Control Of Smooth Pursuit Eye Movements Research Articles

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.

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").

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.

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.

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.

Contextual Effects on Smooth-Pursuit Eye Movements

Segregating a moving object from its visual context is particularly relevant for the control of smooth-pursuit eye movements. We examined the interaction between a moving object and a stationary or moving visual context to determine the role of the context motion signal in driving pursuit. Eye movements were recorded from human observers to a medium-contrast Gaussian dot that moved horizontally at constant velocity. A peripheral context consisted of two vertically oriented sinusoidal gratings, one above and one below the stimulus trajectory, that were either stationary or drifted into the same or opposite direction as that of the target at different velocities. We found that a stationary context impaired pursuit acceleration and velocity and prolonged pursuit latency. A drifting context enhanced pursuit performance, irrespective of its motion direction. This effect was modulated by context contrast and orientation. When a context was briefly perturbed to move faster or slower eye velocity changed accordingly, but only when the context was drifting along with the target. Perturbing a context into the direction orthogonal to target motion evoked a deviation of the eye opposite to the perturbation direction. We therefore provide evidence for the use of absolute and relative motion cues, or motion assimilation and motion contrast, for the control of smooth-pursuit eye movements.

Roles of the cerebellum in pursuit-vestibular interactions.

This mini-review focuses on cerebellar roles in on-line control of smooth-pursuit eye movements during vestibular stimulation in primates. The smooth-pursuit system is necessary to track smoothly moving targets and must interact with the vestibular system during movement of the head and/or whole body to maintain the precision of eye movements in space (i.e. gaze movements). This interaction requires calculation of gaze velocity commands that match the eye velocity in space to the actual target velocity. Two cerebellar regions, the floccular lobe that consists of the flocculus and ventral paraflocculus, and the dorsal vermis, are known to be involved in smooth-pursuit. However, potential differences in their involvement are incompletely understood. To understand their roles, in particular whether the output of these regions codes gaze velocity or eye velocity, simple-spike activity of Purkinje (P-) cells was examined during smooth-pursuit and pursuit-vestibular interaction tasks in various directions in head-restrained monkeys. The results showed differences in discharge characteristics of vertical and horizontal P-cells within the floccular lobe and between the floccular lobe and dorsal vermis. These differences and other available evidence suggest that the dorsal vermis is involved more in the control of gaze movement whereas the floccular lobe primarily controls eye movement (in the orbit) as a component of the oculomotor neural integrator. Smooth-pursuit without vestibular stimulation cannot dissociate eye movement from gaze movement. To understand the cerebellar role in various aspects of smooth tracking of targets moving in the three dimensional space, more information is needed particularly on how the above mentioned two regions along with the dorsal paraflocclus and underlying deep cerebellar nuclei are involved in vergence tracking, how the cerebellum is involved in prediction and perception of target motion, and whether complex-spike discharge is involved in a fast adaptive process that may be used for prediction in smooth ocular tracking.

Smooth-pursuit eye-movement deficits with chemical lesions in macaque nucleus reticularis tegmenti pontis.

Anatomic and neuronal recordings suggest that the nucleus reticularis tegmenti pontis (NRTP) of macaques may be a major pontine component of a cortico-ponto-cerebellar pathway that subserves the control of smooth-pursuit eye movements. The existence of such a pathway was implicated by the lack of permanent pursuit impairment after bilateral lesions in the dorsolateral pontine nucleus. To provide more direct evidence that NRTP is involved with regulating smooth-pursuit eye movements, chemical lesions were made in macaque NRTP by injecting either lidocaine or ibotenic acid. Injection sites first were identified by the recording of smooth-pursuit-related modulations in neuronal activity. The resulting lesions caused significant deficits in both the maintenance and the initiation of smooth-pursuit eye movements. After lesion formation, the gain of constant-velocity, maintained smooth-pursuit eye movements decreased, on the average, by 44%. Recovery of the ability to maintain smooth-pursuit eye movements occurred over approximately 3 days when maintained pursuit gains attained normal values. The step-ramp, "Rashbass" task was used to investigate the effects of the lesions on the initiation of smooth-pursuit eye movements. Eye accelerations averaged over the initial 80 ms of pursuit initiation were determined and found to be decremented, on the average, by 48% after the administration of ibotenic acid. Impairments in the initiation and maintenance of smooth-pursuit eye movements were directional in nature. Upward pursuit seemed to be the most vulnerable and was impaired in all cases independent of lesioning agent and type of pursuit investigated. Downward smooth pursuit seemed more resistant to the effects of chemical lesions in NRTP. Impairments in horizontal tracking were observed with examples of deficits in ipsilaterally and contralaterally directed pursuit. The results provide behavioral support for the physiologically and anatomic-based conclusion that NRTP is a component of a cortico-ponto-cerebellar circuit that presumably involves the pursuit area of the frontal eye field (FEF) and projects to ocular motor-related areas of the cerebellum. This FEF-NRTP-cerebellum path would parallel a middle and medial superior temporal cerebral cortical area-dorsolateral pontine nucleus-cerebellum pathway also known to be involved with regulating smooth-pursuit eye movements.

