The frontal eye field provides the goal of saccadic eye movement

Summary Microstimulation of oculomotor regions in primate cortex normally evokes saccadic eye movements of stereotypic directions and amplitudes. The fixed-vector nature of the evoked movements is compatible with the creation of either an artificial retinal or motor error signal. However, when microstimulation is applied during an ongoing natural saccade, the starting eye position of the evoked movement differs from the eye position at stimulation onset (due to the latency of the evoked saccade). An analysis of the effect of this eye position discrepancy on the trajectory of the eventual evoked saccade can clarify the oculomotor role of the structure stimulated. The colliding saccade paradigm of microstimulation was used in the present study to investigate the type of signals conveyed by visual, visuomovement, and movement unit activities in the primate frontal eye field. Colliding saccades elicited from all sites were found to compensate for the portion of the initial movement occurring between stimulation and evoked movement onset, plus a portion of the initial movement occurring before stimulation. This finding suggests that activity in the frontal eye field encodes a retinotopic goal that is converted by a downstream structure into the vector of the eventual saccade. Offprint requests to: J. Schlag, Department of Anatomy and Cell Biology     

The dynamics of small saccadic eye movements

1. The mechanical characteristics of the system comprising the eyeball and its attachments have been determined, by applying rotational forces to the eyeball, and using an accelerometer on a contact lens to measure the resulting movement.

2. The angular acceleration-versus-time curves of small saccades have been recorded. Some of these saccades are made whilst the eye is being vibrated by external forces.

3. A mechanical model of the orbital system has been formulated. This is considered to bear a relationship to the structures in the orbit.

4. The model has been used to deduce the force pattern of the active component in the extraocular muscles during the execution of a saccade. It is concluded that a saccade is initiated by a rapid rise of tension. After a short time, the tension falls to a lower level, which is the new steady-state level. The present findings are therefore basically different from those of previous workers, in that we deduce a change in the force pattern during the course of the movement.

5. In the execution of saccades of various sizes, both the strength and duration of the brief heightened tension are found to vary. For a 4 degree saccade, the transient tension is approximately 36 g, lasting for approximately half of the duration of the saccade.

6. Characteristic features of saccades are interpreted in terms of variations in the duration of the transient excess tension.

7. Differences in the time course of horizontal and vertical saccades are attributed to differences in the elasticity of the muscles involved in the movements.

8. It is suggested that, in view of the similarity of the acceleration-versus-time wave forms, the muscular force pattern which is responsible for rapid head movements is of a similar type to that which has been deduced for saccades.

     

The characteristics and neuronal substrate of saccadic eye movement plasticity

Saccadic eye movements are shifts in the direction of gaze that rapidly and accurately aim the fovea at targets of interest. Saccades are so brief that visual feedback cannot guide them to their targets. Therefore, the saccadic motor command must be accurately specified in advance of the movement and continually modified to compensate for growth, injury, and aging, which otherwise would produce dysmetric saccades. When a persistent dysmetria occurs in subjects with muscle weakness or neural damage or is induced in normal primates by the surreptitious jumping of a target forward or backward as a saccade is made to acquire the target, saccadic amplitude changes to reduce the dysmetria. Adaptation of saccadic amplitude or direction occurs gradually and is retained in the dark, thus representing true motor plasticity. Saccadic adaptation is more rapid in humans than in monkeys, usually is incomplete in both species, and is slower and less robust for amplitude increases than decreases. Adaptation appears to be motor rather than sensory. In humans, adaptation of saccades that would seem to require more sensory-motor processing does not transfer to saccades that seem to require less, suggesting the existence of distributed adaptation loci. In monkeys, however, transfer from more simple to more complex saccades is robust, suggesting a common adaptation site. Neurophysiological data from both species indicate that the oculomotor cerebellum is crucial for saccadic adaptation. This review shows that the precise, voluntary behaviors known as saccadic eye movements provide an alternative to simple reflexes for the study of the neuronal basis of motor learning.     

