Control Of Pursuit Eye Movements Research Articles

A theory of direction selectivity for macaque primary visual cortex

This paper offers a theory for the origin of direction selectivity (DS) in the macaque primary visual cortex, V1. DS is essential for the perception of motion and control of pursuit eye movements. In the macaque visual pathway, neurons with DS first appear in V1, in the Simple cell population of the Magnocellular input layer 4Cα. The lateral geniculate nucleus (LGN) cells that project to these cortical neurons, however, are not direction selective. We hypothesize that DS is initiated in feed-forward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of 1) different visual response dynamics of ON and OFF LGN cells and 2) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that, together with item 2, produce distinct response time courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Cα in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broadband in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.

A self-trainable depth perception method from eye pursuit and motion parallax

When humans move in a lateral direction (frontal plane), they intuitively understand the motion parallax phenomenon while jointly developing sensory neurons and pursuit eye movements with the help of their life-long learning experiences. At that time, various ranges of motion parallax effects are used to extract meaningful pieces of information such as relative depth of variously positioned objects and the spatial separation between the robot and the fixating object (absolute distance). By mimicking the visual learning in mammals to realize an autonomous robot system, a visual learning framework (Prucksakorn, 2016) was proposed to concurrently develop both visual sensory coding and pursuit eye movement with an addition of depth perception. Within the proposed framework, an artificial neural network was used to learn the relationship between the eye movements and the absolute distance. Nonetheless, the limitation of the proposed framework is that the predefined single lateral body movement cannot fully evoke the motion parallax effect for depth perception. Here, we extend the presented visual learning framework to accurately and autonomously represent the various ranges of absolute distance by using pursuit eye movements from multiple lateral body movements. We show that the proposed model, which is implemented in a HOAP3 humanoid robot simulator, can successfully enhance the smooth pursuit eye movement control with the self-calibrating ability and the distance estimation comparing to the single lateral movement based approach.

Validity of clinical measures of smooth pursuit eye movement control in patients with idiopathic neck pain

BackgroundElectrooculography is useful in detecting smooth pursuit neck torsion (SPNT) abnormalities in patients with neck pain, however, a validated, clinically relevant measure is lacking. ObjectivesTo explore the validity of visual assessment of formal and clinical videotaped SPNT tests in comparison to electrooculography. DesignCross-sectional observational study. MethodTwenty patients with idiopathic neck pain (INP) and twenty healthy controls performed the electrooculography SPNT test: first in neutral, then 45° trunk-under-head torsion to the left then right. The formal video test involved the participant following a horizontal laser stimulus simultaneous to electrooculography. The clinical video test was then performed where the participant followed the clinician's finger in the horizontal direction. One blinded investigator interpreted and analysed the electrooculography trace and two others interpreted the videos. ResultsPatients with INP had a significantly (p < 0.05) greater SPNT difference than healthy controls. Visual observation of the formal test had 82.5% agreement with electrooculography and showed fair sensitivity (63.5%) and good specificity (89.6) whilst the clinical test had 65% agreement with electrooculography and showed poor sensitivity (27.3%) and good specificity (79.3%). There was an 82.5% agreement between investigators for the formal video taped measure. ConclusionsVisual analysis of assessment of SPNT is sufficient for detecting SPNT abnormalities in patients with INP. Accuracy of the clinical method could be improved by, altering how the visual stimulus is presented and including subjective reporting of symptoms to aid diagnosis resulting in implications for future research.

Coordinated Control of Three-Dimensional Components of Smooth Pursuit to Rotating and Translating Textures.

The neural control of pursuit eye movements to visual textures that simultaneously translate and rotate has largely been neglected. Here we propose that pursuit of such targets-texture pursuit-is a fully three-dimensional task that utilizes all three degrees of freedom of the eye, including torsion. Head-fixed healthy human adults (n = 8) tracked a translating and rotating random dot pattern, shown on a computer monitor, with their eyes. Horizontal, vertical, and torsional eye positions were recorded with a head-mounted eye tracker. The torsional component of pursuit is a function of the rotation of the texture, aligned with its visual properties. We observed distinct behaviors between those trials in which stimulus rotation was in the same direction as that of a rolling ball ("natural") in comparison to those with the opposite rotation ("unnatural"): Natural rotation enhanced and unnatural rotation reversed torsional velocity during pursuit, as compared to torsion triggered by a nonrotating random dot pattern. Natural rotation also triggered pursuit with a higher horizontal velocity gain and fewer and smaller corrective saccades. Furthermore, we show that horizontal corrective saccades are synchronized with torsional corrective saccades, indicating temporal coupling of horizontal and torsional saccade control. Pursuit eye movements have a torsional component that depends on the visual stimulus. Horizontal and torsional eye movements are separated in the motor periphery. Our findings suggest that translational and rotational motion signals might be coordinated in descending pursuit pathways.

