Adaptation of catch-up saccades during the initiation of smooth pursuit eye movements

Reduction of retinal speed and alignment of the line of sight are believed to be the respective primary functions of smooth pursuit and saccadic eye movements. As the eye muscles strength can change in the short-term, continuous adjustments of motor signals are required to achieve constant accuracy. While adaptation of saccade amplitude to systematic position errors has been extensively studied, we know less about the adaptive response to position errors during smooth pursuit initiation, when target motion has to be taken into account to program saccades, and when position errors at the saccade endpoint could also be corrected by increasing pursuit velocity. To study short-term adaptation (250 adaptation trials) of tracking eye movements, we introduced a position error during the first catch-up saccade made during the initiation of smooth pursuit—in a ramp-step-ramp paradigm. The target position was either shifted in the direction of the horizontally moving target (forward step), against it (backward step) or orthogonally to it (vertical step). Results indicate adaptation of catch-up saccade amplitude to back and forward steps. With vertical steps, saccades became oblique, by an inflexion of the early or late saccade trajectory. With a similar time course, post-saccadic pursuit velocity was increased in the step direction, adding further evidence that under some conditions pursuit and saccades can act synergistically to reduce position errors.     

Vestibular catch-up saccades in labyrinthine deficiency

During rapid head rotations, saccades ipsiversive with compensatory vestibulo-ocular reflex (VOR) slow phases may augment the deficient VOR and assist gaze stabilization in space. The present experiments compared these vestibular catch-up saccades (VCUSs) with visually and memory-guided saccades. To characterize VCUSs and their relationship to deficiency of the initial VOR, we delivered random, whole-body transients of 1000 and 2800 degrees/s2 peak yaw acceleration around four different eccentric vertical axes in eight unilaterally and one bilaterally vestibulopathic subjects, as well as nine age-matched normal subjects. Eye and head movements were sampled at 1200 Hz using magnetic search coils. Subjects fixed targets at either 500 or 15 cm distance immediately before unpredictable onset of rotation in darkness. Under all testing conditions, normal subjects exhibited only compensatory vestibular slow phases and occasional anticompensatory quick phases. This behavior was also typical of unilaterally vestibulopathic subjects rotated contralesionally. When rotated ipsilesionally, however, vestibulopathic subjects had deficient slow-phase VOR gain with prolonged latency, and six of the nine exhibited saccadic movements in the compensatory direction (VCUSs). Higher head accelerations preferentially evoked VCUSs, but there were no preferred combinations of target distances and eccentric rotation axes. Peak velocities and durations of VCUSs increased with saccade amplitude. The latency distribution for VCUSs peaked around 70 ms, substantially shorter than reported for either visually guided express saccades or vestibular memory contingent saccades. The latency of each VCUS was highly correlated with the gaze error prior to that VCUS. The amplitude of VCUSs was calibrated to gaze position error, such that VCUSs reduced gaze error by an average of 37%. Thus when VOR slow-phase responses cannot compensate fully for head rotation, vestibular gaze position error can nevertheless calibrate the programming of VCUSs to augment the deficient VOR, much like catch-up saccades substitute for deficient visual pursuit.     

Neural activation associated with corrective saccades during tasks with fixation,pursuit and saccades

Corrective saccades are small eye movements that redirect gaze whenever the actual eye position differs from the desired eye position. In contrast to various forms of saccades including pro-saccades, recentering-saccades or memory guided saccades, corrective saccades have been widely neglected so far. The fMRI correlates of corrective saccades were studied that spontaneously occurred during fixation, pursuit or saccadic tasks. Eyetracking was performed during the fMRI data acquisition with a fiber-optic device. Using a combined block and event-related design, we isolated the cortical activations associated with visually guided fixation, pursuit or saccadic tasks and compared these to the activation associated with the occurrence of corrective saccades. Neuronal activations in anterior inferior cingulate, bilateral middle and inferior frontal gyri, bilateral insula and cerebellum are most likely specifically associated with corrective saccades. Additionally, overlapping activations with the established pro-saccade and, to a lesser extent, pursuit network were present. The presented results imply that corrective saccades represent a potential systematic confound in eye-movement studies, in particular because the frequency of spontaneously occurring corrective saccades significantly differed between fixation, pursuit and pro-saccades.     

