Supranuclear Ocular Motor Systems

Properly functioning eye movements facilitate a clear, stable view of the environment. Saccadic eye movements and nystagmus fast phases are 2 types of fast eye movements. Slow eye movements include smooth pursuit, vestibular, optokinetic, and vergence. Reflexive and voluntary conjugate eye movements incorporate cortical, subcortical (basal ganglia), and vestibulocerebellar input to the final common pathways of horizontal and vertical eye movements. The present chapter reviews the anatomy and dysfunction of the supranuclear input to conjugate gaze.

Fixational eye movement waveforms in amblyopia: Characteristics of fast and slow eye movements

Fixational eye movements comprise of fast microsaccades alternating with slow inter-saccadic drifts. These physiologic eye movements play an important role in visual perception. Amblyopic patients are known to have fixation instability, particularly of the amblyopic eye. We examined eye movement abnormalities that contribute to this instability. We found that fixation stability is affected by the presence of fusion maldevelopment nystagmus (FMN). However, some amblyopes can have nystagmus without nasally directed slow phases and reversal in direction of the quick phase on ocular occlusion, features seen in FMN. In patients without nystagmus, we found increased amplitude of fixational saccades and inter-saccadic drifts. We categorized amblyopia patients by type (anisometropic, strabismic, or mixed) and eye movement waveform (no nystagmus, nystagmus without FMN, and FMN). We found specific fast and slow eye movement abnormalities of the fellow and amblyopic eye during fellow, amblyopic and both eyes viewing conditions across eye movement waveforms and types of amblyopia. These eye movement abnormalities can serve as biomarkers that can predict the impact of amblyopia as measured by visual acuity and stereopsis. Evaluation of fixational eye movements in amblyopia could be important to diagnose these common eye diseases and predict treatment effectiveness.

Functional diversity of motoneurons in the oculomotor system

Extraocular muscles contain two types of muscle fibers according to their innervation pattern: singly innervated muscle fibers (SIFs), similar to most skeletal muscle fibers, and multiply innervated muscle fibers (MIFs). Morphological studies have revealed that SIF and MIF motoneurons are segregated anatomically and receive different proportions of certain afferents, suggesting that while SIF motoneurons would participate in the whole repertoire of eye movements, MIF motoneurons would contribute only to slow eye movements and fixations. We have tested that proposal by performing single-unit recordings, in alert behaving cats, of electrophysiologically identified MIF and SIF motoneurons in the abducens nucleus. Our results show that both types of motoneuron discharge in relation to eye position and velocity, displaying a tonic–phasic firing pattern for different types of eye movement (saccades, vestibulo-ocular reflex, vergence) and gaze-holding. However, MIF motoneurons presented an overall reduced firing rate compared with SIF motoneurons, and had significantly lower recruitment threshold and also lower eye position and velocity sensitivities. Accordingly, MIF motoneurons could control mainly gaze in the off-direction, when less force is needed, whereas SIF motoneurons would contribute to increase muscle tension progressively toward the on-direction as more force is required. Anatomically, MIF and SIF motoneurons distributed intermingled within the abducens nucleus, with MIF motoneurons being smaller and having a lesser somatic synaptic coverage. Our data demonstrate the functional participation of both MIF and SIF motoneurons in fixations and slow and phasic eye movements, although their discharge properties indicate a functional segregation.

Closed loop motor-sensory dynamics in human vision

Vision is obtained with a continuous motion of the eyes. The kinematic analysis of eye motion, during any visual or ocular task, typically reveals two (kinematic) components: saccades, which quickly replace the visual content in the retinal fovea, and drifts, which slowly scan the image after each saccade. While the saccadic exchange of regions of interest (ROIs) is commonly considered to be included in motor-sensory closed-loops, it is commonly assumed that drifts function in an open-loop manner, that is, independent of the concurrent visual input. Accordingly, visual perception is assumed to be based on a sequence of open-loop processes, each initiated by a saccade-triggered retinal snapshot. Here we directly challenged this assumption by testing the dependency of drift kinematics on concurrent visual inputs using real-time gaze-contingent-display. Our results demonstrate a dependency of the trajectory on the concurrent visual input, convergence of speed to condition-specific values and maintenance of selected drift-related motor-sensory controlled variables, all strongly indicative of drifts being included in a closed-loop brain-world process, and thus suggesting that vision is inherently a closed-loop process.Author summaryOur eyes do not function like cameras; it has long been known that we are actively scanning our visual environment in order to see. Moreover, it is commonly accepted that our fast eye movements, saccades, are controlled by the brain and are affected by the sensory input. However, our slow eye movements, the ocular drifts, are often ignored when visual acquisition is analyzed. Accordingly, visual processing is typically assumed to be based on computations performed on saccade-triggered snapshots of the retinal state. Our work strongly challenges this model and provides significant evidence for an alternative model, a cybernetic one. We show that the dynamics of the ocular drifts do not allow, and cannot be explained by, open loop visual acquisition. Instead, our results suggest that visual acquisition is part of a closed-loop process, which dynamically and continuously links the brain to its environment.