Age-related performance of human subjects on saccadic eye movement tasks

We measured saccadic eye movements in 168 normal human subjects, ranging in age from 5 to 79 years, to determine age-related changes in saccadic task performance. Subjects were instructed to look either toward (pro-saccade task) or away from (anti-saccade task) an eccentric target under different conditions of fixation. We quantified the percentage of direction errors, the time to onset of the eye movement (saccadic reaction time: SRT), and the metrics and dynamics of the movement itself (amplitude, peak velocity, duration) for subjects in different age groups. Young children (5–8 years of age) had slow SRTs, great intra-subject variance in SRT, and the most direction errors in the anti-saccade task. Young adults (20–30 years of age) typically had the fastest SRTs and lowest intra-subject variance in SRT. Elderly subjects (60–79 years of age) had slower SRTs and longer duration saccades than other subject groups. These results demonstrate very strong age-related effects in subject performance, which may reflect different stages of normal development and degeneration in the nervous system. We attribute the dramatic improvement in performance in the anti-saccade task that occurs between the ages of 5–15 years to delayed maturation of the frontal lobes. Received: 27 October 1997 / Accepted: 27 February 1998     

Sensory biases produce alternation advantage found in sequential saccadic eye movement tasks

In two-choice reaction time tasks, participants respond faster when the correct decision switches across consecutive trials. This alternation advantage has been interpreted as the guessing strategies of participants. Because the participants expect that the correct decision will switch across consecutive trials, they respond faster when this expectation is confirmed and they respond more slowly when it is disconfirmed. In this study, we evaluated the veracity of this expectancy interpretation. After replicating a long-lasting alternation advantage in saccadic reaction times (Experiment 1), we show that reducing the participants ability to guess with a challenging mental rotation task does not change the alternation advantage, which suggests that expectancy is not responsible for the effect (Experiment 2). Next, we used prosaccade and antisaccade responses to dissociate between the sensory and motor contributions of the alternation advantage (Experiment 3) and we found that the alternation advantage originates from sensory processing. The implications of these findings are discussed with regard to guessing strategies, sensory processing, and how these findings may relate to inhibition of return.Jillian H. Fecteau and Crystal Au contributed equally to this work     

The assessment of position of stationary targets perceived during saccadic eye movement

Summary The experiment was performed to establish the accuracy with which visual targets perceived during saccadic eye movement are localised. Subjects were presented with the task of executing saccades of 30° plus amplitude, passing through primary gaze, about the time of peak velocity a 5 ms red flash was presented at some random position (up to 30° left or right of centre) on a horizontal visual display. Subjects were required to indicate the direction in which they thought the flash was localised by fixating in that direction. Observations were made under conditions of prolonged total darkness and in the presence of a contrasting background. Measurement was made of saccade velocity and eye displacement as an index of target positions. Eye displacement was linearly scaled with respect to true target direction. Targets were localised with an average error of 5°–6° although the variance was high. No systematic differences were found between conditions or subjects. Error was unrelated to saccade velocity. It is concluded that during saccadic eye movements the appreciation of target position is maintained with an acceptable degree of accuracy.     

Eye rotation induced dynamics of a Newtonian fluid within the vitreous cavity: the effect of the chamber shape

The dynamics of the vitreous body induced by eye rotations is studied experimentally. In particular, we consider the case in which the vitreous cavity is filled by a Newtonian fluid, either because the vitreous is liquefied or because it has been replaced, after vitrectomy, by a viscous fluid. We employ a rigid Perspex container which models, in a magnified scale, the vitreous cavity of the human eye. The shape of the cavity closely resembles that of the real vitreous chamber; in particular, the anterior part of the container is concave in order to model the presence of the eye lens. The container is filled with glycerol and is mounted on the shaft of a computer-controlled motor which rotates according to a periodic time law. PIV (particle image velocimetry) measurements are taken on the equatorial plane orthogonal to the axis of rotation. The experimental measurements show that the velocity field is strongly influenced by the deformed geometry of the domain. In particular, the formation of a vortex in the vicinity of the lens, which migrates in time towards the core of the domain, is invariably observed. The vortex path is tracked in time by means of a vortex identification technique and it is found that it is significantly influenced by the Womersley number of the flow. Particle trajectories are computed from the PIV measurements. Particles initially located at different positions on the equatorial horizontal plane (perpendicular to the axis of rotation) tend to concentrate in narrow regions adjacent to the lens, thus suggesting the existence, in such regions, of a vertical fluid ejection. Such a strong flow three-dimensionality, which is essentially induced by the irregular shape of the domain, may play a significant role in the mixing processes taking place inside the eye globe. The tangential stresses acting on the rigid boundary of the domain are also computed from the experimental measurements showing that regions subject to particularly intense stresses exist along the boundary close to the lens.     

