Effects of voluntary blinks on saccades,vergence eye movements,and saccade-vergence interactions in humans

Blinks are known to change the kinematic properties of horizontal saccades, probably by influencing the saccadic premotor circuit. The neuronal basis of this effect could be explained by changes in the activity of omnipause neurons in the nucleus raphe interpositus or in the saccade-related burst neurons of the superior colliculus. Omnipause neurons cease discharge during both saccades and vergence movements. Because eyelid blinks can influence both sets of neurons, we hypothesized that blinks would influence the kinematic parameters of saccades in all directions, vergence, and saccade-vergence interactions. To test this hypothesis, we investigated binocular eye and lid movements in five normal healthy subjects with the magnetic search coil technique. The subjects performed conjugate horizontal and vertical saccades from gaze straight ahead to targets at 20 degrees up, down, right, or left while either attempting not to blink or voluntarily blinking. While following the same blink instruction, subjects made horizontal vergence eye movements of 7 degrees and combined saccade-vergence movements with a version amplitude of 20 degrees. The movements were performed back and forth from two targets simultaneously presented nearby (38 cm) and more distant (145 cm). Small vertical saccades accompanied most vergence movements. These results show that blinks change the kinematics (saccade duration, peak velocity, peak acceleration, peak deceleration) of not only horizontal but also of vertical saccades, of horizontal vergence eye movements, and of combined saccade-vergence eye movements. Peak velocity, acceleration, and deceleration of eye movements were decreased on the average by 30%, and their duration increased by 43% on the average when they were accompanied by blinks. The blink effect was time dependent with respect to saccade and vergence onset: the greatest effect occurred 100 ms prior to saccade onset, whereas there was no effect when the blink started after saccade onset. The effects of blinks on saccades and vergence, which are tightly coupled to latency, support the hypothesis that blinks cause profound spatiotemporal perturbations of the eye movements by interfering with the normal saccade/vergence premotor circuits. However, the measured effect may to a certain degree but not exclusively be explained by mechanical interference.     

Directional asymmetry during combined saccade-vergence movements

We investigated relationships between saccadic and vergence components of gaze shifts as 10 human subjects switched visual fixation between targets aligned in the midsagittal plane that lay in different vertical directions and at different distances. When fixation was shifted between a higher distant target and a lower near target, peak convergence velocity followed peak vertical saccadic velocity by a median interval of 12 ms. However, when fixation was shifted between a lower distant target and a higher near target, peak convergence velocity followed peak vertical saccadic velocity by a median interval of 76 ms. For the 2 stimulus arrangements, the median intervals by which peak divergence velocity followed the peak vertical saccadic velocity were 4 and 20 ms, respectively. The dissociation interval between the peak velocities of convergence and upward saccades increased with vertical saccade size, required convergence angle, and elevation of the endpoint of the movement. Velocity waveforms of vergence responses were more skewed when peak velocity was closely associated with saccadic peak velocity than when the vergence responses were delayed. Convergence peak velocities did not vary in any consistent pattern, but divergence peak velocities were generally smaller with responses that were delayed. Vergence movements were accompanied by small, high-frequency conjugate oscillations, suggesting that omnipause neurons were inhibited for both types of responses. In conclusion, the present findings indicate that the dynamic properties of horizontal vergence movements depend on the direction and timing of vertical saccades; these findings suggest experimental tests for current models of saccade-vergence interaction.     

Saccade-vergence interactions in macaques. II. Vergence enhancement as the product of a local feedback vergence motor error and a weighted saccadic burst

In the accompanying paper we reported that intrasaccadic vergence enhancement during combined saccade-vergence eye movements reflects saccadic dynamics, which implies the involvement of saccadic burst signals. This involvement was not predicted by the Multiply Model of Zee et al. We propose a model wherein vergence enhancement is the result of a multiplicative interaction between a weighted saccadic burst signal and a nonvisual short-latency estimate of the vergence motor error at the time of the saccade. The enhancement of vergence velocity by saccades causes the vergence goal to be approached more rapidly than if no saccade had occurred. The adjustment of the postsaccadic vergence velocity to this faster reduction in vergence motor error occurred with a time course too fast for visual feedback. This implies the presence of an internal estimate of the progress of the movement and indicates that vergence responses are under the control of a local feedback mechanism. It also implies that the vergence enhancement signal is included in the vergence feedback loop and is an integral part of the vergence velocity command. Our multiplicative model is able to predict the peak velocity of the vergence enhancement as a function of cyclopean saccadic dynamics, smooth vergence dynamics, and saccade-vergence timing with remarkable precision. It performed equally well for both horizontal and vertical saccades with very similar parameters, suggesting a common mechanism for all saccadic directions. A saccade-vergence additive model is also presented, although it would require external switching elements. Possible neural implementations are discussed.     

