Investigating saccade programming in the praying mantis Tenodera aridifolia using distracter interference paradigms

To investigate the saccadic system in the mantis, I applied distracter interference paradigms. These involved presenting the mantis with a fixation target and one or several distracters supposed to affect saccades towards the target. When a single target was presented, a medium-sized target located in its lower visual field elicited higher rates of saccade response. This preference for target size and position was also observed when a target and a distracter were presented simultaneously. That is, the mantis chose and fixated the target rather than a distracter that was much smaller or larger than the target, or was located above the target. Furthermore, the mantis' preference was not affected by increasing the number of distracters. However, the presence of the distracter decreased the occurrence rate of saccade and increased the response time to saccade. I conclude that distracter interference paradigms are an effective way of investigating the visual processing underlying saccade generation in the mantis. Possible mechanisms of saccade generation in the mantis are discussed.     

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.     

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.     

Saccadic Momentum and Facilitation of Return Saccades Contribute to an Optimal Foraging Strategy

The interest in saccadic IOR is funneled by the hypothesis that it serves a clear functional purpose in the selection of fixation points: the facilitation of foraging. In this study, we arrive at a different interpretation of saccadic IOR. First, we find that return saccades are performed much more often than expected from the statistical properties of saccades and saccade pairs. Second, we find that fixation durations before a saccade are modulated by the relative angle of the saccade, but return saccades show no sign of an additional temporal inhibition. Thus, we do not find temporal saccadic inhibition of return. Interestingly, we find that return locations are more salient, according to empirically measured saliency (locations that are fixated by many observers) as well as stimulus dependent saliency (defined by image features), than regular fixation locations. These results and the finding that return saccades increase the match of individual trajectories with a grand total priority map evidences the return saccades being part of a fixation selection strategy that trades off exploration and exploitation.     

Cognitive Control of Saccadic Eye Movements in Children with Developmental Coordination Disorder

The ability to use advance information to prepare and execute a movement requires cognitive control of behaviour (e.g., anticipation and inhibition). Our aim was to explore the integrity of saccadic eye movement control in developmental coordination disorder (DCD) and typically developing (TD) children (8–12 years) and assess how these children plan and inhibit saccadic responses, the principal mechanisms within visual attention control. Eye movements and touch responses were measured (separately and concurrently) in Cued and Non-Cued conditions. We found that children with DCD had similar saccade kinematics to the TD group during saccade initiation. Advance information decreased hand movement duration in both groups during Cued trials, but decrements in accuracy were significantly worse in the DCD group. In addition, children with DCD exhibited greater inhibitory errors and inaccurate fixation during the Cued trials. Thus, children with DCD were reasonably proficient in executing saccades during reflexive (Non-Cued) conditions, but showed deficits in more complex control processes involving prediction and inhibition. These findings have implications for our understanding of motor control in children with DCD.     

Different programming modes of human saccadic eye movements as a function of stimulus eccentricity: Indications of a functional subdivision of the visual field

1. Voluntary saccadic eye movements were made toward flashes of light on the horizontal meridian, whose duration and distance from the point of fixation were varied; eye movements were measured using d.c.-electrooculography.—2. Targets within 10°–15° eccentricity are usually reached by one saccadic eye movement. When the eyes turn toward targets of more than 10°–15° eccentricity, the first saccadic eye movement falls short of the target by an angle usually not exceeding 10°. The presence of the image of the target off the fovea (visual error signal) subsequent to such an undershoot elicits, after a short interval, corrective saccades (usually one) which place the image of the target on the fovea. In the absence of a visual error signal, the probability of occurrence of corrective saccades is low, but it increases with greater target eccentricities. These observations suggest that there are different, eccentricity-dependent modes of programming saccadic eye movements.—3. Saccadic eye movements appear to be programmed in retinal coordinates. This conclusion is based on the observations that, irrespective of the initial position of the eyes in the orbit, a) there are different programming modes for eye movements to targets within and beyond 10°–15° from the fixation point, and b_ the maximum velocity of saccadic eye movements is always reached at 25° to 30° target eccentricity. —4. Distributions of latency and intersaccadic interval (ISI) are frequently multimodal, with a separation between modes of 30 to 40 msec. These observations suggest that saccadic eye movements are produced by mechanisms which, at a frequency of 30 Hz, process visual information. —5. Corrective saccades may occur after extremely short intervals (30 to 60 msec) regardless of whether or not a visual error signal is present; the eyes may not even come to a complete stop during these very short intersaccadic intervals. It is suggested that these corrective saccades are triggered by errors in the programming of the initial saccadic eye movements, and not by a visual error signal. —6. The exitence of different, eccentricity-dependent programming modes of saccadic eye movements, is further supported by anatomical, physiological, psychophysical, and neuropathological observations that suggest a dissociation of visual functions dependent on retinal eccentricity. Saccadic eye movements to targets more eccentric than 10°–15° appear to be executed by a mechanism involving the superior colliculus (perhaps independent of the visual cortex), whereas saccadic eye movements to less eccentric targets appear to depend on a mechanism involving the geniculo-cortical pathway (perhaps in collaboration with the superior colliculus).     

