Sensory processing of motor inaccuracy depends on previously performed movement and on subsequent motor corrections: a study of the saccadic system

When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.     

Lateralization of saccadic latency during monocular presentation of stimuli to a leading and non-leading eye

Saccadic latencies were studied in ten healthy subjects. Peripheral targets were presented monocularly to a leading and nonleading eyes in the right and left hemifields. SS (single step) and OVERLAP (200 ms) schemes of visual stimulation were used. Under OVERLAP conditions, the saccadic latency was longer by 30-39 ms and the number of long-latency saccades was higher than under SS conditions, especially in subjects with mixed asymmetry profiles. In the majority of subjects with right asymmetry profile, the latencies of saccades during stimulation of the leading eye were by 12 ms shorter than during stimulation of the nonleading eye, and the latencies of right saccades were by 24 ms shorter than that of the left saccades independently of the stimulated eye. The obtained results explain some characteristic features of hemyspheric asymmetry in organization of saccadic movements.     

Error Correcting Mechanisms during Antisaccades: Contribution of Online Control during Primary Saccades and Offline Control via Secondary Saccades

Errors in eye movements can be corrected during the ongoing saccade through in-flight modifications (i.e., online control), or by programming a secondary eye movement (i.e., offline control). In a reflexive saccade task, the oculomotor system can use extraretinal information (i.e., efference copy) online to correct errors in the primary saccade, and offline retinal information to generate a secondary corrective saccade. The purpose of this study was to examine the error correction mechanisms in the antisaccade task. The roles of extraretinal and retinal feedback in maintaining eye movement accuracy were investigated by presenting visual feedback at the spatial goal of the antisaccade. We found that online control for antisaccade is not affected by the presence of visual feedback; that is whether visual feedback is present or not, the duration of the deceleration interval was extended and significantly correlated with reduced antisaccade endpoint error. We postulate that the extended duration of deceleration is a feature of online control during volitional saccades to improve their endpoint accuracy. We found that secondary saccades were generated more frequently in the antisaccade task compared to the reflexive saccade task. Furthermore, we found evidence for a greater contribution from extraretinal sources of feedback in programming the secondary “corrective” saccades in the antisaccade task. Nonetheless, secondary saccades were more corrective for the remaining antisaccade amplitude error in the presence of visual feedback of the target. Taken together, our results reveal a distinctive online error control strategy through an extension of the deceleration interval in the antisaccade task. Target feedback does not improve online control, rather it improves the accuracy of secondary saccades in the antisaccade task.     

The Human Frontal Oculomotor Cortical Areas Contribute Asymmetrically to Motor Planning in a Gap Saccade Task

Background

Saccadic eye movements are used to rapidly align the fovea with the image of objects of interest in peripheral vision. We have recently shown that in children there is a high preponderance of quick latency but poorly planned saccades that consistently fall short of the target goal. The characteristics of these multiple saccades are consistent with a lack of proper inhibitory control of cortical oculomotor areas on the brainstem saccade generation circuitry.

Methodology/Principal Findings

In the present paper, we directly tested this assumption by using single pulse transcranial magnetic stimulation (TMS) to transiently disrupt neuronal activity in the frontal eye fields (FEF) and supplementary eye fields (SEF) in adults performing a gap saccade task. The results showed that the incidence of multiple saccades was increased for ispiversive but not contraversive directions for the right and left FEF, the left SEF, but not for the right SEF. Moreover, this disruption was most substantial during the ∼50 ms period around the appearance of the peripheral target. A control condition in which the dorsal motor cortex was stimulated demonstrated that this was not due to any non-specific effects of the TMS influencing the spatial distribution of attention.

Conclusions/Significance

Taken together, the results are consistent with a direction-dependent role of the FEF and left SEF in delaying the release of saccadic eye movements until they have been fully planned.     

Binocular coordination of the eyes during reading

Saccadic eye movements and fixations are the behavioral means by which we visually sample text during reading. Human oculomotor control is governed by a complex neurophysiological system involving the brain stem, superior colliculus, and several cortical areas. A very widely held belief among researchers investigating primate vision is that the oculomotor system serves to orient the visual axes of both eyes to fixate the same target point in space. It is argued that such precise positioning of the eyes is necessary to place images on corresponding retinal locations, such that on each fixation a single, nondiplopic, visual representation is perceived. Vision works actively through a continual sampling process involving saccades and fixations. Here we report that during normal reading, the eyes do not always fixate the same letter within a word. We also demonstrate that saccadic targeting is yoked and based on a unified cyclopean percept of a whole word since it is unaffected if different word parts are delivered exclusively to each eye via a dichoptic presentation technique. These two findings together suggest that the visual signal from each eye is fused at a very early stage in the visual pathway, even when the fixation disparity is greater than one character (0.29 deg), and that saccade metrics for each eye are computed on the basis of that fused signal.     