Gravity modulates Listing's plane orientation during both pursuit and saccades

Previous studies have shown that the spatial organization of all eye orientations during visually guided saccadic eye movements (Listing's plane) varies systematically as a function of static and dynamic head orientation in space. Here we tested if a similar organization also applies to the spatial orientation of eye positions during smooth pursuit eye movements. Specifically, we characterized the three-dimensional distribution of eye positions during horizontal and vertical pursuit (0.1 Hz, +/-15 degrees and 0.5 Hz, +/-8 degrees) at different eccentricities and elevations while rhesus monkeys were sitting upright or being statically tilted in different roll and pitch positions. We found that the spatial organization of eye positions during smooth pursuit depends on static orientation in space, similarly as during visually guided saccades and fixations. In support of recent modeling studies, these results are consistent with a role of gravity on defining the parameters of Listing's law.     

Accuracies of saccades to moving targets during pursuit initiation and maintenance

The overall goals of the studies presented here were to compare (1) the accuracies of saccades to moving targets with either a novel or a known target motion, and (2) the relationships between the measures of target motion and saccadic amplitude during pursuit initiation and maintenance. Since resampling of position error just prior to saccade initiation can confound the interpretation of results, the target ramp was masked during the planning and execution of the saccade. The results suggest that saccades to moving targets were significantly more accurate if the target motion was known from the early part of the trial (e.g., during pursuit maintenance) than in the case of novel target motion (e.g., during pursuit initiation); both these types of saccades were more accuate than those when target motion information was not available. Using target velocity in space as a rough estimate of the magnitude of the extra-retinal signal during pursuit maintenance, the saccadic amplitude was significantly associated with the extra-retinal target motion information after accounting for the position error. In most subjects, this association was stronger than the one between retinal slip velocity and saccadic amplitude during pursuit initiation. The results were similar even when the smooth eye motion prior to the saccade was controlled. These results suggest that different sources of target motion information (retinal image velocity vs internal representation of previous target motion in space) are used in planning saccades during different stages of pursuit. The association between retinal slip velocity and saccadic amplitude is weak during initiation, thus explaining poor saccadic accuracy during this stage of pursuit.     

Activity of mesencephalic vertical burst neurons during saccades and smooth pursuit

The activity of vertical burst neurons (BNs) was recorded in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF-BNs) and in the interstitial nucleus of Cajal (NIC-BNs) in head-restrained cats while performing saccades or smooth pursuit. BNs emitted a high-frequency burst of action potentials before and during vertical saccades. On average, these bursts led saccade onset by 14 +/- 4 ms (mean +/- SD, n = 23), and this value was in the range of latencies ( approximately 5-15 ms) of medium-lead burst neurons (MLBNs). All NIC-BNs (n = 15) had a downward preferred direction, whereas riMLF-BNs showed either a downward (n = 3) or an upward (n = 5) preferred direction. We found significant correlations between saccade and burst parameters in all BNs: vertical amplitude was correlated with the number of spikes, maximum vertical velocity with maximum of the spike density, and saccade duration with burst duration. A correlation was also found between instantaneous vertical velocity and neuronal activity during saccades. During fixation, all riMLF-BNs and approximately 50% of NIC-BNs (7/15) were silent. Among NIC-BNs active during fixation (8/15), only two cells had an activity correlated with the eye position in the orbit. During smooth pursuit, most riMLF-BNs were silent (7/8), but all NIC-BNs showed an activity that was significantly correlated with the eye velocity. This activity was unaltered during temporary disappearance of the visual target, demonstrating that it was not visual in origin. For a given neuron, its ON-direction during smooth pursuit and saccades remained identical. The activity of NIC-BNs during both saccades and smooth pursuit can be described by a nonlinear exponential function using the velocity of the eye as independent variable. We suggest that riMLF-BNs, which were not active during smooth pursuit, are vertical MLBNs responsible for the generation of vertical saccades. Because NIC-BNs discharged during both saccades and pursuit, they cannot be regarded as MLBNs as usually defined. NIC-BNs could, however, be the site of convergence of both the saccadic and smooth pursuit signals at the premotoneuronal level. Alternatively, NIC-BNs could participate in the integration of eye velocity to eye position signals and represent input neurons to a common integrator.     

