Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys

Step-ramp target motion evokes a characteristic sequence of presaccadic smooth eye movement in the direction of the target ramp, catch-up targets to bring eye position close to the position of the moving target, and postsaccadic eye velocities that nearly match target velocity. I have analyzed this sequence of eye movements in monkeys to reveal a strong postsaccadic enhancement of pursuit eye velocity and to document the conditions that lead to that enhancement. Smooth eye velocity was measured in the last 10 ms before and the first 10 ms after the first saccade evoked by step-ramp target motion. Plots of eye velocity as a function of time after the onset of the target ramp revealed that eye velocity at a given time was much higher if measured after versus before the saccade. Postsaccadic enhancement of pursuit was recorded consistently when the target stepped 3 degrees eccentric on the horizontal axis and moved upward, downward, or away from the position of fixation. To determine whether postsaccadic enhancement of pursuit was invoked by smear of the visual scene during a saccade, I recorded the effect of simulated saccades on the presaccadic eye velocity for step-ramp target motion. The 3 degrees simulated saccade, which consisted of motion of a textured background at 150 degrees/s for 20 ms, failed to cause any enhancement of presaccadic eye velocity. By using a strategically selected set of oblique target steps with horizontal ramp target motion, I found clear enhancement for saccades in all directions, even those that were orthogonal to target motion. When the size of the target step was varied by up to 15 degrees along the horizontal meridian, postsaccadic eye velocity did not depend strongly either on the initial target position or on whether the target moved toward or away from the position of fixation. In contrast, earlier studies and data in this paper show that presaccadic eye velocity is much stronger when the target is close to the center of the visual field and when the target moves toward versus away from the position of fixation. I suggest that postsaccadic enhancement of pursuit reflects activation, by saccades, of a switch that regulates the strength of transmission through the visual-motor pathways for pursuit. Targets can cause strong visual motion signals but still evoke low presaccadic eye velocities if they are ineffective at activating the pursuit system.     

Understanding the function of visual short-term memory: Transsaccadic memory, object correspondence, and gaze correction.

Visual short-term memory (VSTM) has received intensive study over the past decade, with research focused on VSTM capacity and representational format. Yet, the function of VSTM in human cognition is not well understood. Here, the authors demonstrate that VSTM plays an important role in the control of saccadic eye movements. Intelligent human behavior depends on directing the eyes to goal-relevant objects in the world, yet saccades are very often inaccurate and require correction. The authors hypothesized that VSTM is used to remember the features of the current saccade target so that it can be rapidly reacquired after an errant saccade, a task faced by the visual system thousands of times each day. In 4 experiments, memory-based gaze correction was accurate, fast, automatic, and largely unconscious. In addition, a concurrent VSTM load interfered with memory-based gaze correction, but a verbal short-term memory load did not. These findings demonstrate that VSTM plays a direct role in a fundamentally important aspect of visually guided behavior, and they suggest the existence of previously unknown links between VSTM representations and the occulomotor system. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Initiation of disjunctive smooth pursuit in monkeys: evidence that Hering's law of equal innervation is not obeyed by the smooth pursuit system

Monkeys generated disjunctive smooth pursuit eye movements when they tracked visual targets that moved toward or away from them. Eye acceleration was computed during the initial 100 msec of pursuit (the open-loop interval) for various target trajectories. The initial acceleration of either eye was a function of the target's motion with respect to that eye, regardless of whether or not the pursuit was conjugate or disjunctive, or performed with one eye occluded. Eye movements produced by fusional vergence could be separated temporally from eye movements produced by smooth pursuit using step-ramp paradigms. The separation of the two responses demonstrates that the fusional vergence system operates in parallel with the smooth pursuit system, presumably to minimize disparity, but not to generate disjunctive components of smooth pursuit eye movements.     

What Kind of Memory Supports Visual Marking?