Overlap of saccadic and pursuit eye movement systems in the brain stem reticular formation.

Recent physiological studies have suggested that there are several sites of interaction between the neural pathways that control saccadic eye movements and those that control visual pursuit movements. To address the question of saccade/pursuit interaction from a neuroanatomical point of view, we have studied the connections from the smooth and saccadic eye movement subregions of the frontal eye field (FEFsem and FEFsac, respectively) to the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) in four Cebus apella monkeys. The riMLF has traditionally been considered to be a premotor center for vertical saccadic eye movements on the basis of single neuron recording experiments, microstimulation experiments, and surgical or chemical lesion experiments. We localized the functional subregions of the FEF with the use of low-threshold (< or =50 microA) intracortical microstimulation. Biotinylated dextran amine or lectin from triticum vulgaris (wheat germ), peroxidase labeled, was placed into these functionally defined subregions to label anterogradely the terminals of axons that originated in the FEF. Our results demonstrate that both the FEFsem and FEFsac send direct projections to the ipsilateral riMLF. The distribution and density of labeling from the FEFsem are comparable to those from the FEFsac. The direct FEFsem-to-riMLF projection suggests a possible role of the riMLF in smooth pursuit eye movements and supports the hypothesis that there is interaction between the saccadic and pursuit subsystems at the brain stem level.     

Alpha-band power in the left frontal cortex discriminates the execution of fixed stimulus during saccadic eye movement

NB-2/contactin-5 plays an important role in synapse formation in the developing auditory system of rodents. In this study, to further elucidate the molecular role of NB-2 in synapse formation, we examined the interaction between NB-2 and amyloid precursor-like protein 1 (APLP1), as well as their possible co-localization at the synapse. Pull-down assays and cell surface binding assays demonstrated that NB-2 interacts with APLP1. Furthermore, the protein expression profile of APLP1 in western blots was similar to that of NB-2, and localization of APLP1 mRNA partially overlapped that of NB-2 mRNA. In cultured hippocampal neurons, immunofluorescence signals for both NB-2 and APLP1 overlapped with synapsin, a presynaptic marker. Biochemical analysis showed that both NB-2 and APLP1 were enriched in the presynaptic fraction. These results indicate that NB-2 forms a cis-complex with APLP1 on the presynaptic membrane.     

Alpha-band power in the left frontal cortex discriminates the execution of fixed stimulus during saccadic eye movement

Introduction: The saccadic paradigm has been used to investigate specific cortical networks involving attention. The behavioral and electrophysiological investigations of the SEM contribute significantly to the understanding of attentive patterns presented of neurological and psychiatric disorders and sports performance. Objective: The current study aimed to investigate absolute alpha power changes in sensorimotor brain regions and the frontal eye fields during the execution of a saccadic task. Methods: Twelve healthy volunteers (mean age: 26.25; SD: ±4.13) performed a saccadic task while the electroencephalographic signal was simultaneously recorded for the cerebral cortex electrodes. The participants were instructed to follow the LEDs with their eyes, being submitted to two different task conditions: a fixed pattern versus a random pattern. Results: We found a moment main effect for the C3, C4, F3 and F4 electrodes and a condition main effect for the F3 electrode. We also found interaction between factor conditions and frontal electrodes. Conclusions: We conclude that absolute alpha power in the left frontal cortex discriminates the execution of the two stimulus presentation patterns during SEM.     