Direct recordings in human cortex reveal the dynamics of gamma-band [50–150Hz] activity during pursuit eye movement control

The time course of neural activity in human brain regions involved in mediating pursuit eye movements is unclear. To address this question, we recorded intracerebral electroencephalography activity in eight epileptic patients while they performed a pursuit task that dissociates reactive, predictive and inhibited pursuits. A sustained gamma band (50-150 Hz) activity corresponding to pursuit maintenance was observed in the pursuit (and not saccade) area of the frontal eye field (FEF), in the ventral intraparietal sulcus (VIPS) and in occipital areas. The latency of gamma increase was found to precede target onset in FEF and VIPS, suggesting that those areas could also be involved during pursuit preparation/initiation. During pursuit inhibition, a sustained gamma band response was observed within prefrontal areas (pre-supplementary-motor-area, dorso-lateral prefrontal and frontopolar cortex). This study describes for the first time the dynamics of the neural activity in four areas of the pursuit system, not previously available in humans. These findings provide novel timing constraints to current models of the human pursuit system and establish the relevance of direct recordings to precisely relate eye movement behavior with neural activity in humans.

Role of anticipation and prediction in smooth pursuit eye movement control in Parkinson's disease

Patients with Parkinson's disease (PD) have difficulties in the control of self-guided (i.e., internally driven) movements. The basal ganglia provide a nonspecific internal cue for the development of a preparatory activity for a given movement in the sequence of repetitive movements. Controversy surrounds the question of whether PD patients are capable of (1) anticipating (before an external trigger appears; i.e., anticipation) and (2) predicting movement velocity once a moving target shortly disappears from the visual scene (i.e., prediction). To dissociate between these two components, we examined internally driven (extraretinal generated) smooth pursuit eye movements in PD patients and age-matched healthy controls by systematically varying target blanking periods of a trapezoidally moving target in four paradigms (initial blanking, midramp blanking, blanking after a short ramp, and no blanking). Compared to controls, PD patients showed (1) decreased smooth pursuit gain (without blanking), (2) deficient anticipatory pursuit (prolonged pursuit initiation latency; reduced eye velocity before target onset in the early onset blanking paradigm), and (3) preserved extraretinal predictive pursuit velocity (midramp target blanking). Deficient anticipation of future target motion was not related to either disease duration or the general motor impairment (UPDRS). We conclude that PD patients have difficulties in anticipating future target motion, which may play a role for the mechanisms involved in deficient gait initiation and termination of PD. In contrast, they remain unimpaired in their capacity of building up an internal representation of continuous target motion. This may explain the clinical advantage of medical devices that use visual motion to improve gait initiation (e.g., "PD glasses").

Altered transfer of visual motion information to parietal association cortex in untreated first-episode psychosis: Implications for pursuit eye tracking

Visual motion processing and its use for pursuit eye movement control represent a valuable model for studying the use of sensory input for action planning. In psychotic disorders, alterations of visual motion perception have been suggested to cause pursuit eye tracking deficits. We evaluated this system in functional neuroimaging studies of untreated first-episode schizophrenia ( N = 24), psychotic bipolar disorder patients ( N = 13) and healthy controls ( N = 20). During a passive visual motion processing task, both patient groups showed reduced activation in the posterior parietal projection fields of motion-sensitive extrastriate area V5, but not in V5 itself. This suggests reduced bottom-up transfer of visual motion information from extrastriate cortex to perceptual systems in parietal association cortex. During active pursuit, activation was enhanced in anterior intraparietal sulcus and insula in both patient groups, and in dorsolateral prefrontal cortex and dorsomedial thalamus in schizophrenia patients. This may result from increased demands on sensorimotor systems for pursuit control due to the limited availability of perceptual motion information about target speed and tracking error. Visual motion information transfer deficits to higher-level association cortex may contribute to well-established pursuit tracking abnormalities, and perhaps to a wider array of alterations in perception and action planning in psychotic disorders.