Processing of retinal and extraretinal signals for memory-guided saccades during smooth pursuit

It is an essential feature for the visual system to keep track of self-motion to maintain space constancy. Therefore the saccadic system uses extraretinal information about previous saccades to update the internal representation of memorized targets, an ability that has been identified in behavioral and electrophysiological studies. However, a smooth eye movement induced in the latency period of a memory-guided saccade yielded contradictory results. Indeed some studies described spatially accurate saccades, whereas others reported retinal coding of saccades. Today, it is still unclear how the saccadic system keeps track of smooth eye movements in the absence of vision. Here, we developed an original two-dimensional behavioral paradigm to further investigate how smooth eye displacements could be compensated to ensure space constancy. Human subjects were required to pursue a moving target and to orient their eyes toward the memorized position of a briefly presented second target (flash) once it appeared. The analysis of the first orientation saccade revealed a bimodal latency distribution related to two different saccade programming strategies. Short-latency (<175 ms) saccades were coded using the only available retinal information, i.e., position error. In addition to position error, longer-latency (>175 ms) saccades used extraretinal information about the smooth eye displacement during the latency period to program spatially more accurate saccades. Sensory parameters at the moment of the flash (retinal position error and eye velocity) influenced the choice between both strategies. We hypothesize that this tradeoff between speed and accuracy of the saccadic response reveals the presence of two coupled neural pathways for saccadic programming. A fast striatal-collicular pathway might only use retinal information about the flash location to program the first saccade. The slower pathway could involve the posterior parietal cortex to update the internal representation of the flash once extraretinal smooth eye displacement information becomes available to the system.     

Evidence for synergy between saccades and smooth pursuit during transient target disappearance

Visual tracking of moving objects requires prediction to compensate for visual delays and minimize mismatches between eye and target position and velocity. In everyday life, objects often disappear behind an occluder, and prediction is required to align eye and target at reappearance. Earlier studies investigating eye motion during target blanking showed that eye velocity first decayed after disappearance but was sustained or often recovered in a predictive way. Furthermore, saccades were directed toward the unseen target trajectory and therefore appeared to correct for position errors resulting from eye velocity decay. To investigate the synergy between smooth and saccadic eye movements, this study used a target blanking paradigm where both position and velocity of the target at reappearance could vary independently but were presented repeatedly to facilitate prediction. We found that eye velocity at target reappearance was only influenced by expected target velocity, whereas saccades responded to the expected change of target position at reappearance. Moreover, subjects exhibited on-line adaptation, on a trial-by-trial basis, between smooth and saccadic components; i.e., saccades compensated for variability of smooth eye displacement during the blanking period such that gaze at target reappearance was independent of the level of smooth eye displacement. We suggest these results indicate that information arising from efference copies of saccadic and smooth pursuit systems are combined with the goal of adjusting eye position at target reappearance. Based on prior experimental evidence, we hypothesize that this spatial remapping is carried out through interactions between a number of identified neurophysiological structures.     

Amplitude criteria and anticipatory saccades during smooth pursuit eye movements in schizophrenia.

Increased frequency of anticipatory saccades during smooth pursuit eye movements is a potential marker of genetic risk for schizophrenia even in the absence of clinical symptomology. The operational definition of anticipatory saccades has often included an amplitude criterion; however, these amplitude criteria have often differed across studies. This study reports on the effect of varying amplitude criteria on the effect size in a comparison of 29 schizophrenic adults and 29 normal subjects during a 16.7 degrees/s constant velocity task. The inclusion of small amplitude anticipatory saccades, with amplitudes of 1-4 degrees, consistently increased effect size (largest effect size = 1.61). The inclusion of large anticipatory saccades, with amplitudes of 4 degrees or greater, had an inconsistent impact on effect size. The separation of anticipatory saccades into leading saccades (anticipatory saccades with amplitude 1-4 degrees) and large anticipatory saccades (amplitude > 4 degrees) deserves further exploration.     