Pursuit disorder and saccade dysmetria after caudal fastigial inactivation in the monkey

The caudal fastigial nuclei (cFN) are the output nuclei by which the medio-posterior cerebellum influences the production of saccadic and pursuit eye movements. We investigated the consequences of unilateral inactivation on the pursuit eye movement made immediately after an interceptive saccade toward a centrifugal target. We describe here the effects when the target moved along the horizontal meridian with a 10 or 20°/s speed. After muscimol injection, the monkeys were unable to track the present location of the moving target. During contralesional tracking, the velocity of postsaccadic pursuit was reduced. This slowing was associated with a hypometria of interceptive saccades such that gaze direction always lagged behind the moving target. No correlation was found between the sizes of saccade undershoot and the decreases in pursuit speed. During ipsilesional tracking, the effects on postsaccadic pursuit were variable across the injection sessions, whereas the interceptive saccades were consistently hypermetric. Here also, the ipsilesional pursuit disorder was not correlated with the saccade hypermetria either. The lack of correlation between the sizes of saccade dysmetria and changes of postsaccadic pursuit speed suggests that cFN activity exerts independent influences on the neural processes generating the saccadic and slow eye movements. It also suggests that the cFN is one locus where the synergy between the two motor categories develops in the context of tracking a moving visual target. We explain how the different fastigial output channels can account for these oculomotor tracking disorders. NEW & NOTEWORTHY Inactivation of the caudal fastigial nucleus impairs the ability to track a moving target. The accuracy of interceptive saccades and the velocity of postsaccadic pursuit movements are both altered, but these changes are not correlated. This absence of correlation is not compatible with an impaired common command feeding the circuits producing saccadic and pursuit eye movements. However, it suggests an involvement of caudal fastigial nuclei in their synergy to accurately track a moving target.

Motor action of the frontal eye field on the eyes and neck in the monkey

Focal stimulation in the frontal eye field (FEF) evoked eye movements that were often accompanied by neck movements. Experiments were performed with concurrent recording of both movements in trained monkeys. We recorded neck forces under a head-restrained condition with a force-measuring system. With the system, we measured forces along the x-, y-, and z-axes and torque about the z-axis. Torque about the z-axis that represented yaw rotation of the head was significantly affected by stimulation. We found that stimulation generated two types of motor actions of the eyes and neck. In the first type, contraversive neck forces were evoked by stimulation of the medial part of the FEF, where contraversive saccadic eye movements with large amplitudes were evoked. When the stimulus intensity was increased, saccades were evoked in an all-or-none manner, whereas the amplitude of neck forces increased gradually. In the second type, contraversive neck forces were evoked by stimulation of the medial and caudal part of the FEF, where ipsiversive slow eye movements were evoked. The depth profiles of amplitudes of neck forces were almost parallel to those of eye movements in individual stimulation tracks. The present results suggest that the FEF is involved in the control of motor actions of the neck as well as the eyes. The FEF area associated with contraversive saccades and contraversive neck movements may contribute to a gaze shift process, whereas that associated with ipsiversive slow eye movements and contraversive neck movements may contribute to a visual stabilization process. NEW & NOTEWORTHY Focal stimulation in the frontal eye field (FEF) evoked eye and neck movements. We recorded neck forces under a head-restrained condition with a force-measuring system. Taking advantage of this approach, we could analyze slow eye movements that were dissociated from the vestibuloocular reflex. We found ipsiversive slow eye movements in combination with contraversive neck forces, suggesting that the FEF may be a source of a corollary discharge signal for compensatory eye movements during voluntary neck movements.

Learning the trajectory of a moving visual target and evolution of its tracking in the monkey

An object moving in the visual field triggers a saccade that brings its image onto the fovea. It is followed by a combination of slow eye movements and catch-up saccades that try to keep the target image on the fovea as long as possible. The accuracy of this ability to track the “here-and-now” location of a visual target contrasts with the spatiotemporally distributed nature of its encoding in the brain. We show in six experimentally naive monkeys how this performance is acquired and gradually evolves during successive daily sessions. During the early exposure, the tracking is mostly saltatory, made of relatively large saccades separated by low eye velocity episodes, demonstrating that accurate (here and now) pursuit is not spontaneous and that gaze direction lags behind its location most of the time. Over the sessions, while the pursuit velocity is enhanced, the gaze is more frequently directed toward the current target location as a consequence of a 25% reduction in the number of catch-up saccades and a 37% reduction in size (for the first saccade). This smoothing is observed at several scales: during the course of single trials, across the set of trials within a session, and over successive sessions. We explain the neurophysiological processes responsible for this combined evolution of saccades and pursuit in the absence of stringent training constraints. More generally, our study shows that the oculomotor system can be used to discover the neural mechanisms underlying the ability to synchronize a motor effector with a dynamic external event.