Auditory deprivation during infancy affects the control of pursuit eye movements

Auditory deprivation during infancy affects the control of pursuit eye movements

Mossy and climbing fiber collateral inputs in monkey cerebellar paraflocculus lobulus petrosus and hemispheric lobule VII and their relevance to oculomotor functions

Recent lesion studies on monkeys suggest that the cerebellar lobulus petrosus of the paraflocculus (LP) and crura I and II of hemispheric lobule VII (H-7) are involved in smooth pursuit eye movement control. To reveal the relationship between the LP and H-7, we studied mossy and climbing fiber collateral inputs to these areas in four cynamolgus monkeys. After unilateral injections of retrograde tracers into the LP, labeled mossy fibers were seen ipsilaterally in the crura I and II of H-7. A very small number of labeled mossy fiber collaterals were also seen in the dorsal paraflocculus (DP). Labeled climbing fibers were seen exclusively in the ipsilateral crus I. No labeled mossy/climbing fibers were seen in the flocculus, ventral paraflocculus and other cortical areas. Combined injections of fast blue in the LP and cholera toxin subunit B in the posterior crus I and crus II of H-7 resulted in a small number of the double-labeled pontine and principal olivary neurons. Combined injections in the LP and DP induced only a few double-labeled neurons in the pontine nuclei, and no double-labeled neurons in the olivary nuclei. These results suggest that the LP and crura I and II of H-7 may share some of their mossy and climbing fiber inputs and mediate similar functional roles involving smooth pursuit eye movement control.

Difference of climbing fiber input sources between the primate oculomotor-related cerebellar vermis and hemisphere revealed by a retrograde tracing study

The cerebellar flocculus–paraflocculus complex, vermal lobule VII (V-7) and hemispheric lobule VII (H-7) are involved in learning-dependent smooth pursuit eye movement control. To locate the sources of climbing fiber inputs to the H-7 and V-7, we injected retrograde tracers and examined the locations of retrogradely labeled neurons in the inferior olive in 4 monkeys. After the injection of cholera toxin B (CTB) into the H-7, retrogradely labeled neurons were observed abundantly in cell group d, i.e., dorsal cap, of the caudal medial accessory olive (MAO) and ventral lamella of principal olive (PO). After injections of fast blue (FB) into the V-7, retrogradely labeled neurons were observed mainly in cell group b of MAO, but rarely in cell group d or PO. Cell group d is known to receive inputs from the nucleus optic tract (NOT) and project climbing fibers to the flocculus and ventral paraflocculus, and cell group b is known to receive inputs from the superior colliculus. These results suggest that the three oculomotor cerebellar areas may use different visual signals for the control of smooth pursuit: the flocculus–paraflocculus complex and H-7 receive visual climbing fiber inputs derived mainly from the NOT via cell group d, while the V-7 receive visual climbing fiber inputs derived mainly from the superior colliculus via cell group b.

Role of primate cerebellar lobulus petrosus of paraflocculus in smooth pursuit eye movement control revealed by chemical lesion

The primate lobulus petrosus (LP) of the cerebellar paraflocculus receives inputs from visual system-related pontine nuclei, and projects to eye movement-related cerebellar nuclei. To reveal a potential involvement of LP in oculomotor control, we lesioned LP unilaterally by local injections of ibotenic acid in three Macaca fuscata. We examined the effects of lesion on eye movements evoked by step (3°)–ramp (5–15°/s) moving target. To step–ramp moving target, the monkeys showed an initial slow eye movement and later a small catch-up saccade, which was followed by the post-saccadic pursuit nearly matching to the velocity of the ramp target motion. After LP lesioning, the velocity of post-saccadic pursuits in the ipsiversive and down-ward directions decreased by 20–40% in all three monkeys. These deficits lasted for at least 1 month, and some recovery was observed. In the amplitudes of catch-up saccades, no consistent changes were seen among the three monkeys after LP lesioning. These results suggest an involvement of LP in the primate smooth pursuit eye movement control.