Smooth-pursuit eye movements elicited by first-order and second-order motion

The perception of the displacement of luminance-defined contours (i.e., first-order motion) is an important and well-examined function of the visual system. It can be explained, for example, by the operation of elementary motion detectors (EMDs), which cross-correlate the spatiotemporal luminance distribution. More recent studies using second-order motion stimuli, i.e., shifts of the distribution of features such as contrast, texture, flicker, or motion, extended classic concepts of motion perception by including nonlinear or hierarchical processing in the EMD. Smooth-pursuit eye movements can be used as a direct behavioral probe for motion processing. The ability of the visual system to extract motion signals from the spatiotemporal changes of the retinal image can be addressed by analyzing the elicited eye movements. We measured the eye movement response to moving objects defined by two different types of first-order motion and two different types of second-order motion. Our results clearly showed that the direction of smooth-pursuit eye movements was always determined by the direction of object motion. In particular, in the case of second-order motion stimuli, smooth-pursuit did not follow the retinal image motion. The latency of the initial saccades during pursuit of second-order stimuli was slightly but significantly increased, compared with the latency of saccades elicited by first-order motion. The processing of second-order motion in the peripheral visual field was less exact than the processing of first-order motion in the peripheral field. Steady state smooth-pursuit eye speed did not reflect the velocity of second-order motion as precisely as that of first-order motion, and the resulting retinal error was compensated by saccades. Interestingly, for slow second-order stimuli we observed that the eye could move faster than the target, leading to small, corrective saccades in the opposite direction to the ongoing smooth-pursuit eye movement. We conclude from our results that both visual perception and the control of smooth-pursuit eye movements have access to processing mechanisms extracting first- and second-order motion.

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.

Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey.

1. Anatomical and single-unit recording studies suggest that the dorsolateral pontine nucleus (DLPN) in monkey is a major link in the projection of descending visual motion information to the cerebellum. Such studies coupled with cortical and cerebellar lesion results suggest a major role for this basilar pontine region in the mediation of smooth-pursuit eye movements. 2. To provide more direct evidence that this pontine region is involved in the control of smooth-pursuit eye movements, focal chemical lesions were made in DLPN in the vicinity of previously recorded visual motion and pursuit-related neurons. Eye movement responses were subsequently recorded in these lesioned animals under several behavioral paradigms. 3. A major deficit in smooth-pursuit performance was produced after unilateral DLPN lesions generated either reversibly with lidocaine or more permanently with ibotenic acid. Pursuit impairments were observed during steady-state tracking of sinusoidal target motion as well as during the initiation of pursuit tracking to sudden ramp target motion. Through the use of the latter technique, initial eye acceleration was reduced to less than one-half of normal for animals with large lesions of the dorsolateral and lateral pontine nuclei. 4. The pursuit deficit in all animals was directional in nature and was not dependent on the visual hemifield in which the motion stimulus occurred. The largest effect for horizontal tracking occurred in all animals for pursuit directed ipsilateral to the lesion. Animals also showed major deficits in one or both directions of vertical pursuit, although the primary direction of the vertical impairment was variable from animal to animal. 5. Chemical lesions in the DLPN also produced comparable deficits in the initiation of optokinetic-induced smooth eye movements in the ipsilateral direction. In contrast to this effect on the initial optokinetic response, in the one lesioned animal studied during prolonged constant velocity optokinetic drum rotation, smooth eye speed increased slowly over a 10- to 15-s period to reach a level that closely matched drum speed. These results suggest that pathways outside the DLPN can generate the steady-state optokinetic response. 6. Saccades to stationary targets were normal after DLPN lesions, but corrective saccades made to targets moving in the direction ipsilateral to the lesion were much more hypometric than similar prelesion control saccades. 7. The pursuit deficits produced by lidocaine injections recovered within 30 min. The ibotenic acid deficits were maximal approximately 1 day after the injection and recovered rapidly thereafter over a time period of 3-7 days.(ABSTRACT TRUNCATED AT 400 WORDS)

The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity.