Blink effects on ongoing smooth pursuit eye movements in humans

Blinks are known to affect eye movements, e.g., saccades, slow and fast vergence, and saccade-vergence interaction, in two ways: by superimposition of blink-associated eye movements and changes of the central premotor activity in the brainstem. The goal of this study was to determine, for the first time, the effects of trigeminal evoked blinks on ongoing smooth pursuit eye movements which could be related to visual sensory or premotor neuronal changes. This was compared to the effect of a target disappearing for 100–300 ms duration during ongoing smooth pursuit (blank paradigm) in order to control for the visual sensory effects of a blink. Eye and blink movements were recorded in eight healthy subjects with the scleral search coil technique. Blink-associated eye movements during the first 50% of the blink duration were non-linearly superimposed on the smooth pursuit eye movements. Immediately after the blink-associated eye movements, the pursuit velocity slowly decreased by an average of 3.2±2.1°/s. This decrease was not dependent on the stimulus direction. The pursuit velocity decrease caused by blinks which occluded the pupil more than 50% could be explained mostly by blanking the visual target. However, small blinks that did not occlude the pupil (<10% of lid closure) also decreased smooth pursuit velocity. Thus, this blink effect on pursuit velocity cannot be explained by blink-associated eye movements or by the blink having blanked the visual input. We propose that part of this effect might either be caused by incomplete visual suppression during blinks and/or a change in the activity of omnipause neurons.     

The effect of microstimulation of the oculomotor vermis on discharges of fastigial neurons and visually-directed saccades in macaques

The present study confirmed our previous reports that neurons in the fastigial oculomotor region (FOR) of the macaque show presaccadic bursts during contralateral saccades and that the burst duration is closely related to the duration of the accompanying saccade. Furthermore, when the burst duration was reduced by subthreshold electrical stimulation applied to the oculomotor vermis prior to the onset of the burst, the impending visually-directed saccade became hypometric. The reduction in the burst duration was closely related to the degree of the hypometria. Since saccadic burst neurons in the FOR constitute the sole output channel for saccadic signals of the oculomotor vermis, the findings support the hypothesis that the cerebellum can regulate the amplitude of eye movements.     

Saccade-related activity in the fastigial oculomotor region of the macaque monkey during spontaneous eye movements in light and darkness

Saccade-related burst neurons were recorded in the caudal part of the fastigial nucleus (fastigial oculomotor region) during spontaneous eye movements and fast phases of optokinetic and vestibular nystagmus in light and darkness from three macaque monkeys. All neurons (n=47) were spontaneously active and exhibited a burst of activity with each saccade and fast phase of nystagmus. Most neurons (n=31) only exhibited a burst of activity, whereas those remaining also exhibited a pause in firing rate before or after the burst. Burst parameters varied considerably for similar saccades. For horizontal saccades all neurons, except for three, had a preferred direction with an earlier onset of burst activity to the contralateral side. For contralateral saccades the burst started on average 17.5 ms before saccade onset, whereas the average lead-time for ipsilateral saccades was only 6.5 ms. Three neurons were classified as isotropic with similar latencies and peak burst activity in all directions. None of the neurons had a preferred direction with an earlier onset of burst activity to the ipsilateral side. Burst duration increased with saccade amplitude, whereas peak burst activity was not correlated with amplitude. There was no relationship between peak burst activity and peak eye velocity. In the dark, neurons generally continued to burst with each saccade and fast phase of nystagmus. Burst for saccades in the dark was compared with burst for saccades of similar amplitude and direction in the light. Saccades in the dark had a longer duration and peak burst activity was reduced on average to 62% (range 36–105%). In three neurons a burst in the dark was no longer clearly distinguishable above the ongoing spontaneous activity. These data suggest that the saccade-related burst neurons in the FOR modify saccadic profiles by directly influencing acceleration and deceleration, respectively, of individual eye movements. This could be achieved by an input to the inhibitory and excitatory burst neurons of the saccadic burst generator in the brainstem. From neuroanatomical studies it is known that FOR neurons project directly to the brainstem regions containing the immediate premotor structures for saccade generation.     