Eye movement control by the cerebral cortex

This review focuses on eye movement control by the cerebral cortex, mainly in humans. Data have emerged based on the important contribution of recent techniques such as transcranial magnetic stimulation and functional magnetic resonance imaging, which provide complementary results to those of the classical lesion and electrical stimulation studies. The location of the human frontal eye field and its role in pursuit eye movement control were recently detailed. Cumulative evidence for the role of the dorsolateral prefrontal cortex in unwanted reflexive saccade inhibition, short-term spatial memory and prediction suggests that this area controls decisional processes governing ocular motor behaviour. The organization of spatial memory in the dorsolateral prefrontal cortex (short-term), the parahippocampal cortex (medium-term) and the hippocampal formation (long-term) is also reviewed with the results of recent transcranial magnetic stimulation studies. The relatively complicated anatomy of the posterior parietal cortex in humans is briefly described followed by some additional results concerning the location of the parietal eye field - within the posterior half of the intraparietal sulcus - and its role in visuo-spatial integration and attention. The other areas involved in spatial attention are also examined in the light of several recent contributing reports. Lastly, there are also new functional magnetic resonance imaging findings concerning the posterior cingulate cortex, which appears to be mainly involved in the control of externally guided eye movements and attentional mechanisms. Many new findings on the organization of saccades and pursuit eye movements at the cortical level have recently been reported. Furthermore, eye movements are increasingly used as a tool to elucidate relatively complex neuropsychological processes such as attention, spatial memory, motivation and decisional processes, and a considerable number of reports dealing with these questions have been observed.

Adaptive control of pursuit eye movements in humans

Adaptive control of pursuit eye movements in humans

Neuronal mechanisms for detection of motion in the field of view

The visual system cannot rely only upon information from the retina to perceive object motion because identical retinal stimulations can be evoked by the movement of objects in the field of view as well as by the movements of retinal images self-evoked by eye movements. We clearly distinguish the two situations, perceiving object motion in the first case and stationarity in the second. The present work deals with the neuronal mechanisms that are likely involved in the detection of real motion. In monkeys, cells that are able to distinguish real from self-induced motion (real-motion cells) are distributed in several cortical areas of the dorsal visual stream. We suggest that the activity of these cells is responsible for motion perception, and hypothesize that these cells are the elements of a cortical network representing an internal map of a stable visual world. Supporting this view are the facts that: (i) the same cortical regions in humans are activated in brain imaging studies during perception of object motion; and (ii) lesions of these same regions produce selective impairments in motion detection, so that patients interpret any retinal image motion as object motion, even when they result from her/his eye movements. Among the areas of the dorsal visual stream rich in real-motion cells, V3A and V6, likely involved in the fast form and motion analyses needed for visual guidance of action, could use real-motion signals to orient the animal’s attention towards moving objects, and/or to help grasping them. Areas MT/V5, MST and 7a, known to be involved in the control of pursuit eye movements and in the analysis of visual signals evoked by slow ocular movements, could use real-motion signals to give a proper evaluation of motion during pursuits.

Extraretinal Inputs to Neurons in the Rostral Superior Colliculus of the Monkey During Smooth-Pursuit Eye Movements

The intermediate and deep layers of the monkey superior colliculus (SC) are known to be important for the generation of saccadic eye movements. Recent studies have also provided evidence that the rostral SC might be involved in the control of pursuit eye movements. However, because rostral SC neurons respond to visual stimuli used to guide pursuit, it is also possible that the pursuit-related activity is simply a visual response. To test this possibility, we recorded the activity of neurons in the rostral SC as monkeys smoothly pursued a target that was briefly extinguished. We found that almost all rostral SC neurons in our sample maintained their pursuit-related activity during a brief visual blink, which was similar to the maintained activity they also exhibited during blinks imposed during fixation. These results indicate that discharge of rostral SC neurons during pursuit is not simply a visual response, but includes extraretinal signals.

