Julie Quinet

Fastigial oculomotor region and the control of foveation during fixation.

When primates maintain their gaze directed toward a visual target (visual fixation), their eyes display a combination of miniature fast and slow movements. An involvement of the cerebellum in visual fixation is indicated by the severe gaze instabilities observed in patients suffering from cerebellar lesions. Recent studies in non-human primates have identified a cerebellar structure, the fastigial oculomotor region (FOR), as a major cerebellar output nucleus with projections toward oculomotor regions in the brain stem. Unilateral inactivation of the FOR leads to dysmetric visually guided saccades and to an offset in gaze direction when the animal fixates a visual target. However, the nature of this fixation offset is not fully understood. In the present work, we analyze the inactivation-induced effects on fixation. A novel technique is adopted to describe the generation of saccades when a target is being fixated (fixational saccades). We show that the offset is the result of a combination of impaired saccade accuracy and an altered encoding of the foveal target position. Because they are independent, we propose that these two impairments are mediated by the different projections of the FOR to the brain stem, in particular to the deep superior colliculus and the pontomedullary reticular formation. Our study demonstrates that the oculomotor cerebellum, through the activity in the FOR, regulates both the amplitude of fixational saccades and the position toward which the eyes must be directed, suggesting an involvement in the acquisition of visual information from the fovea.

Influence of background illumination on fixation and visually guided saccades in the rhesus monkey

The influence of background illumination on saccades towards small target LEDs was examined in three rhesus monkeys. In darkness, fixational saccades and those aimed at horizontal targets had a trajectory that was biased upward. This bias was not observed in the illuminated condition. For horizontal saccades, the magnitude of the vertical final errors depended on target eccentricity relative to starting eye position. Downward saccades undershot the location where eye position landed in the illuminated condition whereas upward saccades overshot less eccentric targets. Background illumination also influenced the latency of saccades. The change in accuracy that affects large saccades is interpreted as resulting from a change in the encoding of the desired displacement signal that feeds the local feedback loop controlling saccade trajectory.

Cognitive regulation of saccadic velocity by reward prospect.

It is known that expectation of reward speeds up saccades. Past studies have also shown the presence of a saccadic velocity bias in the orbit, resulting from a biomechanical regulation over varying eccentricities. Nevertheless, whether and how reward expectation interacts with the biomechanical regulation of saccadic velocities over varying eccentricities remains unknown. We addressed this question by conducting a visually guided double‐step saccade task. The role of reward expectation was tested in monkeys performing two consecutive horizontal saccades, one associated with reward prospect and the other not. To adequately assess saccadic velocity and avoid adaptation, we systematically varied initial eye positions, saccadic directions and amplitudes. Our results confirmed the existence of a velocity bias in the orbit, i.e., saccadic peak velocity decreased linearly as the initial eye position deviated in the direction of the saccade. The slope of this bias increased as saccadic amplitudes increased. Nevertheless, reward prospect facilitated velocity to a greater extent for saccades away from than for saccades toward the orbital centre, rendering an overall reduction in the velocity bias. The rate (slope) and magnitude (intercept) of reward modulation over this velocity bias were linearly correlated with amplitudes, similar to the amplitude‐modulated velocity bias without reward prospect, which presumably resulted from a biomechanical regulation. Small‐amplitude (≤ 5°) saccades received little modulation. These findings together suggest that reward expectation modulated saccadic velocity not as an additive signal but as a facilitating mechanism that interacted with the biomechanical regulation.

Visuo-motor deficits induced by fastigial nucleus inactivation

The contribution of the cerebellar vermal lobules VIc/VII and of the caudal part of the fastigial nucleus (cFN) to the control of saccadic eye movements has been established by converging neurophysiological approaches. The precise delineation of these saccade-related territories in the medio-posterior cerebellum (MPC) has stimulated the development of detailed investigations of its output nucleus, the cFN. In the present paper, we review recent studies that describe the deficits of the saccadic displacement of the line of sight (gaze) induced by a reversible cFN inactivation under different experimental situations (head restrained, head-unrestrained or body-unrestrained). These data first indicate that the MPC does not solely influence the generation of saccadic eye movements but also the accompanying head movements during saccadic shifts of gaze in the head-unrestrained animal. They also support, in agreement with anatomical data, a distributed influence of the MPC on several levels of the sensory-motor system for orienting gaze, rather than a limited control of the immediate pre-motor structures.

Cerebellar control of saccade dynamics: contribution of the fastigial oculomotor region.