The “efferent copy” hypothesis in saccadic programming in cats

Eye movements were investigated in cats while following a visual target. Wire coils implanted into the eyes served as transducers; the animal was placed in a revolving magnetic field (the magnetic search coil technique). The linear nature of amplitude-velocity relationships in saccadic eye movements was demonstrated. With combined head and eye movements, slope of plot was unrelated to maximum velocity of head movement over the entire test range (of up to 250 deg/sec); saccades decelerated when the head was immobile. Duration of gaze shift rose as it increased in amplitude. Amplitude of gaze was found to depend on head velocity. Experimentally obtained data on the interaction between head and eye movements when combined in following a target may be interpreted from the aspect of a mechanism operating to suppress saccadic signals by an efferent copy signal for head movement.M. V. Lomonosov State University, Moscow. Translated from Neirofiziologiya, Vol. 20, No. 5, pp. 631–637, September–October, 1988.     

Eye and head movements to visual and auditory targets

Coordinated eye-head movements evoked by the presentation of visual, auditory and combined audio-visual targets were studied in 24 human subjects. At 60 deg located targets latencies of eye and head movements were shorter for auditory than for visual stimuli. Latencies were shorter for bisensory than for monosensory targets. The eye and head latencies were differently influenced by the modality of the stimulus when the eccentricity of the target was changed, but not by the variation of the stimulus duration. The different responses of the eye and the head depending on target modality and target eccentricity can be partially attributed to perceptual and central processing mechanisms, and are important to answer the question about the initial event in coordinated eye-head orientation.     

Saccadic eye movements modulate visual responses in the lateral geniculate nucleus

We studied the effects of saccadic eye movements on visual signaling in the primate lateral geniculate nucleus (LGN), the earliest stage of central visual processing. Visual responses were probed with spatially uniform flickering stimuli, so that retinal processing was uninfluenced by eye movements. Nonetheless, saccades had diverse effects, altering not only response strength but also the temporal and chromatic properties of the receptive field. Of these changes, the most prominent was a biphasic modulation of response strength, weak suppression followed by strong enhancement. Saccadic modulation was widespread, and affected both of the major processing streams in the LGN. Our results demonstrate that during natural viewing, thalamic response properties can vary dramatically, even over the course of a single fixation.     

Influence of Retinal Image Shifts and Extra-Retinal Eye Movement Signals on Binocular Rivalry Alternations

Previous studies have indicated that saccadic eye movements correlate positively with perceptual alternations in binocular rivalry, presumably because the foveal image changes resulting from saccades, rather than the eye movement themselves, cause switches in awareness. Recently, however, we found evidence that retinal image shifts elicit so-called onset rivalry and not percept switches as such. These findings raise the interesting question whether onset rivalry may account for correlations between saccades and percept switches.We therefore studied binocular rivalry when subjects made eye movements across a visual stimulus and compared it with the rivalry in a ‘replay’ condition in which subjects maintained fixation while the same retinal displacements were reproduced by stimulus displacements on the screen. We used dichoptic random-dot motion stimuli viewed through a stereoscope, and measured eye and eyelid movements with scleral search-coils.Positive correlations between retinal image shifts and perceptual switches were observed for both saccades and stimulus jumps, but only for switches towards the subjects'' preferred eye at stimulus onset. A similar asymmetry was observed for blink-induced stimulus interruptions. Moreover, for saccades, amplitude appeared crucial as the positive correlation persisted for small stimulus jumps, but not for small saccades (amplitudes < 1°). These findings corroborate our tenet that saccades elicit a form of onset rivalry, and that rivalry is modulated by extra-retinal eye movement signals.     

Probability of Seeing Increases Saccadic Readiness

Associating movement directions or endpoints with monetary rewards or costs influences movement parameters in humans, and associating movement directions or endpoints with food reward influences movement parameters in non-human primates. Rewarded movements are facilitated relative to non-rewarded movements. The present study examined to what extent successful foveation facilitated saccadic eye movement behavior, with the hypothesis that foveation may constitute an informational reward. Human adults performed saccades to peripheral targets that either remained visible after saccade completion or were extinguished, preventing visual feedback. Saccades to targets that were systematically extinguished were slower and easier to inhibit than saccades to targets that afforded successful foveation, and this effect was modulated by the probability of successful foveation. These results suggest that successful foveation facilitates behavior, and that obtaining the expected sensory consequences of a saccadic eye movement may serve as a reward for the oculomotor system.     

