suprathreshold target spot presented on top of one of two peripheral images, and they did so with either a speeded manual button press (humans) or a speeded saccadic eye movement response (humans and monkeys). Crucially, the two images, one with a visual form and the other with a partially phase-scrambled visual form, were completely irrelevant to the task. In both manual (covert) and oculomotor (overt) response modalities, and in both humans and monkeys, response times were faster when the target was congruent with a visual form than when it was incongruent. Importantly, incongruent targets were associated with almost all errors, suggesting that forms automatically captured selection behaviors. These findings demonstrate that mid-level perceptual processes associated with visual form recognition contribute to covert and overt spatial selection. This indicates that neural circuits associated with target selection, such as the superior colliculus, may have privileged access to visual form information.SIGNIFICANCE STATEMENT Spatial selection of visual information either with (overt) or without (covert) foveating eye movements is critical to primate behavior. However, it is still not clear whether spatial maps in sensorimotor regions known to guide overt and covert spatial selection are influenced by peripheral visual forms. We probed the ability of humans and monkeys to perform overt and covert target selection in the presence of spatially congruent or incongruent visual forms. Even when completely task-irrelevant, images of visual objects had a dramatic effect on target selection, acting much like spatial cues used in spatial attention tasks. Our results demonstrate that traditional brain circuits for orienting behaviors, such as the superior colliculus, likely have privileged access to visual object representations.

Rapid stimulus-driven modulation of slow ocular position drifts.

The eyes are never still during maintained gaze fixation. When microsaccades are not occurring, ocular position exhibits continuous slow changes, often referred to as drifts. Unlike microsaccades, drifts remain to be viewed as largely random eye movements. Here we found that ocular position drifts can, instead, be very systematically stimulus-driven, and with very short latencies. We used highly precise eye tracking in three well trained macaque monkeys and found that even fleeting (~8 ms duration) stimulus presentations can robustly trigger transient and stimulus-specific modulations of ocular position drifts, and with only approximately 60 ms latency. Such drift responses are binocular, and they are most effectively elicited with large stimuli of low spatial frequency. Intriguingly, the drift responses exhibit some image pattern selectivity, and they are not explained by convergence responses, pupil constrictions, head movements, or starting eye positions. Ocular position drifts have very rapid access to exogenous visual information.

Vision is a highly complex, active process. As we observe and interact with the world around us, we constantly use eye movements to capture the visual information we need. In fact, our eyes continue to make tiny, unconscious movements even when we try to fix our gaze on something. There are two main types of tiny eye movements. The first kind, so called microsaccades, are fast, microscopic flicks that happen every second or half-second. The other kind, termed drift, is a slower, gradual motion that takes place between microsaccades, or at any time when other eye movements are not happening. However, we know far less about drifts than about any other eye movements: both the reason why they occur and the brain mechanisms controlling them are still unclear. Many scientists think that drifts are largely random movements, without any set direction. However, eye drifts do sometimes align with other behaviours ­ for example, they can help compensate for small, subtle head movements ­ suggesting that drifts may not be completely random after all. Malevich, Buonocore and Hafed therefore set out to test the hypothesis that eye drifts could, under the right circumstances, in fact be highly directed movements. These experiments used precise sensors to track eye movements in macaque monkeys, which had been trained to fix their gaze on images or shapes (stimuli) presented on a screen. This revealed that presenting new stimuli, even for a few thousandths of a second, could repeatedly trigger drifts. This reaction also happened quickly, starting less than one hundredth of a second after presentation of the stimulus. Further tests, using different images, revealed that the drifts were not only simply reacting to any new stimuli but also appeared to be a partially selective response to specific types of images. These tended to have larger features and less fine detail. For example, a picture of a landscape with large swaths of sky or hilltops would much more reliably trigger the eye drifts than a finely detailed checkerboard pattern, with many small squares alternating between black and white. These results suggested that drifts, far from being random movements, could be another tool for the brain to process visual information. This work sheds new light on the potential role of eye movements in vision, and adds another layer of complexity to the question of how we see. Malevich et al. hope that this study will inspire further research into the brain mechanisms behind ocular drifts.