Vestibular catch-up saccades augmenting the human transient heave linear vestibulo-ocular reflex

Vestibular catch-up saccades (VCUS) cued by the semicircular canals can supplement the deficient angular vestibulo-ocular reflex during transient rotations to stabilize gaze in people with unilateral vestibular deafferentation (Tian et al. 2000). However, a possible analogous role for VCUS to augment a deficient linear vestibulo-ocular reflex (LVOR) has not been carefully studied. We investigated VCUS in 9 younger, 8 older normal, and 12 vestibulopathic subjects undergoing directionally random heave (interaural) translations at 0.5 g peak acceleration. Eye and head movements were sampled at 1,200 Hz using magnetic search coils and a cranial accelerometer. Subjects fixated visible targets 200, 50, or 15 cm distant immediately before unpredictable onset of translation in either darkness or light. Evoked slow phase eye rotations opposite to the direction of head translation accounted for only 19–70% of ideal eye position, being less for nearer targets, and VCUS commonly occurred to augment the deficiency. Eye position error relative to geometric ideal was highly correlated to VCUS amplitude (P<0.001). This error was systematically corrected by VCUS whose latency decreased, and speed and frequency increased, with decreasing target distance. When targets remained visible, nearly all subjects made VCUS for nearer targets. In darkness, VCUS for the nearest target were significantly less common for older normal and vestibulopathic subjects than in younger normal subjects (P<0.001). In older and vestibulopathic subjects, VCUS latency was significantly prolonged. We conclude that otolith-mediated VCUS calibrated to target distance assist LVOR slow phases, but the ability to generate VCUS in darkness is impaired in older normal and vestibulopathic subjects. In the presence of visual information, VCUS can be generated in older and vestibulopathic subjects, albeit at prolonged latency perhaps indicating visual augmentation of deficient vestibular input.     

Validity of Listing's law during fixations, saccades, smooth pursuit eye movements, and blinks

In its original formulation, Listing's law referred only to eye positions during steady fixation. In recent years, however, several studies have suggested that Listing's law can be extended to the movements of the eyes, including during saccades and smooth pursuit. A major problem in deciding whether or not Listing's law is obeyed during eye movements is the influence of any spontaneous fluctuations in torsional eye position. To try to settle this question, the three-dimensional position of the eyes (around the three axes: horizontal, vertical, and torsional) was recorded with dual search coils in five normal subjects during fixations, 20° saccades, blinks, and 20° pursuit movements with a 20°/s stimulus velocity. Eye movements across a wide range of horizontal positions were measured at different elevations of gaze during 11 min. Variability (as reflected in the standard deviation of torsional eye position) was used as a measure of the validity of Listing's law. After linear detrending single trials, each lasting 21.5 s, to remove the effects of drift over minutes, the reduction in the standard deviation of torsional position in tertiary eye positions was 54% assuming a planar and 58% assuming a second-order curved Listing's surface. We attributed this long-term fluctuation of the torsional signal to slippage of the coil on the eye. The remaining variability was mainly due to short-term fluctuation of eye torsion over seconds. The impact of hysteresis, associated with consecutive centrifugal-centripetal horizontal movements, on the variability of torsional eye position appeared negligible. Peak increases in the standard deviation from the fixation baseline after fitting individual Listing's planes for each trial were 348% during blinks, 141% during saccades, and 72% during pursuit movements (median value of five subjects). In conclusion, Listing's law during blinks, saccades, and pursuit is less valid than during fixations, which raises doubts about the existence of an internal Listing's law operator for eye movements. Possibly, central eye velocity commands do not comply with Listing's law.     

Phoria adaptation after sustained symmetrical convergence: influence of saccades

We recorded divergence eye movements after short (4 s) and long (36 s) periods of sustained symmetrical convergence (30°) in nine normal human subjects using the search coil technique. Following the long period of convergence, alignment after the initial 1,250 ms of divergence was more converged than after the short period of convergence, showing short-term “phoria adaptation”. The first 1,000 ms of divergence, however, could be slower, faster or relatively unchanged, depending upon the subject. A change in the timing and/or amplitude of associated saccades (which accelerate ongoing vergence) between the long and short stimuli accounted for much of the difference in the rate of divergence. The differences in saccade pattern during early divergence following the long and short periods of convergence may reflect changes in attentional focus (to near or to far).     