Saccade-vergence interactions in humans.

1. We recorded eye movements in four normal human subjects during refixations between targets calling for various combinations of saccades and vergence. We confirmed and extended prior observations of 1) transient changes in horizontal ocular alignment during both pure horizontal saccades (relative divergence followed by relative convergence) and pure vertical saccades (usually divergence for upward and convergence for downward saccades); 2) occasional, high-frequency (20-25 Hz), conjugate oscillations along the axis orthogonal to the main saccade; and 3) the speeding up of horizontal vergence by both horizontal and vertical saccades. 2. To interpret these findings, we developed a hypothesis for the generation of vergence to step changes in target depth, both with and without associated saccades. The essential features of this hypothesis are 1) the transient changes in horizontal ocular alignment during pure horizontal saccades reflect asymmetries in the mechanical properties of the lateral and medial rectus muscles causing adduction to lag abduction; 2) pure vergence movements in response to step changes in target depth are generated by a neural network that uses a desired change in vergence position as its input command and instantaneous vergence motor error (the difference between the desired change and the actual change in vergence) to drive vergence premoter neurons; and 3) the facilitation of horizontal vergence by saccades arises from nonlinear interactions in central premotor circuits. 3. The hypothetical network for generating pure vergence to step changes in target depth is analogous in structure to the local feedback model for the generation of saccades and has the same conceptual appeal. With the assumption of a single nonlinearity describing the relationship between a vergence motor error signal and the output of the neurons that generate promoter vergence velocity commands, this model generates pure vergence movements with peak velocity-amplitude relationships and trajectories that closely match those of experimental data. 4. Several types of models are proposed for the central, nonlinear interaction that occurs when saccades and vergence are combined. Common to all models is the idea that omnidirectional pause neurons (OPN), which are thought to gate activity for saccade burst neurons, also gate activity for saccade-related vergence. In one model we hypothesize the existence of a separate class of saccade-related vergence burst neurons, which generate premotor horizontal vergence commands but only during saccades. In a second model we hypothesize separate right eye and left eye saccadic burst neurons that receive not only conjugate, but also equal but oppositely directed vergence error signals.(ABSTRACT TRUNCATED AT 400 WORDS)     

Saccadic and smooth pursuit eye movements: computational modeling of a common inhibitory mechanism in brainstem

The oculomotor system coordinates different types of eye movements in order to orient the visual axis, including saccade and smooth pursuit,. It was traditionally thought that the premotor pathways for these different eye movements are largely separate. In particular, a group of midline cells in the pons called omnipause neurons were considered to be part of only the saccadic system. Recent experimental findings have shown activity modulation of these brainstem premotor neurons during both kinds of eye movements. In this study, we propose a new computational model of the brainstem circuitry underlying the generation of saccades and smooth pursuit eye movements. Similar models have been developed earlier, but mainly looking at pure saccades. Here, we integrated recent neurophysiological findings on omnipause neuron activity during smooth pursuit. Our computational model can mimic some new experimental findings as the similarity of "eye velocity profile" with "omnipause neuron pattern of activity" in pursuit movement. We showed that pursuit neuron activity is augmented during catch-up saccades; this increment depends on the initial pursuit velocity in catch-up saccade onset. We conclude that saccadic and pursuit components of catch-up saccades are added to each other nonlinearly.     

Stimulation in the rostral pole of monkey superior colliculus: effects on vergence eye movements