1. Purkinje cell activity was recorded from lobules VI and VII of the cerebellar vermis during the performance of visuooculomotor tasks designed to dissociate the signals related to head, smooth-pursuit eye, and retinal image movements. Task-related modulations in the simple spike discharge rates of 157 cells were observed in three alert monkeys. 2. Of 65 Purkinje cells that were completely tested for all three signals, all exhibited smooth-pursuit eye movement-related activity. An additional vestibular or visual response was observed in 17 and 11% of the cells, respectively. Eye, head, and retinal image velocity signals were all recorded in the same unit in 52% of the Purkinje cells. The responses of 5% of the fully tested cells were associated with changes in the direction of eye, head, and retinal image movement. 3. The observed sensorioculomotor responses were direction selective in 98% of the Purkinje cells. For the Purkinje cells that were fully tested, 60% of the cells exhibited peak discharge rates for ipsilateral and 40% for contralateral eye velocity. Of these Purkinje cells, 45% exhibited eye, head, and retinal image velocity signals with equivalent direction preferences. 4. Of 42 Purkinje cells tested, 88% demonstrated some kinds of interactive responses during combined eye and sensory stimulation. The interaction of eye and head velocity signals has been discussed in a companion paper (38). The modulation in discharge rate observed during tracking in the presence of a random dot background pattern could be predicted from the dissociated responses to smooth pursuit in the dark and to movements of the background pattern during suppression of eye movements. 5. The sensitivity to smooth-pursuit eye velocity averaged 1.4 times the sensitivity to head velocity. In 80% of the Purkinje cells, however, the sensitivity to eye velocity exceeded the sensitivity to head velocity by an average of only 10%. The sensitivity to smooth-pursuit eye velocity averaged 1.6 times the sensitivity to retinal image velocity. 6. An increase in Purkinje cell discharge rate was observed during the open-loop period of the initiation of smooth-pursuit eye movements. This open-loop response was consistent with the presence of a visual signal during ocular pursuit, since these cells were also shown to be responsive to a dissociated retinal image velocity signal. Furthermore, the magnitude of the open-loop response indicated an enhancement of the sensitivity to retinal image velocity when visual information became behaviorally significant.(ABSTRACT TRUNCATED AT 400 WORDS)

The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. I. Eye and head movement-related activity.

1. The observation of smooth-pursuit eye and retinal image velocity signals in lobules VI and VII of the vermis has given rise to the hypothesis that a neural correlate of a target velocity signal exists in this region of the cerebellum (29). However, activity signaling head velocity is also required to regenerate a target velocity signal. Vermal Purkinje cell activity was, therefore, recorded during the performance of paradigms designed to dissociate head movement-related responses. 2. The activity of 107 Purkinje cells was found to be related to horizontal head velocity. Of these, 52% increased their discharge rate for ipsilaterally directed passive head movement (type I), and 48% were excited by contralateral head movements (type II). 3. In five Purkinje cells in which sufficient data were obtained, cell discharge rate increased monotonically with head velocity over the range of 5-40 deg/s. The sensitivity to head velocity at 0.4 Hz +/- 25 deg/s averaged approximately 0.5 spikes.s-1/deg.s-1 in a larger sample of cells (n = 39). The sensitivities to head velocity, at this same frequency and velocity, of type I and type II Purkinje cells were comparable at 0.44 and 0.51 spikes.s-1/deg.s-1, respectively. 4. The Purkinje cell responses led head velocity by an average of 12 degrees at 0.4 Hz +/- 25 deg/s of passive head rotation. The phase shifts associated with type I and II responses were similar with phase leads of 13 and 9 degrees with respect to head velocity, respectively. 5. A linear interaction of smooth-pursuit eye and head velocity signals was observed during the performance of a variety of antiphase and inphase eye and head movement paradigms. The results support the conclusion that some Purkinje cells in lobules VI and VII of the cerebellar vermis encode a gaze velocity signal. Contributions of the head velocity signal to the regeneration of target velocity are considered in a companion paper (32).