Counterproductive Effect of Saccadic Suppression during Attention Shifts

During saccadic eye movements, the processing of visual information is transiently interrupted by a mechanism known as “saccadic suppression” [1] that is thought to ensure perceptual stability [2]. If, as proposed in the premotor theory of attention [3], covert shifts of attention rely on sub-threshold recruitment of oculomotor circuits, then saccadic suppression should also occur during covert shifts. In order to test this prediction, we designed two experiments in which participants had to orient towards a cued letter, with or without saccades. We analyzed the time course of letter identification score in an “attention” task performed without saccades, using the saccadic latencies measured in the “saccade” task as a marker of covert saccadic preparation. Visual conditions were identical in all tasks. In the “attention” task, we found a drop in perceptual performance around the predicted onset time of saccades that were never performed. Importantly, this decrease in letter identification score cannot be explained by any known mechanism aligned on cue onset such as inhibition of return, masking, or microsaccades. These results show that attentional allocation triggers the same suppression mechanisms as during saccades, which is relevant during eye movements but detrimental in the context of covert orienting.     

Attention governs action in the primate frontal eye field

While the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Rather than simply impose a fixed-vector signal, subthreshold stimulation directed saccades away from the FEF movement field, and instead more strongly in the direction of visual motion. These results demonstrate that the attentional effects of FEF stimulation govern visually guided saccades, and suggest that the two roles of the FEF work together to select both the features of a target and the appropriate movement to foveate it.     

Bumblebee Homing: The Fine Structure of Head Turning Movements

Changes in flight direction in flying insects are largely due to roll, yaw and pitch rotations of their body. Head orientation is stabilized for most of the time by counter rotation. Here, we use high-speed video to analyse head- and body-movements of the bumblebee Bombus terrestris while approaching and departing from a food source located between three landmarks in an indoor flight-arena. The flight paths consist of almost straight flight segments that are interspersed with rapid turns. These short and fast yaw turns (“saccades”) are usually accompanied by even faster head yaw turns that change gaze direction. Since a large part of image rotation is thereby reduced to brief instants of time, this behavioural pattern facilitates depth perception from visual motion parallax during the intersaccadic intervals. The detailed analysis of the fine structure of the bees’ head turning movements shows that the time course of single head saccades is very stereotypical. We find a consistent relationship between the duration, peak velocity and amplitude of saccadic head movements, which in its main characteristics resembles the so-called "saccadic main sequence" in humans. The fact that bumblebee head saccades are highly stereotyped as in humans, may hint at a common principle, where fast and precise motor control is used to reliably reduce the time during which the retinal images moves.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Saccadic automatism in babies during rapid sleep

Characteristics of rapid eye movements (saccades) in babies (six babies of 1-8 months age) recorded by electrooculography method in paradoxical phase of sleep are analyzed in comparison with analogous data in adults during sleep and in alertness in various conditions of eye movements recording. Coincidence of distribution curves of intersaccadic intervals and amplitudes of saccades in babies and adults is revealed. It is also found that the most frequently met intervals (in the range up to 1 s) in sleep and wakefulness are of comparable values 71.5-90.5%. On the basis of the obtained data the suggestion is made about automation of saccades, forming the base of saccadic activity and manifested in babies and adults during sleep and also in wakefulness, against the background of which other kinds of oculomotor activity are realized. Automation of saccades is formed in early ontogenesis.     

Saccades during Attempted Fixation in Parkinsonian Disorders and Recessive Ataxia: From Microsaccades to Square-Wave Jerks

During attempted visual fixation, saccades of a range of sizes occur. These “fixational saccades” include microsaccades, which are not apparent in regular clinical tests, and “saccadic intrusions”, predominantly horizontal saccades that interrupt accurate fixation. Square-wave jerks (SWJs), the most common type of saccadic intrusion, consist of an initial saccade away from the target followed, after a short delay, by a “return saccade” that brings the eye back onto target. SWJs are present in most human subjects, but are prominent by their increased frequency and size in certain parkinsonian disorders and in recessive, hereditary spinocerebellar ataxias. Here we asked whether fixational saccades showed distinctive features in various parkinsonian disorders and in recessive ataxia. Although some saccadic properties differed between patient groups, in all conditions larger saccades were more likely to form SWJs, and the intervals between the first and second saccade of SWJs were similar. These findings support the proposal of a common oculomotor mechanism that generates all fixational saccades, including microsaccades and SWJs. The same mechanism also explains how the return saccade in SWJs is triggered by the position error that occurs when the first saccadic component is large, both in the healthy brain and in neurological disease.     