The fastigial oculomotor region is the output by which the medioposterior cerebellum influences the generation of saccades. Recent inactivation studies reported observations suggesting an involvement in their dynamics (velocity and duration). In this work, we tested this hypothesis in the head-restrained monkey with the electrical microstimulation technique. More specifically, we studied the influence of duration, frequency, and current on the saccades elicited by fastigial stimulation and starting from a central (straight ahead) position. The results show ipsilateral or contralateral saccades whose amplitude and dynamics depend on the stimulation parameters. The duration and amplitude of their horizontal component increase with the duration of stimulation up to a maximum amplitude. Varying the stimulation frequency mostly changes their latency and the peak velocity (for contralateral saccades). Current also influences the metrics and dynamics of saccades: the horizontal amplitude and peak velocity increase with the intensity, whereas the latency decreases. The changes in peak velocity and in latency observed in contralateral saccades are not correlated. Finally, we discovered that contralateral saccades can be evoked at sites eliciting ipsilateral saccades when the stimulation frequency is reduced. However, their onset is timed not with the onset but with the offset of stimulation. These results corroborate the hypothesis that the fastigial projections toward the pontomedullary reticular formation (PMRF) participate in steering the saccade, whereas the fastigiocollicular projections contribute to the bilateral control of visual fixation. We propose that the cerebellar influence on saccade generation involves recruiting neurons and controlling the size of the active population in the PMRF.

Electrical Microstimulation of the Fastigial Oculomotor Region in the Head-Unrestrained Monkey

It has been shown that inactivation of the caudal fastigial nucleus (cFN) by local injection of muscimol leads to inaccurate gaze shifts in the head-unrestrained monkey and that the gaze dysmetria is primarily due to changes in the horizontal amplitude of eye saccades in the orbit. Moreover, changes in the relationship between amplitude and duration are observed for only the eye saccades and not for the head movements. These results suggest that the cFN output primarily influences a neural network involved in moving the eyes in the orbit. The present study further tested this hypothesis by examining whether head movements could be evoked by electrical microstimulation of the saccade-related region in the cFN. Long stimulation trains (200-300 ms) evoked staircase gaze shifts that were ipsi- or contralateral, depending on the stimulated site. These gaze shifts were small in amplitude and were essentially accomplished by saccadic movements of the eyes. Head movements were observed in some sites but their amplitudes were very small (mean=2.4 degrees). The occurrence of head movements and their amplitude were not enhanced by increasing stimulation frequency or intensity. In several cases, electrically evoked gaze shifts exhibited an eye-head coupling that was different from that observed in visually triggered gaze shifts. This study provides additional observations suggesting that the saccade-related region in the cFN modulates the generation of eye movements and that the deep cerebellar output region involved in influencing head movements is located elsewhere.

Does the Brain Extrapolate the Position of a Transient Moving Target

When an object moves in the visual field, its motion evokes a streak of activity on the retina and the incoming retinal signals lead to robust oculomotor commands because corrections are observed if the trajectory of the interceptive saccade is perturbed by a microstimulation in the superior colliculus. The present study complements a previous perturbation study by investigating, in the head-restrained monkey, the generation of saccades toward a transient moving target (100–200 ms). We tested whether the saccades land on the average of antecedent target positions or beyond the location where the target disappeared. Using target motions with different speed profiles, we also examined the sensitivity of the process that converts time-varying retinal signals into saccadic oculomotor commands. The results show that, for identical overall target displacements on the visual display, saccades toward a faster target land beyond the endpoint of saccades toward a target moving slower. The rate of change in speed matters in the visuomotor transformation. Indeed, in response to identical overall target displacements and durations, the saccades have smaller amplitude when they are made in response to an accelerating target than to a decelerating one. Moreover, the motion-related signals have different weights depending upon their timing relative to the target onset: early signals are more influential in the specification of saccade amplitude than later signals. We discuss the “predictive” properties of the visuo-saccadic system and the nature of this location where the saccades land, after providing some critical comments to the “hic-et-nunc” hypothesis (Fleuriet and Goffart, 2012). SIGNIFICANCE STATEMENT Complementing the work of Fleuriet and Goffart (2012), this study is a contribution to the more general scientific research aimed at understanding how ongoing action is dynamically and adaptively adjusted to the current spatiotemporal aspects of its goal. Using the saccadic eye movement as a probe, we provide results that are critical for investigating and understanding the neural basis of motion extrapolation and prediction.

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.