Control Of Saccadic Eye Movements Research Articles

Cognitive control of saccadic eye movements

The saccadic eye movement system provides researchers with a powerful tool with which to explore the cognitive control of behaviour. It is a behavioural system whose limited output can be measured with exceptional precision, and whose input can be controlled and manipulated in subtle ways. A range of cognitive processes (notably those involved in working memory and attention) have been shown to influence saccade parameters. Researchers interested in the relationship between cognitive function and psychiatric disorders have made extensive use of saccadic eye movement tasks to draw inferences as to the cognitive deficits associated with particular psychopathologies. The purpose of this review is to provide researchers with an overview of the research literature documenting cognitive involvement in saccadic tasks in healthy controls. An appreciation of this literature provides a solid background against which to interpret the deficits on saccadic tasks demonstrated in patient populations.

Role of Primate Cerebellar Hemisphere in Voluntary Eye Movement Control Revealed by Lesion Effects

The anatomical connection between the frontal eye field and the cerebellar hemispheric lobule VII (H-VII) suggests a potential role of the hemisphere in voluntary eye movement control. To reveal the involvement of the hemisphere in smooth pursuit and saccade control, we made a unilateral lesion around H-VII and examined its effects in three Macaca fuscata that were trained to pursue visually a small target. To the step (3 degrees)-ramp (5-20 degrees/s) target motion, the monkeys usually showed an initial pursuit eye movement at a latency of 80-140 ms and a small catch-up saccade at 140-220 ms that was followed by a postsaccadic pursuit eye movement that roughly matched the ramp target velocity. After unilateral cerebellar hemispheric lesioning, the initial pursuit eye movements were impaired, and the velocities of the postsaccadic pursuit eye movements decreased. The onsets of 5 degrees visually guided saccades to the stationary target were delayed, and their amplitudes showed a tendency of increased trial-to-trial variability but never became hypo- or hypermetric. Similar tendencies were observed in the onsets and amplitudes of catch-up saccades. The adaptation of open-loop smooth pursuit velocity, tested by a step increase in target velocity for a brief period, was impaired. These lesion effects were recognized in all directions, particularly in the ipsiversive direction. A recovery was observed at 4 wk postlesion for some of these lesion effects. These results suggest that the cerebellar hemispheric region around lobule VII is involved in the control of smooth pursuit and saccadic eye movements.

Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

The current dominant concept for the control of saccadic eye movements by the basal ganglia is that release from tonic GABAergic inhibition by the substantia nigra pars reticulata (SNr) triggers burst firings of intermediate gray layer (SGI) neurons in the superior colliculus (SC) to allow saccade initiation. This hypothesis is based on the assumption that SNr cells inhibit excitatory projection neurons in the SGI. Here we show that nigrotectal fibers are connected to local GABAergic neurons in the SGI with a similar frequency to non-GABAergic neurons. This was accomplished by applying neuroanatomical tracing and slice electrophysiological experiments in GAD67-green fluorescent protein (GFP) knock-in mice, in which GABAergic neurons specifically express GFP. We also found that GABA(A), but not GABA(B), receptors subserve nigrotectal transmission. The present results revealed a novel aspect on the role of the basal ganglia in the control of saccades, e.g., the SNr not only regulates burst initiation but also modulates the spatiotemporal properties of premotor neurons via connections to local GABAergic neurons in the SC.

Familial congenital oculomotor apraxia: Clinical and electro-oculographic features

The electro-oculographic (EOG) features of both horizontal and vertical eye movements in congenital oculomotor apraxia (COMA) were not previously reported. A girl referred to the ophthalmologic department for abnormal eye movements was diagnosed as COMA. The same abnormal ocular movements were observed in her younger sister and her father who was unaware of his difficulties to initiate voluntary saccades. When performed, EOG recordings of all horizontal and vertical saccadic eye movements were severely altered whatever the age of the patient. Pursuit was normal for these patients. It confirms that the control of saccadic eye movements is still altered in adults in both directions horizontal and vertical that were never reported. EOG is necessary to rule out inherited form of this saccade initiation failure.

5. Role of the amygdala in the control of saccadic eye movements

5. Role of the amygdala in the control of saccadic eye movements

Brief intermittent light stimulation disrupts saccadic oculomotor control

This study sought to determine the effect of very brief, single and multiple pulses of light on spatial and temporal aspects of saccadic eye movements. Twelve visually normal, young adult subjects participated in the experiments. Horizontal eye position was monitored as subjects attempted to track target step displacements in the presence of either single or multiple brief flashes of light in the visual field. Three primary findings were observed: (1) increased saccadic latency, (2) increased time for target acquisition and (3) increased initial saccadic error. The present findings suggest the influence of attentional processes and/or visual masking effects on saccadic eye movement control.