Recent studies have indicated that the superior colliculus (SC), traditionally considered to be saccade-related, may play a role in the coding of eye movements in both direction and depth. Similarly, it has been suggested that omnidirectional pause neurons are not only involved in the initiation of saccades, but can also modulate vergence eye movements. These new developments provide a challenge for current oculomotor models that attempt to describe saccade-vergence coordination and the neural mechanisms that may be involved. In this paper, we have attempted to study these aspects further by investigating the role of the rostral pole of the SC in the control of vergence eye movements. It is well-known that, by applying long-duration electrical stimulation to rostral sites in the monkey SC, saccadic responses can be prevented and interrupted. We have made use of these properties to extend this paradigm to eye movements that contain a substantial depth component. We found that electrical intervention in the rostral region also has a clear effect on vergence. For an eye movement to a near target, stimulation leads to a significant suppression and change in dynamics of the pure vergence response during the period of stimulation, but the depth component cannot be prevented entirely. When these paradigms are implemented for 3D refixations, the saccade is inactivated, as expected, while the vergence component is often suppressed more than in the case of the pure vergence. The data lead us to conclude that the rostral SC, presumably indirectly via connections with the pause neurons, can affect vergence control for both pure vergence and combined 3D responses. Suppression of the depth component is incomplete, in contrast to the directional movement, and is often different in magnitude for 3D refixations and pure vergence responses. The results are discussed in connection with current models for saccade-vergence interaction.     

The brain stem saccadic burst generator encodes gaze in three-dimensional space

When we look between objects located at different depths the horizontal movement of each eye is different from that of the other, yet temporally synchronized. Traditionally, a vergence-specific neuronal subsystem, independent from other oculomotor subsystems, has been thought to generate all eye movements in depth. However, recent studies have challenged this view by unmasking interactions between vergence and saccadic eye movements during disconjugate saccades. Here, we combined experimental and modeling approaches to address whether the premotor command to generate disconjugate saccades originates exclusively in "vergence centers." We found that the brain stem burst generator, which is commonly assumed to drive only the conjugate component of eye movements, carries substantial vergence-related information during disconjugate saccades. Notably, facilitated vergence velocities during disconjugate saccades were synchronized with the burst onset of excitatory and inhibitory brain stem saccadic burst neurons (SBNs). Furthermore, the time-varying discharge properties of the majority of SBNs (>70%) preferentially encoded the dynamics of an individual eye during disconjugate saccades. When these experimental results were implemented into a computer-based simulation, to further evaluate the contribution of the saccadic burst generator in generating disconjugate saccades, we found that it carries all the vergence drive that is necessary to shape the activity of the abducens motoneurons to which it projects. Taken together, our results provide evidence that the premotor commands from the brain stem saccadic circuitry, to the target motoneurons, are sufficient to ensure the accurate control shifts of gaze in three dimensions.     

A new local feedback model of the saccadic burst generator

1. To accommodate the finding that the superior colliculus is an important input to the brain stem pathways that generate saccades (the saccadic burst generator), a new model of the burst generator is proposed. Unlike the model of Robinson (61) from which it was derived, the model attempts to match a neural replica of change in eye position, which is the output of the burst generator, to a neural replica of change in target position, which is the output of the colliculus and the input to the model. 2. The elements of the model correspond to neurons known or thought to be associated with the actual primate saccadic burst generator and are mostly connected together in accord with the results of anatomical and physiological experiments. 3. The model was simulated on a digital computer to compare its behavior with that of the actual burst generator under normal and experimental conditions. Simulated peak burst frequency and saccade duration matched that obtained from monkey excitatory burst neurons and inhibitory burst neurons for saccades up to 15 degrees but did not match at larger sizes; stimulation of the omnipause neurons caused an interruption of the saccade, and the saccade resumed at the end of stimulation as in actual data; the model can generate the abnormally long-duration saccades seen under decreased alertness or various pathologies by changing the burst generator inputs and without having to change any properties of the neurons themselves or their connections; a simulated horizontal and vertical burst generator pair connected only through the omnipause neurons can generate realistic oblique saccades. 4. The implications of the model for higher-order control of the saccadic burst generator are discussed.     

Dynamic coding of vertical facilitated vergence by premotor saccadic burst neurons

To redirect our gaze in three-dimensional space we frequently combine saccades and vergence. These eye movements, known as disconjugate saccades, are characterized by eyes rotating by different amounts, with markedly different dynamics, and occur whenever gaze is shifted between near and far objects. How the brain ensures the precise control of binocular positioning remains controversial. It has been proposed that the traditionally assumed "conjugate" saccadic premotor pathway does not encode conjugate commands but rather encodes monocular commands for the right or left eye during saccades. Here, we directly test this proposal by recording from the premotor neurons of the horizontal saccade generator during a dissociation task that required a vergence but no horizontal conjugate saccadic command. Specifically, saccadic burst neurons (SBNs) in the paramedian pontine reticular formation were recorded while rhesus monkeys made vertical saccades made between near and far targets. During this task, we first show that peak vergence velocities were enhanced to saccade-like speeds (e.g., >150 vs. <100 degrees/s during saccade-free movements for comparable changes in vergence angle). We then quantified the discharge dynamics of SBNs during these movements and found that the majority of the neurons preferentially encode the velocity of the ipsilateral eye. Notably, a given neuron typically encoded the movement of the same eye during horizontal saccades that were made in depth. Taken together, our findings demonstrate that the brain stem saccadic burst generator encodes integrated conjugate and vergence commands, thus providing strong evidence for the proposal that the classic saccadic premotor pathway controls gaze in three-dimensional space.     