In visual search tasks, if a set of items is presented for 1 s before another set of new items (containing the target) is added, search can be restricted to the new set. The process that eliminates old items from search is visual marking. This study investigates the kind of memory that distinguishes the old items from the new items during search. Using an accuracy paradigm in which perfect marking results in 100% accuracy and lack of marking results in near chance performance, the authors show that search can be restricted to new items not by visual short-term memory (VSTM) of old locations but by a limited capacity and slow-decaying VSTM of new locations and a high capacity and fast-decaying memory for asynchrony. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The effect of items in working memory on the deployment of attention and the eyes during visual search.

Paying attention to an object facilitates its storage in working memory. The authors investigate whether the opposite is also true: whether items in working memory influence the deployment of attention. Participants performed a search for a prespecified target while they held another item in working memory. In some trials this memory item was present in the search display as a distractor. Such a distractor has no effect on search time if the search target is in the display. In that case, the item in working memory is unlikely to be selected as a target for an eye movement, and if the eyes do land on it, fixation duration is short. In the absence of the target, however, there is a small but significant effect of the memory item on search time. The authors conclude that the target for visual search has a special status in working memory that allows it to guide attention. Guidance of attention by other items in working memory is much weaker and can be observed only if the search target is not present in the display. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Bilateral eye movements enhance the retrieval of episodic memories.

Two experiments examining effects of eye movements on episodic memory retrieval are reported. Thirty seconds of horizontal saccadic eye movements (but not smooth pursuit or vertical eye movements) preceding testing resulted in selective enhancement of episodic memory retrieval for laboratory (Experiment 1) and everyday (Experiment 2) events. Eye movements had no effects on implicit memory. Eye movements were also associated with more conservative response biases relative to a no eye movement condition. Episodic memory improvement induced by bilateral eye movements is hypothesized to reflect enhanced interhemispheric interaction, which is associated with superior episodic memory (S. D. Christman & R. E. Propper. 2001). Implications for neuropsychological mechanisms underlying eye movement desensitization and reprocessing (F. Shapiro, 1989, 2001), a therapeutic technique for posttraumatic stress disorder, are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Organization of visual short-term memory.

The authors examined the organization of visual short-term memory (VSTM). Using a change-detection task, they reported that VSTM stores relational information between individual items. This relational processing is mediated by the organization of items into spatial configurations. The spatial configuration of visual objects is important for VSTM of spatial locations, colors, and shapes. When color VSTM is compared with location VSTM, spatial configuration plays an integral role because configuration is important for color VSTM, whereas color is not important for location VSTM. The authors also examined the role of attention and found that the formation of configuration is modulated by both top-down and bottom-up attentional factors. In summary, the authors proposed that VSTM stores the relational information of individual visual items on the basis of global spatial configuration. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Retinal masking during pursuit eye movements: Implications for spatiotopic visual persistence.

White (1976) reported that presentation of a masking stimulus during a pursuit eye movement interfered with the perception of a target stimulus that shared the same spatial, rather than retinal, coordinates as the mask. This finding has been interpreted as evidence for the existence of spatiotopic visual persistence. We doubted White's results because they implied a high degree of position constancy during pursuit eye movements, contrary to previous research, and because White did not monitor Ss' eye position during pursuit; if White's Ss did not make continuous pursuit eye movements, it might appear that masking was spatial when in fact it was retinal. We attempted to replicate White's results and found that when eye position was monitored to ensure that subjects made continuous pursuit movements, masking was retinal rather than spatial. Ss' phenomenal impressions also indicated that retinal, rather than spatial, factors underlay performance in this task. The implications of these and other results regarding the existence of spatiotopic visual persistence are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The effect of the gap paradigm on the latency of human smooth pursuit of eye movement

When a temporal gap is introduced between the extinction of a central fixation target and the illumination of an eccentric target (the gap paradigm), normal human subjects initiate saccadic eye movements towards the eccentric target at lower latency than when there is no gap. The aim of this study was to examine the latency of human smooth pursuit eye movements using a modified gap paradigm. Smooth pursuit latency was reduced in gap tasks, and the magnitude of reduction was related to the duration of the gap. The distribution of smooth pursuit latencies was also altered. It thus appears that human smooth pursuit latency is modulated in a similar manner to saccade latency in gap tasks.     