An fMRI Study of Saccadic and Smooth-Pursuit Eye Movement Control in Patients with Age-Related Macular Degeneration

To compare the cortical networks that underlie oculomotor function in patients with age-related macular degeneration (AMD) with those in normally sighted control subjects, using functional magnetic resonance imaging (fMRI). Six patients with bilateral geographic retinal atrophy due to AMD (age range, 55-83 years) were recruited for the study. The visual acuities of the patients ranged from 20/76 (0.58 logMAR) to 20/360 (1.26 logMAR). An additional six younger (age range, 22-31 years) and six older (age range, 54-78 years) normally sighted individuals were recruited as control subjects. fMRI data were acquired on a 3.0-Tesla, scanner while subjects performed visually guided saccade (VGS) and smooth-pursuit (SmP) tasks. Contrasts between VGS and fixation on a stationary target identified a network of activation that included the frontal eye fields (FEFs), supplementary eye fields (SMA/SEFs), prefrontal cortex (PFC), intraparietal sulci (IPS), and the areas of the visual cortex (MT/V5, V2/V3, and V1) in control subjects and patients. A similar network was identified for comparisons between SmP and periods of fixation. Marked variability was observed in the performance of both tasks across all patients. For both tasks, the patients generally showed increased PFC and IPS activation, with decreased activation in visual cortex compared with the control subjects. The patients showed significantly increased activation of the FEFs and SMA/SEFs in the SmP task, compared with the control subjects. These data suggest that performance of both eye movement tasks required greater involvement of the cortical regions generally implicated in attention and effort in patients with AMD.

Connectivity modulation of early visual processing areas during covert and overt tracking tasks

The brain regions for pursuit and saccadic eye movement processing are well known. There is, however, little knowledge about the interaction between these areas during voluntary eye movements. With 8 subjects, we investigated the dynamics of cortical areas involved in control of saccadic and smooth pursuit eye movements. We explored the connectivity between V1, hMT+, and LIP. Additionally, we explored the effects caused by shifting covert attention between pursuit and saccade targets. We modeled 15 plausible models, selecting the best one using a new group comparison approach for DCM models. Effective connectivity from V1 to hMT+ was shown to depend on whether subjects attended covertly or overtly to the targets. Comparing active tracking tasks resulted in effects in accordance with current theories of the eye movement processing system.

Saccadic impairments in Huntington’s disease

Huntington's disease (HD), a progressive neurological disorder involving degeneration in basal ganglia structures, leads to abnormal control of saccadic eye movements. We investigated whether saccadic impairments in HD (N = 9) correlated with clinical disease severity to determine the relationship between saccadic control and basal ganglia pathology. HD patients and age/sex-matched controls performed various eye movement tasks that required the execution or suppression of automatic or voluntary saccades. In the "immediate" saccade tasks, subjects were instructed to look either toward (pro-saccade) or away from (anti-saccade) a peripheral stimulus. In the "delayed" saccade tasks (pro-/anti-saccades; delayed memory-guided sequential saccades), subjects were instructed to wait for a central fixation point to disappear before initiating saccades towards or away from a peripheral stimulus that had appeared previously. In all tasks, mean saccadic reaction time was longer and more variable amongst the HD patients. On immediate anti-saccade trials, the occurrence of direction errors (pro-saccades initiated toward stimulus) was higher in the HD patients. In the delayed tasks, timing errors (eye movements made prior to the go signal) were also greater in the HD patients. The increased variability in saccadic reaction times and occurrence of errors (both timing and direction errors) were highly correlated with disease severity, as assessed with the Unified Huntington's Disease Rating Scale, suggesting that saccadic impairments worsen as the disease progresses. Thus, performance on voluntary saccade paradigms provides a sensitive indicator of disease progression in HD.

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.

Neglect as a disorder of prior probability

Subjects with spatial neglect are slower and more variable in detecting visual targets, especially on the side opposite their brain injuries. These deficits can be seen by plotting cumulative distribution functions (CDF) of response times (RT). I demonstrate that dividing RT’s by their means normalizes the RT CDF’s of neglect subjects. The motivation for this transformation comes from Carpenter’s LATER model [Carpenter, R. H. S., & Williams, M. L. L. (1995). Neural computation of log likelihood in control of saccadic eye movements. Nature, 377, 59–62]. The most direct interpretation of this result is that some symptoms of neglect reflect abnormal estimates of stimulus prior probability.