Torsion during saccades between tertiary positions

We systematically studied the effect of saccade direction and saccade starting position on the velocity profile of the saccade. Saccades were made between targets placed at optical infinity by dichoptic presentation. This arrangement was chosen to evoke conjugate eye movements. Eye movements were recorded binocularly, including torsion. Horizontal and vertical movements of the eyes are strongly correlated (r? 0.95) during the saccade, torsional movements are much less so (r█ 0.67). Listing’s law would predict that the three-dimensional versional velocity of the eye would be located in a plane that is tilted out of Listing’s plane by an amount that depends on the saccade’s starting position (half angle rule). Taking together all saccades that started from the same initial position a plane could be fitted through the velocity vectors. However, this plane was tilted less relative to Listing’s plane than predicted by the half angle rule. The deviation was especially large for the yaw component of the tilt (56% of predicted). For the pitch component the prediction was better (81% of predicted). In addition, we find that the torsional velocity during the fast “intrasaccadic” part of the motion can be unequal in the two eyes. The implications for three-dimensional models of saccadic control are discussed.     

Posterior vermal Purkinje cells in macaques responding during saccades, smooth pursuit, chair rotation and/or optokinetic stimulation.

Anatomical locations of the Purkinje cells (P cells), showing modulations in activity during either saccadic or smooth-pursuit eye movements, during primate chair rotation, or in response to optokinetic stimulation, were studied in the posterior vermes of monkeys trained to move their eyes with a visual target. The majority (68.3%) of the responsive P cells were saccade-related units. They were located exclusively in vermal lobules VIc and VII: the oculomotor vermis. Most P cells sensitive to chair rotation were located in vermal lobules VIa,b and VIII (91.2%), designated as the paraoculomotor vermis. The P cells which modulated activity during smooth-pursuit eye movements, associated with eye position, or during optokinetic stimulation were found in both the oculomotor and paraoculomotor vermis. There were 25 P cells which modulated their activity during smooth pursuit in the oculomotor vermis. Among them, only three responded also to optokinetic stimulation but none was sensitive to chair-rotation stimulation. These findings suggest that the control of saccadic eye movements is the primary function of the oculomotor vermis.     

Cortical potentials during the gap prior to express saccades and fast regular saccades

When a temporal gap is introduced between the offset of the central fixation point and the appearance of a new target, saccadic reaction time is reduced (gap effect) and a special population of extremely fast saccades occurs (express saccades). It has been hypothesized that the gap triggers a readiness signal, which is responsible for the reduced saccadic reaction times. Here we recorded event-related potentials during the gap to in vestigate the central processes associated with the gener ation of fast regular saccades and express saccades. Prior to the execution of fast regular saccades, subjects pro duced a slow negative shift, with a maximum at frontal and central channels that started 40 ms after fixation offset. This widespread negativity is similar to a readiness potential. Anticipatory saccades were preceded by an increased frontal and parietal negativity. Prior to express saccades, a frontal negativity was observed, which started 135 ms after the disappearance of the fixation point. It is assumed that the frontal negativity prior to express saccades corresponds to the fixation-disengagement dis charge described in the frontal eye field of monkeys. Therefore, we hypothesize that fast regular saccades are the result of an increased readiness signal, while express saccades are the result of specific preparatory processes.     

Intrasaccadic target steps during the deceleration of primary saccades affect the latency of corrective saccades

This study investigates how visually guided saccades and subsequent corrective saccades are affected by a secondary target step occurring at different times during the primary saccade. Eye movements of human subjects were measured by means of a differential infrared light reflection technique while the subjects performed visually guided saccades to a laser spot in darkness. The target was stepped backward or onward during the targeting saccade. While the intrasaccadic target step did not influence gain, peak velocity or skewness of the primary saccade, it had a significant effect on the subsequent corrective saccade when the secondary target step occurred during the deceleration phase of the primary saccade: the latency of the corrective saccade was significantly increased compared with the one performed under the single-step control condition. This increase also occurred when single target steps were presented randomly intermixed with backward and onward double target steps and even between selected sub-samples of saccades with identical postsaccadic visual error. If the target step occurred early during the primary saccade, the latency of the corrective saccade was not changed. This indicates that visual information sampled during the deceleration phase of a saccade can lead to a cancellation of the normal trigger mode of corrective saccades. Received: 9 April 1999 / Accepted: 23 June 1999     