Properties of memory-guided saccades toward targets flashed during smooth pursuit in human subjects

PURPOSE: This study in human subjects investigated whether or not the saccade system can monitor smooth changes of the eye position in total darkness. METHODS: The authors studied the properties of memory-guided saccades toward targets flashed during pursuit eye movements (target velocities of 15 degrees/s, 30 degrees/s, and 45 degrees/s) in four normal human subjects. Subjects were instructed to execute memory-guided saccades toward the position of the flashed target in total darkness when the pursuit target was extinguished. RESULTS: The vector of the saccade was more highly correlated with the vector of "spatial error" (the vector from the position of the eye at the time of the saccade to the position of the flashed target in space) than with the vector of "retinal error" (the vector from the position of the eye at the time of the presentation of the flashed target to the position of the flashed target). The amplitude and direction errors of memory-guided saccades were correlated with the amplitude of the retinal error but not with amplitude of eye deviation after the presentation of the flashed target. Pursuit velocity did not affect the error of the saccade. CONCLUSIONS: These findings suggest that the saccade system can monitor smooth changes of the eye position in total darkness, regardless of the velocity of pursuit, and that the accuracy of memory-guided saccades is dependent only on the amplitude of the retinal error.     

Disruption of the Saccharomyces cerevisiae YAP3 gene reduces the proteolytic degradation of secreted recombinant human albumin

In real-life situations, such as during locomotion, or while driving a vehicle, it is necessary to maintain visual fixation and tracking in the presence of the visual flow of the surroundings, which represents a potentially adequate stimulus for the elicitation of optokinetic nystagmus. The present study is concerned with the influence of vestibular disorders, whether pathological or experimentally induced, on those cortically controlled fixation mechanisms, predominantly in the smooth pursuit system, which are involved in suppressing optokinetic information. The study examines the possibility of obtaining an objective measure to assist in counselling patients with unilateral vestibular loss on their vehicle driving ability. To this end, the influence of optokinetic and vestibular stimulation on the execution of smooth pursuit target tracking was measured by recording eye movements during a combination of standard pursuit tasks (0.25, 0.5 and 1 Hz sinusoidal) against standard optokinetic striped backgrounds (0, 30 and 60 degrees/sec). The influence of vestibular imbalance, induced in healthy subjects (n = 35) by unilateral caloric irrigation, and caused by unilateral vestibular loss (in five patients), was also examined under these conditions. During induced vestibular imbalance in normal subjects, and to a greater extent in the tested patients, significant deficits in smooth pursuit gain and increases in saccade frequency were observed during target pursuit against an optokinetic background. Moreover, the findings indicate that the most sensitive parameter for the influence of vestibular optokinetic stimuli on smooth pursuit is frequency of saccades, rather than the gain factor. The tests described here are appropriate for clinical and medico-legal assessment of the influence of vestibular disorder on vehicle driving.     

Visual short-term memory benefit for objects on different 3-D surfaces.

Visual short-term memory (VSTM) plays an important role in visual cognition. Although objects are located on different 3-dimensional (3-D) surfaces in the real world, how VSTM capacity may be influenced by the presence of multiple 3-D surfaces has never been examined. By manipulating binocular disparities of visual displays, the authors found that more colored objects could be held in VSTM when they were placed on 2 rather than on 1 planar 3-D surfaces. This between-surface benefit in VSTM was present only when binding of objects' colors to their 3-D locations was required (i.e., when observers needed to remember which color appeared where). When binding was not required, no between-surface benefit in VSTM was observed. This benefit in VSTM could not be attributed to the number of spatial locations attended within a given surface. It was not due to a general perceptual grouping effect either, because grouping by motion and grouping by different regions of the same surface did not yield the same benefit. This increment in capacity indicates that VSTM benefits from the placement of objects in a 3-D scene. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A note on formal learning theory