The saccadic and neurological deficits in type 3 Gaucher disease

Our objective was to characterize the saccadic eye movements in patients with type 3 Gaucher disease (chronic neuronopathic) in relationship to neurological and neurophysiological abnormalities. For approximately 4 years, we prospectively followed a cohort of 15 patients with Gaucher type 3, ages 8-28 years, by measuring saccadic eye movements using the scleral search coil method. We found that patients with type 3 Gaucher disease had a significantly higher regression slope of duration vs amplitude and peak duration vs amplitude compared to healthy controls for both horizontal and vertical saccades. Saccadic latency was significantly increased for horizontal saccades only. Downward saccades were more affected than upward saccades. Saccade abnormalities increased over time in some patients reflecting the slowly progressive nature of the disease. Phase plane plots showed individually characteristic patterns of abnormal saccade trajectories. Oculo-manual dexterity scores on the Purdue Pegboard test were low in virtually all patients, even in those with normal cognitive function. Vertical saccade peak duration vs amplitude slope significantly correlated with IQ and with the performance on the Purdue Pegboard but not with the brainstem and somatosensory evoked potentials. We conclude that, in patients with Gaucher disease type 3, saccadic eye movements and oculo-manual dexterity are representative neurological functions for longitudinal studies and can probably be used as endpoints for therapeutic clinical trials. TRIAL REGISTRATION: ClinicalTrials.gov NCT00001289.     

Both Lexical and Non-Lexical Characters Are Processed during Saccadic Eye Movements

On average our eyes make 3–5 saccadic movements per second when we read, although their neural mechanism is still unclear. It is generally thought that saccades help redirect the retinal fovea to specific characters and words but that actual discrimination of information only occurs during periods of fixation. Indeed, it has been proposed that there is active and selective suppression of information processing during saccades to avoid experience of blurring due to the high-speed movement. Here, using a paradigm where a string of either lexical (Chinese) or non-lexical (alphabetic) characters are triggered by saccadic eye movements, we show that subjects can discriminate both while making saccadic eye movement. Moreover, discrimination accuracy is significantly better for characters scanned during the saccadic movement to a fixation point than those not scanned beyond it. Our results showed that character information can be processed during the saccade, therefore saccades during reading not only function to redirect the fovea to fixate the next character or word but allow pre-processing of information from the ones adjacent to the fixation locations to help target the next most salient one. In this way saccades can not only promote continuity in reading words but also actively facilitate reading comprehension.     

Looking for Discriminating Is Different from Looking for Looking’s Sake

Recent studies provide evidence for task-specific influences on saccadic eye movements. For instance, saccades exhibit higher peak velocity when the task requires coordinating eye and hand movements. The current study shows that the need to process task-relevant visual information at the saccade endpoint can be, in itself, sufficient to cause such effects. In this study, participants performed a visual discrimination task which required a saccade for successful completion. We compared the characteristics of these task-related saccades to those of classical target-elicited saccades, which required participants to fixate a visual target without performing a discrimination task. The results show that task-related saccades are faster and initiated earlier than target-elicited saccades. Differences between both saccade types are also noted in their saccade reaction time distributions and their main sequences, i.e., the relationship between saccade velocity, duration, and amplitude.     

Oculomotor activities in monkeys with N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced syndrome of parkinsonism

In twoMacaca rhesus monkeys that received repeated N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) injections (single dose 0.2 mg/kg, i.m.; cumulative dose 11.2–13.3 mg), changes in characteristics of spontaneous saccadic eye movements and vestibulo-ocular reflex (VOR) were evaluated. With the development of severe behavioral disturbances, amplitude of spontaneous saccadic eye movements gradually decreased. Pronounced changes in duration of saccadic eye movements, frequency of spontaneous saccades, and their pattern were observed. No changes in parameters of VOR slow component were recorded, but high total MPTP doses suppressed fast phase of the reflex.Neirofiziologiya/Neurophysiology, Vol. 25, No. 3, pp. 184–190, May–June, 1993.