Blood circulation and fluid dynamics in the eye.

The nutrition of the intraocular tissues is accomplished by the retinal vessels, the uveal vessels, and by the aqueous humor. Both morphologically and physiologically the retinal vessels are similar to those in the brain. The endothelial cells of the capillaries are attached to each other by tight junctions, the resistance vessels respond poorly to a large number of drugs, and the blood flow through the retina is autoregulated and very little affected by the sympathetic nervous system. The blood vessels of the iris also have morphological and permeability characteristics similar to those in the brain but they are under a strong influence from the sympathetic nerves and react to many drugs. The blood flow is autoregulated. The blood vessels of the choroid and the ciliary processes are similar to those in the small intestine and in the kidney. The endothelial cells of the capillaries are fenestrated; the vessels respond to sympathetic nervous stimulation and to a large number of vasoactive drugs. Autoregulation of the blood flow is intermediate in the ciliary body and very poor or absent in the choroid...     

Suppressive effects of a peripheral grating displacement during saccadic eye movement and during fixation

Summary Rapid displacement of a peripheral grating reduced sensitivity to test flashes presented at the center of gaze equally well, whether the displacement was produced by mirror movement during fixation or by saccadic eye movement with the grating stationary. Small 0.5 ° flashes in the retinal periphery were not affected by distant grating displacements, but large (5.0 °) flashes were suppressed. Thus there is a size-selective suppressive mechanism which does not affect small stimuli except at the fovea.This research was supported by NIH (NEI) grant No. 5R01 EY01497 to Dr. Brooks and by NIH (NEI) Postdoctoral Fellowship No. 5F32 EY05 191-03 to Dr. Impelman     

White matter fiber integrity of the saccadic eye movement network differs between schizophrenia and healthy groups

Recent diffusion tensor imaging (DTI) studies suggest that altered white matter fiber integrity is a pathophysiological feature of schizophrenia. Lower white matter integrity is associated with poor cognitive control, a characteristic of schizophrenia that can be measured using antisaccade tasks. Although the functional neural correlates of poor antisaccade performance have been well documented, fewer studies have investigated the extent to which white matter fibers connecting the functional nodes of this network contribute to antisaccade performance. The aim of the present study was to assess the white matter structural integrity of fibers connecting two functional nodes (putamen and medial frontal eye fields) of the saccadic eye movement network implicated in poor antisaccade performance in schizophrenia. To evaluate white matter integrity, DTI was acquired on subjects with schizophrenia and two comparison groups: (a) behaviorally matched healthy comparison subjects with low levels of cognitive control (LCC group), and (b) healthy subjects with high levels of cognitive control (HCC group). White matter fibers were tracked between functional regions of interest generated from antisaccade fMRI activation maps, and measures of diffusivity were quantified. The results demonstrated lower white matter integrity in the schizophrenia group than in the HCC group, but not the LCC group who showed similarly poor cognitive control performance. Overall, the results suggest that these alterations are not specific to the disease process of schizophrenia, but may rather be a function of uncontrolled cognitive factors that are concomitant with the disease but also observed in some healthy people.     

Inhibition of return in saccadic eye movements

Inhibition of return (IOR) is a phenomenon in which responses generated to targets at previously attended locations are delayed. It has been suggested that IOR affords a mechanism for optimizing the inspection of novel locations and that it is generated by oculomotor reflexes mediated by the superior colliculus. In this investigation, we measured the effects of IOR on the metrics of saccadic eye movements made to novel and previously attended locations. Saccades made to cued target locations, as well as to other targets within the same hemifield, had longer latencies than saccades made towards the novel, uncued hemifield. We further found that the amplitudes of saccades towards the cued hemifield were more hypometric, but only when the amplitude could not be pre-programmed. These results provide evidence that IOR influences spatial, as well as temporal, parameters of saccadic eye movements and suggest that the exogenous orienting of attention, in addition to influencing target detection, also influences oculomotor programming.