Encoding of Smooth Pursuit Direction and Eye Position by Neurons of Area MSTd of Macaque Monkey

The spike activity of neurons was recorded from the dorsal bank of the superior temporal sulcus (area MSTd) of alert behaving macaque monkeys performing visual fixation or target tracking tasks, with the aim of studying the tuning features of these neurons with both the direction of slow eye movement and the position of gaze. One hundred thirty-two neurons were tested for several fixation points and tracking directions. Many of them (43%) tuned to the direction of pursuit, regardless of the angle of gaze. Some (18%) showed a tonic discharge modulated by the static position of the eyes without pursuit direction specificity. A substantial number of cells (22%) were characterized by a discharge rate tuned to pursuit direction but influenced also by angle of gaze. Tuning curves for eye movement direction presented an average bandwidth of 130 degrees and turned out to be continuously overlapping, suggesting a sort of vector coding of smooth pursuit direction. Gaze fields of eye position (EP) neurons were mostly ramp-like, with center of ramps shifted away from the straight ahead, implying a form of scalar coding of gaze eccentricity. The different categories of cells were intermingled and close to each other, suggesting possible reciprocal interactions within the same cortical area. These results show that EP and pursuit direction are signaled mainly by separate neuronal elements in area MSTd. Moreover, some cells can integrate both signals. Taking into account the visual responses of MSTd neurons to large, textured, moving fields, it is suggested that this area could be the site of interaction between visuo-oculomotor signals related to visual motion detection, slow eye movement direction, and EP. This signal interaction may be important for integrative functions such as analysis of external or self-induced visual motion, cortical control of pursuit eye movements, and eye/head coordination.

Upbeat nystagmus: Clinicopathological and pathophysiological considerations

We describe an electro-oculographic study of upbeat nystagmus in 4 patients, with neuropathological correlation in one. All patients had lesions in the pontine tegmentum. The electro-oculographic data may be explained by imbalanced vertical vestibular or smooth pursuit eye movement control. The nystagmus stopped or reversed direction during convergence or in supine head positions. We propose that changes in the intensity or direction of upbeat nystagmus that are induced by convergence or changes in head position, are caused by vertical imbalance in the otolithic-ocular reflex, when superimposed on an imbalanced vestibulo-ocular reflex (VOR). Imbalance of the otolithic-ocular reflex and the vertical VOR are caused by damage in the pontomedullary tegmentum.

Neural control of pursuit eye movements.

Neural control of pursuit eye movements.R EckmillerR EckmillerSearch for more papers by this authorPublished Online:01 Jul 1987https://doi.org/10.1152/physrev.1987.67.3.797MoreSectionsPDF (10 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByBrain Activation during Smooth-Pursuit Eye MovementsNeuroImage, Vol. 17, No. 3Role of Arcuate Frontal Cortex of Monkeys in Smooth Pursuit Eye Movements. I. Basic Response Properties to Retinal Image Motion and PositionMasaki Tanaka, and Stephen G. Lisberger1 June 2002 | Journal of Neurophysiology, Vol. 87, No. 6Functional Anatomy of Pursuit Eye Movements in Humans as Revealed by fMRILaurent Petit, and James V. Haxby1 July 1999 | Journal of Neurophysiology, Vol. 82, No. 1The cerebellum as a predictor of neural messages—II. Role in motor control and motion sicknessNeuroscience, Vol. 56, No. 3Central neuroanatomical organisation of the rat visuomotor systemProgress in Neurobiology, Vol. 41, No. 2Longitudinal tracking responses of the weakly electric fish, SternopygusJournal of Comparative Physiology A, Vol. 171, No. 6Generation of smooth-pursuit eye movements: neuronal mechanisms and pathwaysNeuroscience Research, Vol. 11, No. 2Computational model of the motor program generator for pursuitJournal of Neuroscience Methods, Vol. 21, No. 2-4 More from this issue > Volume 67Issue 3July 1987Pages 797-857 Copyright & PermissionsCopyright © 1987 by American Physiological Societyhttps://doi.org/10.1152/physrev.1987.67.3.797PubMed3299410History Published online 1 July 1987 Published in print 1 July 1987 Metrics

Selection of sensory information in control of pursuit eye movements

Ss performed fixation shifts between moving and stationary targets that were presented against a visually complex background. Post-saccade pursuit latencies were far shorter than the response lags previously reported for the pursuit control system. This is interpreted as evidence for control of initial post-saccade pursuit velocity by pre-saccade image velocity information selected from a limited region of peripheral retina.