Admixture analysis of smooth pursuit eye movements in probands with schizophrenia and their relatives suggests gain and leading saccades are potential endophenotypes

Abnormalities during a smooth pursuit eye movement task (SPEM) are common in schizophrenic patients and their relatives. This study assessed various components of SPEM performance in first-degree unaffected relatives of schizophrenic patients. One hundred individuals with schizophrenia, 137 unaffected first-degree relatives, and 69 normal controls completed a 16.7 degrees/s SPEM task. Smooth pursuit gain, catch-up saccades (CUS), large anticipatory saccades, and leading saccades (LS) were identified. Groups were compared with parametric and admixture analyses. Schizophrenic patients performed more poorly than unaffected relatives and normals on gain, CUS, and LS. Unaffected relatives were more frequently impaired than normals only on gain and LS. Relatives of childhood-onset and adult-onset probands had similar impairments. Gain and frequency of leading saccades may be genetic endophenotypes in childhood-onset and adult-onset schizophrenia.     

Frequency analysis of the surface electromyogram during sustained isometric contractions

Summary Four male and four female volunteers served as subjects in these experiments to assess the frequency components of the surface EMG during and following brief (3 s) and sustained isometric contractions of the handgrip muscles. Two types of fatiguing contractions were performed. Contractions were either maintained to fatigue at a constant tension of up to 100% of their strength or were maintained as a sustained maximal effort in the unfatigued or previously fatigued muscle. The frequency components of the surface EMG were assessed by calculating the power spectra of 1.5 s samples of the EMG from a fundamental frequency of 4 Hz through the first 128 harmonics by Fourier analysis; the centre frequencies of the resultant power spectra were then used as an index of the mean frequency of the EMG. The results of these experiments showed that the centre frequency was independent of the tension exerted by the muscle during brief isometric contractions but decreased linearly with time throughout the duration of fatiguing isometric contractions at tensions between 25 and 100% MVC. During sustained maximal effort, the frequency initially decreased linearly with time. However, once the target tension could no longer be maintained, the centre frequency remained constant throughout the remainder of the contraction. The frequency was found to recover within 1 min following exercise at all tensions examined.     

Fourier analysis of saccades in monkeys and humans

1. By recording eye movements with the search coil technique and subjecting them to an accurate infinite Fourier transform algorithm, we describe the Fourier spectra of human and monkey saccades. In both species we find heretofore undescribed features consisting of a regular pattern of local minima in the power plot, which cannot be attributed to noise. The frequency of these minima is well correlated with saccade duration. 2. Computer simulation shows that if the pulse component of the saccade is considered to be rectangular, then the first of these minima (called M1) occurs at a frequency that is the reciprocal of the duration of the pulse. 3. Comparing the position of this component during individual monkey saccades with electrophysiological recordings of motoneurons during the same saccades leads to the conclusion that these minima are related to the burst components in ocular motoneuron discharges. Specifically, the reciprocals of the frequencies of these minima are correlated with the duration of the burst component in the motoneuron discharge. 4. In the Fourier spectra of human saccades, the relationship of the frequency of M1 to saccadic duration is a function similar to that in the monkey. This adds to the evidence that the human saccade also is driven by a pulse-step signal. 5. In both monkeys and humans, T1, the reciprocal of the frequency of M1, is shorter than both the saccade duration and the burst duration of individual motoneurons, even though neurophysiological studies in monkeys generally report the saccadic burst duration to be equal to the saccade duration. This probably arises because the saccadic pulse is not rectangular, with the extremes contributing very little energy to the Fourier spectrum. By further computer modeling we show these shape effects explicitly: as the rise- and falltime increase, making the pulse less rectangular, T1 becomes shorter; in addition, as the asymmetry of rise and fall increases, the depth of the minima is reduced. We conclude that T1 measures the "effective pulse" duration of the motoneuron. 6. There is a difference in the relationship of effective pulse duration to the saccade duration between short and long saccades. For saccades shorter than approximately 40 ms in the human and 50 ms in the monkey, the pulse width as measured by this technique varies little with saccade duration. For longer saccades, effective pulse width increases linearly with duration. We agree with others that for short saccades the pulse is both height- and width-modulated; but for longer saccades, height modulation saturates and only width modulation remains.(ABSTRACT TRUNCATED AT 400 WORDS)