Post-Saccadic Face Processing Is Modulated by Pre-Saccadic Preview: Evidence from Fixation-Related Potentials.

Humans actively sample their environment with saccadic eye movements to bring relevant information into high-acuity foveal vision. Despite being lower in resolution, peripheral information is also available before each saccade. How the pre-saccadic extrafoveal preview of a visual object influences its post-saccadic processing is still an unanswered question. The current study investigated this question by simultaneously recording behavior and fixation-related brain potentials while human subjects made saccades to face stimuli. We manipulated the relationship between pre-saccadic "previews" and post-saccadic images to explicitly isolate the influences of the former. Subjects performed a gender discrimination task on a newly foveated face under three preview conditions: scrambled face, incongruent face (different identity from the foveated face), and congruent face (same identity). As expected, reaction times were faster after a congruent-face preview compared with a scrambled-face preview. Importantly, intact face previews (either incongruent or congruent) resulted in a massive reduction of post-saccadic neural responses. Specifically, we analyzed the classic face-selective N170 component at occipitotemporal electroencephalogram electrodes, which was still present in our experiments with active looking. However, the post-saccadic N170 was strongly attenuated following intact-face previews compared with the scrambled condition. This large and long-lasting decrease in evoked activity is consistent with a trans-saccadic mechanism of prediction that influences category-specific neural processing at the start of a new fixation. These findings constrain theories of visual stability and show that the extrafoveal preview methodology can be a useful tool to investigate its underlying mechanisms.SIGNIFICANCE STATEMENT Neural correlates of object recognition have traditionally been studied by flashing stimuli to the central visual field. This procedure differs in fundamental ways from natural vision, where viewers actively sample the environment with eye movements and also obtain a low-resolution preview of soon-to-be-fixated objects. Here we show that the N170, a classic electrophysiological marker of the structural encoding of faces, also occurs during a more natural viewing condition but is strongly reduced due to extrafoveal preprocessing (preview benefit). Our results therefore highlight the importance of peripheral vision during trans-saccadic processing in building a coherent and stable representation of the world around us.

Memory-guided microsaccades.

Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed "memory-guided" microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior.

The peripheral preview effect with faces: Combined EEG and eye-tracking suggests multiple stages of trans-saccadic predictive and non-predictive processing.

The world appears stable despite saccadic eye-movements. One possible explanation for this phenomenon is that the visual system predicts upcoming input across saccadic eye-movements based on peripheral preview of the saccadic target. We tested this idea using concurrent electroencephalography (EEG) and eye-tracking. Participants made cued saccades to peripheral upright or inverted face stimuli that changed orientation (invalid preview) or maintained orientation (valid preview) while the saccade was completed. Experiment 1 demonstrated better discrimination performance and a reduced fixation-locked N170 component (fN170) with valid than with invalid preview, demonstrating integration of pre- and post-saccadic information. Moreover, the early fixation-related potentials (FRP) showed a preview face inversion effect suggesting that some pre-saccadic input was represented in the brain until around 170 ms post fixation-onset. Experiment 2 replicated Experiment 1 and manipulated the proportion of valid and invalid trials to test whether the preview effect reflects context-based prediction across trials. A whole-scalp Bayes factor analysis showed that this manipulation did not alter the fN170 preview effect but did influence the face inversion effect before the saccade. The pre-saccadic inversion effect declined earlier in the mostly invalid block than in the mostly valid block, which is consistent with the notion of pre-saccadic expectations. In addition, in both studies, we found strong evidence for an interaction between the pre-saccadic preview stimulus and the post-saccadic target as early as 50 ms (Experiment 2) or 90 ms (Experiment 1) into the new fixation. These findings suggest that visual stability may involve three temporal stages: prediction about the saccadic target, integration of pre-saccadic and post-saccadic information at around 50-90 ms post fixation onset, and post-saccadic facilitation of rapid categorization.