Case Report Vestibular Rehabilitation Decreases Fall Risk and Improves Gaze Stability for an Older Individual with Unilateral Vestibular Hypofunction

Partial or total unilateral vestibular loss is the third most common cause of peripheral vestibular dysfunction. Dysfunction of one or both of the vestibular mechanisms can manifest physically as abnormalities of posture, balance, and/or visual acuity. This case report describes physical therapy examination and individualized intervention with vestibular rehabilitation for a patient with unilateral vestibular hypofunction. The patient was an 80-year-old male with electronystamographically confirmed unilateral vestibular loss of 98.3%. He demonstrated altered balance and gaze stability classifying him as having an increased risk for falling. After 5 weeks of individualized vestibular rehabilitation, the patient significantly decreased his fall risk from 11 to 20 of 24 on the Dynamic Gait Index. His gaze stability also improved from a 4 to 1 line disparity with dynamic visual acuity testing. The patient also had a decrease in perceived disability on the Dizziness Handicap Inventory from 30/100 at evaluation to 12/100 at discharge. Individualized vestibular rehabilitation decreased fall risk and improved gaze stability for a patient with significant unilateral vestibular hypofunction.

Quantitative analysis of spontaneous saccade-like rapid eye movements in C57BL/6 mice

Saccadic eye movement is a rapid shift of eye position to capture an object in the environment. In this study, we will describe the fundamental properties of spontaneously evoked saccade-like rapid eye movement (SLREM) in mice in order to establish the mouse experimental model for studying saccades. Spontaneous SLREM were recorded and analyzed in C57BL/6 mice in a quantitative manner, using high-speed video-oculography at a high temporal resolution (240 frames/s) under head-fixed conditions. Mice made spontaneous SLREMs in the dark with median amplitude of 14.3 ± 2.1°, mainly in the horizontal direction. The peak velocity of SLREM increased almost linearly against its amplitude with slope of 43.6 ± 6.1 (°/s)/° in the upward, 63.3 ± 18.0 (°/s)/° in the downward, 51.3 ± 3.9 (°/s)/° in the nasal, and 31.7 ± 3.2 (°/s)/° in the temporal direction. The duration of SLREM was 56.6 ± 23.3 ms in the upward, 57.3 ± 18.0 ms in the downward, 52.0 ± 5.0 ms in the nasal, and 69.3 ± 5.5 ms in the temporal direction. This study provides the basis for analyzing the neural and molecular mechanisms engaged in the control of saccadic eye movements in genetically-engineered mice.

What clinical disorders tell us about the neural control of saccadic eye movements

Saccades are rapid eye movements that redirect the fovea from one object to another. They must be fast and accurate to allow good vision. Saccades represent an ideal system for studying the neural control of movement. This article is a very detailed review written by experts in eye movements. Basic research on normal eye movements has greatly increased understanding of saccadic performance, anatomy and physiology, and led to a large number of control system models. These models simulate normal saccades well, but are challenged by clinical disorders because they often do not incorporate the specific anatomical and physiological substrates needed to model clinically important abnormalities. Historically, studies of saccadic abnormalities in patients have played a critical role in understanding the neural control of saccades because they provide information that complements basic research and thus restricts hypotheses to those that are biologically plausible. The authors specifically review four examples of clinical disorders (slow saccades, interrupted saccades, high-frequency saccadic oscillations, and macrosaccadic oscillations).—Valérie Biousse

Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

Coordinated movements of the eye, head, and body are used to redirect the axis of gaze between objects of interest. However, previous studies of eye-head gaze shifts in head-unrestrained primates generally assumed the contribution of body movement to be negligible. Here we characterized eye-head-body coordination during horizontal gaze shifts made by trained rhesus monkeys to visual targets while they sat upright in a standard primate chair and assumed a more natural sitting posture in a custom-designed chair. In both postures, gaze shifts were characterized by the sequential onset of eye, head, and body movements, which could be described by predictable relationships. Body motion made a small but significant contribution to gaze shifts that were > or =40 degrees in amplitude. Furthermore, as gaze shift amplitude increased (40-120 degrees ), body contribution and velocity increased systematically. In contrast, peak eye and head velocities plateaued at velocities of approximately 250-300 degrees /s, and the rotation of the eye-in-orbit and head-on-body remained well within the physical limits of ocular and neck motility during large gaze shifts, saturating at approximately 35 and 60 degrees , respectively. Gaze shifts initiated with the eye more contralateral in the orbit were accompanied by smaller body as well as head movement amplitudes and velocities were greater when monkeys were seated in the more natural body posture. Taken together, our findings show that body movement makes a predictable contribution to gaze shifts that is systematically influenced by factors such as orbital position and posture. We conclude that body movements are part of a coordinated series of motor events that are used to voluntarily reorient gaze and that these movements can be significant even in a typical laboratory setting. Our results emphasize the need for caution in the interpretation of data from neurophysiological studies of the control of saccadic eye movements and/or eye-head gaze shifts because single neurons can code motor commands to move the body as well as the head and eyes.