Pontine omnipause activity during conjugate and disconjugate eye movements in macaques

Previous reports have shown that saccades executed during vergence eye movements are often slower and longer than conjugate saccades. Lesions in the nucleus raphe interpositus, where pontine omnipause neurons (OPNs) are located, were also shown to result in slower and longer saccades. If vergence transiently suppresses the activity of the OPNs just before a saccade, then reduced presaccadic activity might mimic the behavioral effects of a lesion. To test this hypothesis, 64 OPNs were recorded from 7 alert rhesus monkeys during smooth vergence and saccades with and without vergence. The firing rate of many OPNs was modulated by static vergence angle but not by version and showed transient changes during slow vergence without saccades. This modulation was smooth, and not the abrupt pause seen for saccades, indicating that OPNs do not act as gates for vergence commands. We confirmed that saccades made during both convergence and divergence are significantly slower and longer than conjugate saccades. OPNs paused for all saccades, and the pause lead (interval between pause onset and saccadic onset) was significantly longer for saccades with convergence, in agreement with our hypothesis. Contrary to our hypothesis, pause lead was not longer for saccades with divergence, even though these saccades were slowed as much as those occurring during convergence. Furthermore, there was no significant correlation, on a trial-by-trial basis, between pause lead and saccadic slowing. These results suggest that it is unlikely that presaccadic slowing of OPNs is responsible for the slower saccades seen during vergence movements.     

Saccade-vergence interactions in macaques. I. Test of the omnipause Multiply Model

Horizontal vergence eye movements are movements in opposite directions used to change fixation between far and near targets. The occurrence of a saccade during vergence causes vergence velocity to be transiently enhanced. The goal of this study was to test in the monkey the previously described Multiply Model (Zee et al. 1992) that holds that, in humans, the speeding of vergence during a saccade may be the result of the disinhibition of a subgroup of vergence-related neurons by the saccadic omnipause neurons (OPNs). In agreement with the Multiply Model: 1) the onset of the enhancement was closely related to saccadic onset, and thus linked to the onset of the OPN pause; 2) the magnitude of the vergence velocity enhancement was strongly dependent on saccade-vergence timing. Contrary to the Multiply Model: 1) the peak of the vergence velocity enhancement was dependent on saccadic peak velocity; 2) the dependency on saccadic peak velocity was not the indirect result of a dependency on saccadic duration and therefore on the duration of the OPN pause; 3) the decline of the vergence enhancement, identified by the time of the peak of the enhancement velocity, occurred too early to be linked to the end of the OPN pause; 4) vergence enhancement had a saccadic-like peak-velocity/size main sequence. Overall, the evidence is incompatible with the OPN Multiply hypothesis of vergence enhancement. Alternative models are described in an accompanying paper.     

Eye movement related neurons in the cerebellar nuclei of the alert monkey

Summary In all cerebellar nuclei saccade related neurons can be recorded. In the alert untrained Rhesus monkey these neurons can be classified into short-lead bursters, complex bursters, and tonic burst neurons. Short-lead bursters can be related to the onset or to the length of saccades and blinks. Complex bursters are active in the early (acceleration) or late (deceleration) phase of saccades. Tonic burst neurons, in addition, display maintained activity which is modulated in a complex manner with eye position, during periods of fixation or slow-phase nystagmus. In agreement with clinical and previous experimental data we view these cerebellar output neurons as elements which are not part of the system which basically generates eye movements, but rather as a system which could influence the execution of movements.     