Eye Position Error Influence over "Open-Loop" Smooth Pursuit Initiation.

The oculomotor system integrates a variety of visual signals into appropriate motor plans, but such integration can have widely varying time scales. For example, smooth pursuit eye movements to follow a moving target are slower and longer lasting than saccadic eye movements and it has been suggested that initiating a smooth pursuit eye movement involves an obligatory "open-loop" interval in which new visual motion signals presumably cannot influence the ensuing motor plan for up to 100 ms after movement initiation. However, this view is contrary to the idea that the oculomotor periphery has privileged access to short-latency visual signals. Here, we show that smooth pursuit initiation is sensitive to visual inputs, even in open-loop intervals. We instructed male rhesus macaque monkeys to initiate saccade-free smooth pursuit eye movements and injected a transient, instantaneous eye position error signal at different times relative to movement initiation. We found robust short-latency modulations in eye velocity and acceleration, starting only ∼50 ms after transient signal occurrence and even during open-loop pursuit initiation. Critically, the spatial direction of the injected position error signal had predictable effects on smooth pursuit initiation, with forward errors increasing eye acceleration and backward errors reducing it. Catch-up saccade frequencies and amplitudes were also similarly altered ∼50 ms after transient signals, much like the well known effects on microsaccades during fixation. Our results demonstrate that smooth pursuit initiation is highly sensitive to visual signals and that catch-up saccade generation is reset after a visual transient.SIGNIFICANCE STATEMENT Smooth pursuit eye movements allow us to track moving objects. The first ∼100 ms of smooth pursuit initiation are characterized by smooth eye acceleration and are overwhelmingly described as being "open-loop"; that is, unmodifiable by new visual motion signals. We found that all phases of smooth pursuit, including the so-called open-loop intervals, are reliably modifiable by visual signals. We injected transient flashes resulting in very brief, spatially specific position error signals to smooth pursuit and observed very short-latency changes in smooth eye movements to minimize such errors. Our results highlight the flexibility of the oculomotor system in reacting to environmental events and suggest a functional role for the pervasiveness of visual sensitivity in oculomotor control brain regions.

Transfer function of the rhesus macaque oculomotor system for small-amplitude slow motion trajectories.

Two main types of small eye movements occur during gaze fixation: microsaccades and slow ocular drifts. While microsaccade generation has been relatively well studied, ocular drift control mechanisms are unknown. Here we explored the degree to which monkey smooth eye movements, on the velocity scale of slow ocular drifts, can be generated systematically. Two male rhesus macaque monkeys tracked a spot moving sinusoidally, but slowly, along the horizontal or vertical direction. Maximum target displacement in the motion trajectory was 30 min arc (0.5°), and we varied the temporal frequency of target motion from 0.2 to 5 Hz. We obtained an oculomotor "transfer function" by measuring smooth eye velocity gain (relative to target velocity) as a function of frequency, similar to past work with large-amplitude pursuit. Monkey eye velocities as slow as those observed during slow ocular drifts were clearly target motion driven. Moreover, as with large-amplitude smooth pursuit, eye velocity gain varied with temporal frequency. However, unlike with large-amplitude pursuit, exhibiting low-pass behavior, small-amplitude motion tracking was band pass, with the best ocular movement gain occurring at ~0.8-1 Hz. When oblique directions were tested, we found that the horizontal component of pursuit gain was larger than the vertical component. Our results provide a catalog of the control abilities of the monkey oculomotor system for slow target motions, and they also support the notion that smooth fixational ocular drifts are controllable. This has implications for neural investigations of drift control and the image-motion consequences of drifts on visual coding in early visual areas. NEW & NOTEWORTHY We studied the efficacy of monkey smooth pursuit eye movements for very slow target velocities. Pursuit was impaired for sinusoidal motions of frequency less than ~0.8-1 Hz. Nonetheless, eye trajectory was still sinusoidally modulated, even at velocities lower than those observed during gaze fixation with slow ocular drifts. Our results characterize the slow control capabilities of the monkey oculomotor system and provide a basis for future understanding of the neural mechanisms for slow ocular drifts.