Previous investigations have challenged the generality of the claim that perceived motion in an effective stimulus for smooth pursuit eye movements. The experiments extend the scope of these investigations. Three experiments test the hypothesis that perceived motion can serve as the stimulus for pursuit when the eye movement does not generate constraining retinal error information. Observers viewed retinally stabilized displays that elicited the perception that a stationary target was moving or that a moving target was moving faster than it was actually moving. The results failed to confirm the hypothesis. Relevant literature is reviewed. We conclude that perceived movement can act as a stimulus for pursuit only when the "perceptual target" has no retinal counterpart.     

Smooth pursuit eye movement and schizotypy in the community.

Deficits in smooth pursuit eye movements are well documented in schizophrenia and schizotypic psychopathology. The status of eye tracking dysfunction (ETD) as an endophenotype for schizophrenia liability is relatively robust. However, the relation of ETD to schizophrenia-related deviance in the general population has not been confirmed. This study examined smooth pursuit eye tracking and schizotypal personality features in the general population. Smooth pursuit eye movement and schizotypal features were measured in 300 adult community subjects. The sample included both sexes, subjects with a wide age and educational range, and subjects with no prior history of psychosis. Primary outcome measures were peak gain (eye velocity/target velocity), catch-up saccade rate, and schizotypal feature scores. Total schizotypal features were significantly associated with decreased peak gain and were associated at the trend level with increased catch-up saccade rate. These associations were essentially unchanged after controlling for age, sex, and intellectual level effects. These data confirm a hypothesized association between schizotypal features and poorer eye tracking performance (principally, peak gain) in the general population as well as support the conceptualization of ETD as an endophenotype for schizophrenia liability. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The role of eye movements in subitizing and counting.

Previous work has suggested that eye movements may be necessary for accurate enumeration beyond the subitization range of about 4 items. This study determined the frequency of eye movements normally made during enumeration, their relationship to response times, and whether they are required for accurate performance. This was achieved by monitoring eye movements and comparing performance when observers were allowed to saccade and when they were not. The results showed that (a) there was a sharp increase in saccadic frequency beyond about 4 items (from = 0.2 saccades per item to about 1 per item), and (b) enumeration of fewer than 4 items remained rapid and accurate even when eye movements were prevented, whereas enumeration beyond this became less efficient and sometimes less accurate. The results are discussed in relation to the memory and processing requirements of enumeration tasks. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation

We studied the eye movements evoked by applying small amounts of current (2-50 microA) within the oculomotor vermis of two monkeys. We first compared the eye movements evoked by microstimulation applied either during maintained pursuit or during fixation. Smooth, pursuitlike changes in eye velocity caused by the microstimulation were directed toward the ipsilateral side and occurred at short latencies (10-20 ms). The amplitudes of these pursuitlike changes were larger during visually guided pursuit toward the contralateral side than during either fixation or visually guided pursuit toward the ipsilateral side. At these same sites, microstimulation also often produced abrupt, saccadelike changes in eye velocity. In contrast to the smooth changes in eye velocity, these saccadelike effects were more prevalent during fixation and during pursuit toward the ipsilateral side. The amplitude and type of evoked eye movements could also be manipulated at single sites by changing the frequency of microstimulation. Increasing the frequency of microstimulation produced increases in the amplitude of pursuitlike changes, but only up to a certain point. Beyond this point, the value of which depended on the site and whether the monkey was fixating or pursuing, further increases in stimulation frequency produced saccadelike changes of increasing amplitude. To quantify these effects, we introduced a novel method for classifying eye movements as pursuitlike or saccadelike. The results of this analysis showed that the eye movements evoked by microstimulation exhibit a distinct transition point between pursuit and saccadelike effects and that the amplitude of eye movement that corresponds to this transition point depends on the eye movement behavior of the monkey. These results are consistent with accumulating evidence that the oculomotor vermis and its associated deep cerebellar nucleus, the caudal fastigial, are involved in the control of both pursuit and saccadic eye movements. We suggest that the oculomotor vermis might accomplish this role by altering the amplitude of a motor error signal that is common to both saccades and pursuit.     