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.     

Saccadic tracking of a light grey target in the mantis,Tenodera aridifolia

I presented a horizontally moving square on a computer display to the mantis, Tenodera aridifolia, and examined the effects of target brightness and velocity, and background brightness on its tracking behavior. The mantis tracked a light grey square with more saccadic head movements than a black square, although these squares moved on a homogeneous background. The amplitude of saccades was larger when the light grey square moved at a lower velocity. The background brightness had little effect on the type (smooth or saccadic) of tracking behavior. These results suggest that the saccadic tracking of light grey objects on a homogeneous background may not be caused by low contrast, i.e., the difficulty in discriminating the object from the background. The possible biological significance of saccadic tracking on a homogenous background is discussed.     

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.     

Ocular-Motor Profile and Effects of Memantine in a Familial Form of Adult Cerebellar Ataxia with Slow Saccades and Square Wave Saccadic Intrusions

Fixation instability due to saccadic intrusions is a feature of autosomal recessive spinocerebellar ataxias, and includes square wave intrusions (SWI) and macrosaccadic oscillations (MSO). A recent report suggested that the non-competitive antagonist of NMDA receptors, memantine, could decrease MSO and improve fixation in patients with spinocerebellar ataxia with saccadic intrusions (SCASI). We similarly tested two sisters, respectively of 58 and 60 years, with an unrecognized form of recessive, adult-onset cerebellar ataxia, peripheral neuropathy and slow saccades, who showed prominent SWI and also complained with difficulty in reading. We tested horizontal visually guided saccades (10°–18°) and three minutes of steady fixation in each patient and in thirty healthy controls. Both patients showed a significant reduction of peak and mean velocity compared with control subjects. Large SWI interrupting steady fixation were prominent during steady fixation and especially following visually guided saccades. Eye movements were recorded before and during the treatment with memantine, 20 mg/daily for 6 months. The treatment with memantine reduced both the magnitude and frequency of SWI (the former significantly), but did not modified neurological conditions or saccade parameters. Thus, our report suggests that memantine may have some general suppressive effect on saccadic intrusions, including both SWI and MSO, thereby restoring the capacity of reading and visual attention in these and in other recessive forms of ataxia, including Friedreich’s, in which saccadic intrusions are prominent.     

A Mathematical Model of Optimal Saccadic Eye Movement by a Pair of Muscles

This paper presents a model of saccadic eye movements. Eye movements are considered as being ballistic, since saccades (rapid concurrent movements of both eyes) occur several hundred thousand times per day; visual perception of the environment is interrupted by a saccade. The optimal control was constructed for the motion considered in three consecutively refined assumptions. The controls included in the time-optimal problem were the resultant moment of force exerted by the extraocular muscles, individual moments of force exerted by either muscle of the agonist–antagonist pair, and finally, the rate of change of these moments. This approach is consistent with the view that is currently upheld by physiologists, who believe that a saccade is programmed by the central nervous system before the beginning of an eye movement and is scarcely adjusted during the movement itself. The solution of the optimal control problem and the results obtained by subsequent numerical modeling of saccadic trajectories were compared with the published experimental data. The saccadic trajectories were compared based on the main sequence, the known consistent relationship between saccade amplitude and duration, which is the most widely applied and commonly accepted way of describing saccade data. The main sequence of saccades obtained from the solution of the optimal control problem formulated in the most complete form agreed well with published experimental results.     

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.     

On the predominance of anti-compensatory eye movements in vestibular nystagmus

The predominance of anti-compensatory eye movements in vestibular nystagmus recorded during sinusoidal and post-rotational tests is interpreted in terms of a mathematical model of the vestibulo-ocular system. Namely, a direct pathway between the vestibular nuclei and the saccadic mechanism is assumed. In the range of frequencies of natural head movements this pathway carries on a signal proportional to head angular velocity. Therefore, during active head movements the saccadic mechanism is forced to produce quick eye rotations in the direction of head movement and, thus, to cooperate in the task of picking up visual targets outside the visual field. During passive head movements giving rise to nystagmus the assumed pathway contributes to reduce the error in eye resetting due to the saccadic delay. Analytical considerations and simulation results seem to prove the adequacy of the proposed model.Work supported by the National Research Council (C.N.R.), Rome, Italy     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Human fast negative EEG potentials before express saccades

Fast negative EEG potentials preceding fast regular saccades and express saccades were studied by the method of backward averaging under conditions of monocular stimulation of the right and left eye. "Step" and "gap" experimental paradigms were used for visual stimulation. Analysis of parameters of potentials and their spatiotemporal dynamics suggests that, under conditions of the increased attention and optimal readiness of the neural structures, express saccades appear when the previously chosen program of the future eye movement coincides with the actual target coordinates. We assumed that the saccade latency decreases at the expense of the involvement of the main oculomotor areas of motor and saccadic planning in its initiation; an express saccade can be initiated also by means of direct transmission of the signal from the cortex to the brainstem saccadic generator passing by the superior colliculus. Moreover, anticipating release from the central fixation and attention distraction are necessary for the successful initiation of an express saccade.     

