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A long-standing belief holds that the saccadic and smooth-pursuit eye movement systems are composed of largely separate premotor circuits, at least in the brainstem. One crucial prediction predicated on this belief is that the tonic discharge of omnipause neurons (OPNs), which are thought to be part of only the saccadic system, should not be modulated during pursuit eye movements. This report shows that the discharge of OPNs, in contradiction, is modulated downward during pursuit movements. In contrast to their behavior during saccades, where they pause completely for the duration of the movement, the downward modulation during pursuit did not totally silence OPNs. The depth of the downward modulation was correlated with the speed of the ongoing pursuit movement. Another type of cell, which we have named saccade/pursuit neurons, was recorded in the paramedian pontine reticular formation near the location of OPNs. This subpopulation of burst cells discharged a cascade of spikes for saccades in a preferred direction. They also displayed a lower-frequency sustained discharge of spikes for the duration of pursuit in the same preferred direction. These data suggest a new type of combined model for the organization of the brainstem saccade/pursuit system. In this new combined model, the OPNs form a common inhibitory mechanism for both types of movements, and the saccade/pursuit neurons participate in the eye-velocity modulation of OPN discharge or membrane polarization during either type of movement.

The premotor pathways subserving saccades and smooth-pursuit eye movements are usually thought to be different. Indeed, saccade and smooth-pursuit eye movements have different dynamics and functions. In particular, a group of midline cells in the pons called omnipause neurons (OPNs) are considered to be part of the saccadic system only. It has been established that OPNs keep premotor neurons for saccades under constant inhibition during fixation periods. Saccades occur only when the activity of OPNs has completely stopped or paused. Accordingly, electrical stimulation in the region of OPNs inhibits premotor neurons and interrupts saccades. The premotor relay for smooth pursuit is thought to be organized differently and omnipause neurons are not supposed to be involved in smooth-pursuit eye movements. To investigate this supposition, OPNs were recorded during saccades and during smooth pursuit in the monkey (Macaca mulatta). Unexpectedly, we found that neuronal activity of OPNs decreased during smooth pursuit. The resulting activity reduction reached statistical significance in approximately 50% of OPNs recorded during pursuit of a target moving at 40 degrees /s. On average, activity was reduced by 34% but never completely stopped or paused. The onset of activity reduction coincided with the onset of smooth pursuit. The duration of activity reduction was correlated with pursuit duration and its intensity was correlated with eye velocity. Activity reduction was observed even in the absence of catch-up saccades that frequently occur during pursuit. Electrical microstimulation in the OPNs' area induced a strong deceleration of the eye during smooth pursuit. These results suggest that OPNs form an inhibitory mechanism that could control the time course of smooth pursuit. This inhibitory mechanism is part of the fixation system and is probably needed to avoid reflexive eye movements toward targets that are not purposefully selected. This study shows that saccades and smooth pursuit, although they are different kinds of eye movements, are controlled by the same inhibitory system.

Saccades are typically separated by inter-saccadic fixation intervals (ISFIs) of > or =125 ms. During this time, the saccadic system selects a goal and completes the preparatory processes required prior to executing the subsequent movement. However, in tasks in which competing stimuli are presented, two sequentially executed movements to different goals can be separated by much shorter ISFIs. This suggests that the saccadic system is capable of completing many of the preparatory requirements for a second saccade concurrently with the execution of an initial movement. We recorded single neurons in the superior colliculus (SC) during rapid saccade sequences made by rhesus monkeys performing a search task. We found that during the execution of an initial saccade, activity related to the goal of a quickly following second saccade can be simultaneously maintained in the SC motor map. This activity appears to signal the selection or increased salience of the second saccade goal even before the initial saccade has ended. For movements separated by normal ISFIs (> or =125 ms), we did not observe activity related to concurrent processing, presumably because for these longer ISFI responses, the goal of the second saccade is not selected until after the end of the first saccade. These results indicate that, at the time of an initial saccade, the SC does not necessarily act as a strict winner-take-all network. Rather it appears that the salience of a second visual goal can be simultaneously maintained in the SC. This provides evidence that selection or preparatory activity related to the goal of a second saccade can overlap temporally with activity related to an initial saccade and indicates that such concurrent processing is present even in a structure which is fairly close to the motor output.