Predictive control of saccadic eye movements during errors

Predictive control of saccadic eye movements during errors

What clinical disorders tell us about the neural control of saccadic eye movements

Saccades are rapid eye movements that redirect the fovea from one object to another. A great deal has been learned about the anatomy and physiology of saccades, making them an ideal system for studying the neural control of movement. Basic research on normal eye movements has greatly increased our understanding of saccadic performance, anatomy and physiology, and led to a large number of control system models. These models simulate normal saccades well, but are challenged by clinical disorders because they often do not incorporate the specific anatomical and physiological substrates needed to model clinically important abnormalities. Historically, studies of saccadic abnormalities in patients have played a critical role in understanding the neural control of saccades because they provide information that complements basic research and thus restricts hypotheses to those that are biologically plausible. This review presents four examples of clinical disorders (slow saccades, interrupted saccades, high-frequency saccadic oscillations and macrosaccadic oscillations) that have provided insights into the neurobiology of saccades, have driven the development of new models, and have suggested an explanation or treatment for these disorders. We raise general questions for both scientists and clinicians that will assist in their efforts to understand the neural control of movement, improve diagnostic criteria and develop new treatments.

Somatosensory-Motor Neuronal Activity in the Superior Colliculus of the Primate

The superior colliculus (SC) in primates plays an important role in orienting gaze and arms toward novel stimuli. Here we ask whether neurons in the intermediate and deep layers of the SC are also involved in the interaction with objects. In two trained monkeys we found a large number of SC units that were specifically activated when the monkeys contacted and pushed a target that had been reached with either hand. These neurons, however, were silent when the monkeys simply looked at or reached for the target but did not touch it. The activity related to interacting with objects was spatially tuned and increased with push strength. Neurons in the SC with this type of activity may be involved in a somatosensory-motor feedback loop that monitors the force of the active muscles together with the spatial position of the limb required for proper interaction with an object.

Role of the human supplementary eye field in the control of saccadic eye movements

The precise function of the supplementary eye field (SEF) is poorly understood. Although electrophysiological and functional imaging studies are important for demonstrating when SEF neurones are active, lesion studies are critical to establish the functions for which the SEF is essential. Here we report a series of investigations performed on an extremely rare individual with a highly focal lesion of the medial frontal cortex. High-resolution structural imaging demonstrated that his lesion was confined to the region of the left paracentral sulcus, the anatomical locus of the SEF. Behavioural testing revealed that the patient was significantly impaired when required to switch between anti- and pro-saccades, when there were conflicting rules governing stimulus–response mappings for saccades. Similarly, the results of an arbitrary stimulus–response associative learning task demonstrated that he was impaired when required to select the appropriate saccade from conflicting eye movement responses, but not for limb movements on an analogous manual task. When making memory-guided saccadic sequences, the patient demonstrated hypometria, like patients with Parkinson's disease, but had no significant difficulties in reproducing the order of saccades correctly on a task that emphasized accuracy with a wide temporal segregation between responses. These findings are consistent with the hypothesis that the SEF plays a key role in implementing control when there is conflict between several, ongoing competing saccadic responses, but not when eye movements need to be made accurately in sequence.

The spatio-temporal tuning of the mechanisms in the control of saccadic eye movements

We compared the spatio-temporal tuning of perception to the mechanisms that drive saccadic eye movements. Detection thresholds were measured for Gabor-targets presented left or right of fixation (4 or 8 deg eccentricity), at one of four spatial frequencies (1, 2, 4 or 8 cpd) oscillating at one of three temporal frequencies (1, 8 or 16 Hz). We then measured saccade latency to each target presented at various multiples of detection threshold. Consistent with previous research, latency decreased as a function of contrast. However, at equal detection performance, we found no systematic difference in saccadic latency and no difference in average oculometric performance (% correct saccade direction) across the different target spatio-temporal frequencies. Furthermore, position error remained fairly constant across all conditions. The results are consistent with the idea that the spatio-temporal signals used for perception are the same as those used by the mechanisms driving saccadic eye movements.