Response of the Praying Mantis,Sphodromantis Viridis,to Target Change in Size and to Target Visual Occlusion

Mantises (Mantodea, Mantidae) visually detect insect prey and capture it by a ballistic strike of their specialized forelegs. We tested predatory responses of female mantis, Sphodromantis viridis, to computer generated visual stimuli, to determine the effects of (i) target size and velocity (ii) discrete changes in target size and (iii) visual occlusion. Maximal predatory responses were elicited by stimuli that (i) subtended ~20°–23° horizontally and ~16°–19° vertically, at the eye, and moved across the screen at angular velocities of ~46°–119°/s, (ii) increased in size in a stepwise manner, with step duration ≥0.8 s, while stimuli decreasing in size elicited only peering movements, (iii) Stimuli disappearing gradually behind a virtual occlusion elicited one or more head saccades but not actual interception.     

Directional prediction by the saccadic system

One popular and fruitful approach to understanding what influences the decision of where to look next has been to present targets in a series of trials either to the right or left of a central fixation point and examine sequential effects on saccadic latency. However, there is a problem with this paradigm: Every saccade to a target is necessarily followed by an equal and opposite movement back to the center, yet the potentially confounding influence of this refixation saccade is rarely considered. Here, we introduce a novel random-walk paradigm that eliminates this difficulty. Each successive target appears to the left or right of the previous one, allowing us to study long sequences of saccades uncontaminated by refixations. This exposes a new stimulus-history effect, which is remarkably prolonged and relates primarily to movement direction: A saccade reduces the latency for subsequent movements made in the same direction and retards those in the opposite direction. Although in conventional refixation paradigms this effect cancels out, it is of particular significance in the real world--where our fixation point shifts constantly with the object of interest--and reflects a prediction of the way that real objects typically move.     

The Fixation and Saccade P3

Although most instances of object recognition during natural viewing occur in the presence of saccades, the neural correlates of objection recognition have almost exclusively been examined during fixation. Recent studies have indicated that there are post-saccadic modulations of neural activity immediately following eye movement landing; however, whether post-saccadic modulations affect relatively late occurring cognitive components such as the P3 has not been explored. The P3 as conventionally measured at fixation is commonly used in brain computer interfaces, hence characterizing the post-saccadic P3 could aid in the development of improved brain computer interfaces that allow for eye movements. In this study, the P3 observed after saccadic landing was compared to the P3 measured at fixation. No significant differences in P3 start time, temporal persistence, or amplitude were found between fixation and saccade trials. Importantly, sensory neural responses canceled in the target minus distracter comparisons used to identify the P3. Our results indicate that relatively late occurring cognitive neural components such as the P3 are likely less sensitive to post saccadic modulations than sensory neural components and other neural activity occurring shortly after eye movement landing. Furthermore, due to the similarity of the fixation and saccade P3, we conclude that the P3 following saccadic landing could possibly be used as a viable signal in brain computer interfaces allowing for eye movements.     

Natural and drug-induced variations of velocity and duration of human saccadic eye movements: Evidence for a control of the neural pulse generator by local feedback

The present report considers goal directed human saccadic eye movements. It addresses the question how a given perceived target excentricity is transformed into the innervation pattern that creates the saccade to the target. More specifically, it investigates whether this pattern is an appropriately selected preprogram or whether it is continuously controlled by a local feedback loop that compares a non-visual eye position signal to the perceived target excentricity (a visual signal would be too slow). To this end, the relation between the accuracy of saccades aimed at a given target and their velocity and duration was examined. Duration and velocity were found to vary by as much as 60% while the amplitude showed no related variation and had an almost constant accuracy of about 90%. By administrating diazepam, the variability of saccade duration and velocity could be further increased, but still the amplitude remained almost constant. These results favour the hypothesis that saccadic innervation is controlled by a local feedback loop.This investigation was supported by Deutsche Forschungsgemeinschaft, SFB 70, Gruppe Ulm     

Effects of luminance, size, and angular velocity on the recognition of nonlocomotive prey models by the praying mantis

Adult females of the mantis Tenodera angustipennis were presented with the "nonlocomotive" prey model, a static rectangle with two lines oscillating regularly at its sides, generated on a computer display. The models were varied in rectangle luminance (black, gray, and light gray), rectangle height (0.72, 3.6, and 18 mm), rectangle width (0.72, 3.6, and 18 mm), and angular velocity of oscillating lines (65°, 260°, and 1040°/s) to examine their effects on prey recognition. Before striking the model, the mantis sometimes showed peering movements that involved swaying its body from side to side. The black model of medium size (both height and width) elicited higher rates of fixation, peering, and strike responses than the large, small, or gray model. The model of medium angular velocity elicited a higher strike rate than that of large or small angular velocity, but angular velocity had little effect on fixation and peering. We conclude that mantises respond to a rectangle in deciding whether to fixate, and to both rectangle and lines in deciding whether to strike after fixation. Received: September 2, 1999 / Accepted: March 21, 2000