1. The discharge of neurons in the deeper layers of the monkey superior colliculus was recorded during saccades made to stationary and to smoothly moving visual targets. 2. All neurons that discharged for saccades made to stationary targets also discharged during saccades made to moving targets, but there was a systematic shift in the saccade vector yielding maximal activity (i.e. center of the movement field) of collicular neurons for the latter class of movements. The shift moved the center of the movement fields toward larger-amplitude pursuit saccades for target motion away from the fovea, in comparison with saccades made to stationary targets. However, the discharge at the center of the movement field for pursuit saccades was 14% lower when averaged over the sample of recorded cells. 3. The saccades made during pursuit tracking of moving visual stimuli have different dynamics than saccades made to stationary targets. At similar amplitudes pursuit saccades are slower, and their velocity profiles often show secondary velocity peaks or inflection points and have longer-duration decelerating phases. 4. The combined experimental observations of a change in saccade dynamics and the shift in movement fields in collicular neurons for pursuit saccades are compatible with the hypothesis that saccades made to moving targets are controlled by neural processing in two partially separate pathways. In this theory, one path is concerned with correction of a presaccadic retinal position error (a path that includes the colliculus) and another path is concerned with position extrapolations based on the velocity of the moving target (a path that does not include the colliculus).

The cerebellum is known to participate in visually guided eye movements. The cerebellar uvula receives projections from pontine nuclei that have been implicated in visual motion processing and the generation of smooth pursuit. Single-unit and lesion studies were conducted to determine how the uvula might further process these input signals. Purkinje cells and input fibers were recorded during a variety of visual and oculomotor paradigms. Most Purkinje cells were modulated in either an excitatory or inhibitory fashion by prolonged, horizontal optokinetic drum rotation. A small proportion of cells responded during smooth tracking of a small spot of light. As a paradox to the physiological data, lesions of the uvula produced a profound effect on smooth-pursuit eye movements. Initial eye velocity for pursuit in the direction contraversive to the lesion site was increased substantially following lesions in comparison with prelesion controls. The lesions also affected optokinetic nystagmus in the direction contraversive to the lesion, but not as drastically as they did pursuit. Overall the results suggest that the uvula is not in the neuronal pathway that directly controls pursuit, but instead serves to adjust the gain of this system as a result of abnormal periods of motion of the visual world.

To define predictive behavior and mechanisms in visual smooth pursuit, various target motions were presented to 2 monkeys. Target stimuli included: single sinusoids (1's), triangle waves (T's), sums of 4 nonharmonically related sinusoids (4's), bandpass limited white noise (B's), and wideband white noise (N's). Velocity error was least for 1's, greatest for N's, and intermediate for T's, 4's, and B's. For the bandlimited 4's and B's, monkeys demonstrated the greatest relative amplitude response at the highest frequencies. Predictive mechanisms are classified as short- and long-term, depending on how much past target motion information is employed. The T's and a modification of this stimulus pattern involving a random perturbation were used to test the hypothesis that prediction is based exclusively on short-term signal processing related to target position and its derivatives. The existence of long-term predictive mechanisms in monkey smooth pursuit was unequivocally demonstrated with the use of the latter stimulus.

This article reviews the current state of knowledge of the primate smooth-pursuit system. The emphasis is on the neuronal mechanisms and pathways that control pursuit eye movements in the monkey. The review covers the neuronal structures believed to be involved in pursuit generation from striate cortex to the final premotoneuron structures in the brainstem. Information gathered from physiological and anatomical work is stressed.

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)

Smooth pursuit eye movements in the monkey were studied by measuring the average eye acceleration in the first 100 msec of the ocular response to suddenly moving constant velocity discrete visual targets. The tracking target's motion was initiated on or eccentric to the fovea against a very dimly lit homogeneous background or an illuminated, highly textured, large-field background. The effect of the textured background was always to reduce the initial eye acceleration as compared to that present in the homogeneous background case. Movement of the background in the opposite direction to target spot movement also reduced the initial eye acceleration. In contrast, steady-state tracking measured several hundred msec after the onset of pursuit under the same conditions was only marginally reduced by the presence of the textured background.

The central nervous system is a parallel dynamical system which connects sensory input with motor output for the performance of visual tracking. This paper applies elementary control system tools to extend dynamical neural network models to the visual smooth pursuit system. Observed eye position responses to target motions and characteristics of the plant (eye muscles and orbital mechanics) place dynamical constraints on the interposed neural network controller. In the process of constructing a model for the controller, we show two previous pursuit system models, using efference copy and feedforward compensation, are equivalent from an input-output standpoint. We introduce a controller model possessing a potentially highly parallel implementation and offer an example with supporting neural firing rate data. Changes in time delays or other system dynamics are expected to lead to compensatory adaptive changes in the controller. A scheme to noninvasively simulate such changes in system dynamics was developed. Actual physiologic data of adaptive responses to increased time delay is presented as an example of the utility of this parallel controller. Compensatory changes in our parallel controller model are easily predicted. These results suggest a productive interaction between neural network modeling, neurophysiology, and control systems engineering.