Saccadic adaptation in lateral medullary and cerebellar infarction

To determine the adaptive capability of saccadic eye movements, and its association with enduring saccadic dysmetria in cerebellar and lateral medullary infarction (LMI), we investigated saccadic accuracy and adaptation in 15 patients with cerebellar or lateral medullary infarction, compared with those of 7 patients with diffuse cerebellar atrophy and 11 normal subjects. Saccade adaptation was elicited by a 37.5% backward target step during the primary saccade in both horizontal directions. Horizontal preadaptive saccadic gains were decreased in patients with cerebellar infarction, and contralesionally in patients with LMI. In contrast, adaptive saccadic gain change was reduced in patients with diffuse cerebellar atrophy and cerebellar infarction. Saccadic hypometria and reduced saccadic adaptability were dissociated in the majority of the patients with cerebellar infarctions; seven of the eight patients with cerebellar infarction showed saccadic hypometria and only three of them showed reduced saccadic adaptation, uni- or bilaterally in two with bilateral infarctions and ipsilesionally in one with unilateral infarction. The most commonly affected structure on MRI was the cerebellar hemisphere in the patients either with saccadic hypometria or with reduced saccadic adaptation. All patients with unilateral LMI exhibited normal saccadic gain adaptation in both directions, including those patients with enduring saccadic ipsipulsion. Our results suggest that the cerebellar hemispheres as well as the dorsal vermis and fastigial nucleus may be involved in the control of saccadic accuracy and adaptation. Reduced saccadic adaptation and persisting dysmetria are not tightly linked to each other in the cerebellar or lateral medullary lesions.     

Tests of two hypotheses to account for different-sized saccades during disjunctive gaze shifts

Rapid shifts of the point of visual fixation between objects that lie in different directions and at different depths require disjunctive eye movements. We tested whether the saccadic component of such movements is equal for both eyes (Hering’s law) or is unequal. We compared the saccadic pulses of abducting and adducting movements when horizontal gaze was shifted from a distant to a near target aligned on the visual axis of one eye (Müller paradigm) in ten normal subjects. We similarly compared horizontal saccades made between two distant targets lying in the same field of movement as during the Müller paradigm tests, and between targets lying symmetrically on either side of the midline, at near side of the midline, at near or far. We measured the ratio of the amplitude of the movements of each eye in corresponding directions due to the saccadic component, as well as corresponding ratios of peak velocity and peak acceleration. In response to a Müller test paradigm requiring about 17° of vergence, the change in position of the unaligned eye was typically twice the size of the corresponding movement of the aligned eye. The ratio of peak velocities for the unaligned/aligned eyes was about 1.5, which was greater than for saccades made between distant targets. The ratio of peak acceleration for unaligned/aligned eyes was about 1.0 during shifts from near to far and about 1.3 for shifts from far to near, these values being similar to corresponding ratios for saccades between distant targets. These measurements of peak acceleration indicate that the saccadic pulses sent to each eye during the Müller paradigm are more equal than would be deduced by comparing the changes in eye position. We retested five subjects to compare directly the peak acceleration of saccades made during the Müller paradigm with similar-sized ”conjugate” saccades made between targets at optical infinity. Saccades made during the Müller paradigm were significant slower (P<0.005) than similar-sized conjugate saccades; this indicated that the different-sized movements during Müller paradigm are not simply due differences in saccadic pulse size but are also influenced by the concurrent vergence movement. A model for saccade-vergence interactions, which incorporates equal saccadic pulses for each eye, and differing contributions from convergence and divergence, accounts for many of these findings. Received: 31 December 1998 / Accepted: 14 July 1999     