Saccade Reorienting Is Facilitated by Pausing the Oculomotor Program.

As we look around the world, selecting our targets, competing events may occur at other locations. Depending on current goals, the viewer must decide whether to look at new events or to ignore them. Two experimental paradigms formalize these response options: double-step saccades and saccadic inhibition. In the first, the viewer must reorient to a newly appearing target; in the second, they must ignore it. Until now, the relationship between reorienting and inhibition has been unexplored. In three experiments, we found saccadic inhibition ∼100 msec after a new target onset, regardless of the task instruction. Moreover, if this automatic inhibition is boosted by an irrelevant flash, reorienting is facilitated, suggesting that saccadic inhibition plays a crucial role in visual behavior, as a bottom-up brake that buys the time needed for decisional processes to act. Saccadic inhibition may be a ubiquitous pause signal that provides the flexibility for voluntary behavior to emerge.

Pre-saccadic perception: Separate time courses for enhancement and spatial pooling at the saccade target.

We interact with complex scenes using eye movements to select targets of interest. Studies have shown that the future target of a saccadic eye movement is processed differently by the visual system. A number of effects have been reported, including a benefit for perceptual performance at the target ("enhancement"), reduced influences of backward masking ("un-masking"), reduced crowding ("un-crowding") and spatial compression towards the saccade target. We investigated the time course of these effects by measuring orientation discrimination for targets that were spatially crowded or temporally masked. In four experiments, we varied the target-flanker distance, the presence of forward/backward masks, the orientation of the flankers and whether participants made a saccade. Masking and randomizing flanker orientation reduced performance in both fixation and saccade trials. We found a small improvement in performance on saccade trials, compared to fixation trials, with a time course that was consistent with a general enhancement at the saccade target. In addition, a decrement in performance (reporting the average flanker orientation, rather than the target) was found in the time bins nearest saccade onset when random oriented flankers were used, consistent with spatial pooling around the saccade target. We did not find strong evidence for un-crowding. Overall, our pattern of results was consistent with both an early, general enhancement at the saccade target and a later, peri-saccadic compression/pooling towards the saccade target.

Alteration of the microsaccadic velocity-amplitude main sequence relationship after visual transients: implications for models of saccade control.

Microsaccades occur during gaze fixation to correct for miniscule foveal motor errors. The mechanisms governing such fine oculomotor control are still not fully understood. In this study, we explored microsaccade control by analyzing the impacts of transient visual stimuli on these movements' kinematics. We found that such kinematics can be altered in systematic ways depending on the timing and spatial geometry of visual transients relative to the movement goals. In two male rhesus macaques, we presented peripheral or foveal visual transients during an otherwise stable period of fixation. Such transients resulted in well-known reductions in microsaccade frequency, and our goal was to investigate whether microsaccade kinematics would additionally be altered. We found that both microsaccade timing and amplitude were modulated by the visual transients, and in predictable manners by these transients' timing and geometry. Interestingly, modulations in the peak velocity of the same movements were not proportional to the observed amplitude modulations, suggesting a violation of the well-known "main sequence" relationship between microsaccade amplitude and peak velocity. We hypothesize that visual stimulation during movement preparation affects not only the saccadic "Go" system driving eye movements but also a "Pause" system inhibiting them. If the Pause system happens to be already turned off despite the new visual input, movement kinematics can be altered by the readout of additional visually evoked spikes in the Go system coding for the flash location. Our results demonstrate precise control over individual microscopic saccades and provide testable hypotheses for mechanisms of saccade control in general.NEW & NOTEWORTHY Microsaccadic eye movements play an important role in several aspects of visual perception and cognition. However, the mechanisms for microsaccade control are still not fully understood. We found that microsaccade kinematics can be altered in a systematic manner by visual transients, revealing a previously unappreciated and exquisite level of control by the oculomotor system of even the smallest saccades. Our results suggest precise temporal interaction between visual, motor, and inhibitory signals in microsaccade control.