Distractor interference during smooth pursuit eye movements.

When 2 targets for pursuit eye movements move in different directions, the eye velocity follows the vector average (S. G. Lisberger & V. P. Ferrera, 1997). The present study investigates the mechanisms of target selection when observers are instructed to follow a predefined horizontal target and to ignore a moving distractor stimulus. Results show that at 140 ms after distractor onset, horizontal eye velocity is decreased by about 25%. Vertical eye velocity increases or decreases by 1°/s in the direction opposite from the distractor. This deviation varies in size with distractor direction, velocity, and contrast. The effect was present during the initiation and steady-state tracking phase of pursuit but only when the observer had prior information about target motion. Neither vector averaging nor winner-take-all models could predict the response to a moving to-be-ignored distractor during steady-state tracking of a predefined target. The contributions of perceptual mislocalization and spatial attention to the vertical deviation in pursuit are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Anticipatory saccades during smooth pursuit eye movements and familial transmission of schizophrenia

BACKGROUND: Smooth pursuit eye movement (SPEM) abnormalities are a putative marker of genetic risk for schizophrenia. Accurate SPEM performance requires the subject to activate neural systems responsible for smooth pursuit tracking, while simultaneously suppressing activity of neurons responsible for saccadic movements that would move the eye ahead of the target. This study examined whether specific aspects of SPEM dysfunction cosegregate with genetic risk in parents of schizophrenic probands. METHODS: Eighteen probands and their parents had SPEM recorded. Parents with an ancestral history of schizophrenia were hypothesized to be more likely than their spouses without such a history to carry a genetic risk for schizophrenia. RESULTS: Ten families had a single parent with a positive ancestral history for schizophrenia. The frequency of anticipatory saccades, which were mostly small, and the fraction of total eye movement that they represented were the only measures that differentiated the more likely genetic carrier parents in these families from their spouses and age-matched normals. CONCLUSIONS: Failure to suppress saccadic anticipation of target motion during smooth pursuit appears an aspect of SPEM dysfunction related to presumed genetic risk for schizophrenia.     

The role of perception in the mislocalization of the final position of a moving target.

The judged final position of a moving stimulus has been suggested to be shifted in the direction of motion because of mental extrapolation (representational momentum). However, a perceptual explanation is possible: The eyes overshoot the final position of the target, and because of a foveal bias, the judged position is shifted in the direction of motion. To test this hypothesis, the authors replicated previous studies, but instead of having participants indicate where the target vanished, the authors probed participants' perceptual focus by presenting probe stimuli close to the vanishing point. Identification of probes in the direction of target motion was more accurate immediately after target offset than it was with a delay. Another experiment demonstrated that judgments of the final position of a moving target are affected by whether the eyes maintain fixation or follow the target. The results are more consistent with a perceptual explanation than with a memory account. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The time course of plausibility effects on eye movements in reading: Evidence from noun-noun compounds.

Readers' eye movements were monitored as they read sentences containing noun-noun compounds that varied in frequency (e.g., elevator mechanic, mountain lion). The left constituent of the compound was either plausible or implausible as a head noun at the point at which it appeared, whereas the compound as a whole was always plausible. When the head noun analysis of the left constituent was implausible, reading times on this word were inflated, beginning with the first fixation. This finding is consistent with previous demonstrations of very rapid effects of plausibility on eye movements. Compound frequency did not modulate the plausibility effect, and all disruption was resolved by the time readers' eyes moved to the next word. These findings suggest (contra Kennison, 2005) that the parser initially analyzes a singular noun as a head instead of a modifier. In addition, the findings confirm that the very rapid effect of plausibility on eye movements is not due to strategic factors, because in the present experiment, unlike in previous demonstrations, this effect appeared in sentences that were globally plausible. (PsycINFO Database Record (c) 2010 APA, all rights reserved)