Cerebellar control of saccadic eye movements: its neural mechanisms and pathways

Microstimulation studies on monkeys have shown that the cerebellar cortex which is related to saccadic function is located in lobules VIc and VII of the vermis. This vermal area is designated as the oculomotor vermis and characterized by low thresholds (less than 10 microA) and by saccade-related neuronal activity. The saccade evoked by the vermal stimulation has been shown to be the result of activation of Purkinje-cell axons. On the other hand, an anterograde WGA-HRP transport study has indicated that the Purkinje-cell axons of the oculomotor vermis terminate almost exclusively in a fatigial region which is designated as the fastigial oculomotor region (FOR). Microstimulation of the oculomotor vermis and the ventromedial aspect of the FOR results in saccades which differ in their horizontal directions, with vermal stimulation resulting in ipsilateral and fastigial stimulation resulting in contralateral saccades. Since the ipsilateral saccades evoked from the caudal part of the FN were suppressed by bicuculline, they were the results of stimulation of the Purkinje axons. It has been also shown that stimulation of the oculomotor vermis causes inhibition of FOR neurons. Furthermore, fastigial neurons bursting with saccades can be recorded only within the anatomical confines of the FOR. These data are consistent with the concept that signals from the vermis are transmitted to the saccadic nuclei of the brainstem via the FOR. Neurons in the FOR have been shown to project to various saccade-related nuclei, including the riMLF and PPRF. Some neurons in the FOR have divergent axon collaterals which terminate in both the vertical and horizontal preoculomotor nuclei. When the initial eye position is changed by stimulating the FN prior to visually-guided saccades, monkeys cannot compensate for the stimulation-induced movement. When the stimulation is delived 75-130 ms after the target presentation, saccades are triggered prematurely. The visuomotor processing for saccades seems to be completed during this period, which is approximately half the latency of normal saccades. When saccades were triggered prematurely at an early stage of information processing, the eyes moved first in the direction of evoked saccade and then changed the direction toward the location of the target without any intervening period. The retinal error information sampled before the stimulation was not disturbed by the cerebellar stimulation. These observations suggest that cerebellar output impulses are projected downstream to saccade-programming circuits where visual information has already been converted into motor-command signals. The cerebellum is a domain for parallel processing of visuomotor information.     

Burst discharges of fastigial neurons in macaque monkeys are driven by vision- and memory-guided saccades but not by spontaneous saccades.

Discharges from 61 saccadic burst neurons in the fastigial oculomotor region were recorded for two trained macaque monkeys during vision-guided or memory-guided saccades or spontaneous saccades in the dark. Although these neurons exhibited vigorous, burst discharges during both vision-guided and memory-guided saccades, only weak bursts were observed during spontaneous saccades in the dark. Especially in 10 of the 61 neurons, saccadic burst discharge was almost completely absent during spontaneous saccades in the dark. These findings suggest that the cerebellum plays an important role in the control of vision-guided saccades as well as memory-guided saccades, but not of spontaneous saccades in the dark.     

Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys

1. The discharge of 255 neurons in the fastigial nuclei of three trained macaque monkeys was investigated during visually guided saccades. Responses of these neurons were examined also during horizontal head rotation and during microstimulation of the oculomotor vermis (lobules VIc and VII). 2. One hundred and two units were characterized by bursts of firing in response to visually guided saccades. Ninety-eight of these (96.1%) were located within the anatomic confines of the fastigial oculomotor region (FOR), on the basis of reconstruction of recording sites. During contralateral saccades, these neurons showed bursts that preceded the onset of saccades (presaccadic burst), whereas, during ipsilateral saccades, they showed bursts associated with the end of saccades (late saccadic burst). They were hence named saccadic burst neurons. Sixty-one saccadic burst neurons (62.2%) were inhibited during microstimulation of the oculomotor vermis with currents less than 10 microA. 3. All saccadic burst neurons were spontaneously active, and the resting firing rate varied considerably among units, ranging from 10 to 50 imp/s. The tonic levels of activity did not correlate significantly with eye position. 4. The presaccadic burst started 18.5 +/- 4.7 (SD) ms (n = 45) before the onset of saccades in the optimal direction (the direction associated with the maximum values of burst lead time, number of spikes per burst, and burst duration). Optimal directions covered the entire contralateral hemifield, although there was a slightly higher incidence in both horizontal and upper-oblique directions in the present sample. The duration of the presaccadic burst was highly correlated with the duration of saccade (0.85 less than or equal to r less than or equal to 0.97). 5. The late saccadic burst was most robust in the direction opposite to the optimal in each unit (the nonoptimal direction). Its onset preceded the completion of ipsilateral saccade by 30.4 +/- 5.9 ms. The lead time to the end of saccade was consistent among different units and was constant also for saccades of various sizes. Thus the late saccadic burst started even before the saccade onset when the saccade duration was less than 30 ms. Unlike the presaccadic burst, its duration was not related to the duration of saccade. 6. Discharge rates of saccadic burst neurons were correlated neither to eye positions during fixation nor to the initial eye positions before saccades. 7. Eye-position units and horizontal head-velocity units were located rostral to the FOR.(ABSTRACT TRUNCATED AT 400 WORDS)