Flexible interpretation of a decision rule by supplementary eye field neurons.

Since the environment is in constant flux, decision-making capabilities of the brain must be rapid and flexible. Yet in sensory motion processing pathways of the primate brain where decision making has been extensively studied, the flexibility of neurons is limited by inherent selectivity to motion direction and speed. The supplementary eye field (SEF), an area involved in decision making on moving stimuli, is not strictly a sensory or motor structure, and hence may not suffer such limitations. Here we test whether neurons in the SEF can flexibly interpret the rule of a go/nogo task when the decision boundary in the task changes with each trial. The task rule specified that the animal pursue a moving target with its eyes if and when the target entered a visible zone. The size of the zone was changed from trial to trial in order to shift the decision boundary, and thereby assign different go/nogo significance to the same motion trajectories. Individual SEF neurons interpreted the rule appropriately, signaling go or nogo in compliance with the rule and not the direction of motion. The results provide the first evidence that individual neurons in frontal cortex can flexibly interpret a rule that governs the decision to act.

Supplementary eye fields stimulation facilitates anticipatory pursuit.

Anticipatory movements are motor responses occurring before likely sensory events in contrast to reflexive actions. Anticipatory movements are necessary to compensate for delays present in sensory and motor systems. Smooth pursuit eye movements are often used as a paradigmatic example for the study of anticipation. However, the neural control of anticipatory pursuit is unknown. A previous study suggested that the supplementary eye fields (SEFs) could play a role in the guidance of smooth pursuit to predictable target motion. In this study, we favored anticipatory responses in monkeys by making the parameters of target motion highly predictable and electrically stimulated the SEF before and during this behavior. Stimulation sites were restricted to regions of the SEF where saccades could not be evoked at the same low currents. We found that electrical microstimulation in the SEF increased the velocity of anticipatory pursuit movements and decreased their latency. These effects will be referred to as anticipatory pursuit facilitation. The degree of facilitation was the largest if the stimulation train was delivered near the end of the fixation period, before the moment when anticipatory pursuit usually begins. No anticipatory smooth eye movements could be evoked during fixation without an expectation of target motion. These results suggest that the SEF pursuit area might be involved in the process of guiding anticipatory pursuit.

Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields.

The role of the supplementary eye fields (SEF) during smooth pursuit was investigated with electrical microstimulation. We found that stimulation in the SEF increased the acceleration and velocity of the eyes in the direction of target motion during smooth pursuit initiation but not during sustained pursuit. The increase in eye velocity during initiation will be referred to as pursuit facilitation and was observed at sites where saccades could not be evoked with the same stimulation parameters. On average, electrical stimulation increased eye velocity by approximately 20%. At most sites, the threshold for a significant facilitation was 50 microA with a stimulation frequency of 300 Hz. Facilitation of pursuit initiation depended on the timing of stimulation trains. The effect was most pronounced if the stimulation was delivered before smooth pursuit initiation. On average, eye velocity in stimulation trials increased linearly as a function of eye velocity in control trials, and this function had a slope greater than one, suggesting a multiplicative influence of the stimulation. Stimulation during a fixation task did not evoke smooth eye movements. The latency of catch-up saccades was increased during facilitation, but their accuracy was not affected. Saccades toward stationary targets were not affected by the stimulation. The results are further evidence that the SEF plays a role in smooth pursuit in addition to its known role in saccade planning and suggest that this role may be to control the gain of smooth pursuit during initiation. The covariance between pursuit facilitation and the timing of the catch-up saccade as a result of stimulation suggests that these different eye movements systems are coordinated to achieve a common goal.

Human smooth pursuit direction discrimination.

The smooth pursuit system is usually studied using single moving objects as stimuli. However, the visual motion system can respond to stimuli that must be integrated spatially and temporally (Williams DG, Sekuler R. Vision Res 1984;24:55-62; Watamaniuk SNJ, Sekuler R, Williams DW. Vision Res 1989;29:47-59). For example, when each dot of a random-dot cinematogram (RDC) is assigned a new direction of motion each frame from a narrow distribution of directions, the whole field of dots appears to move in the average direction (Williams and Sekuler, 1984). We measured smooth pursuit eye movements generated in response to small (10 deg diameter) RDCs composed of 250 dynamic random dots. Smooth eye movements were assessed by analyzing only the first 130 ms of eye movements after pursuit initiation (open-loop period). Comparing smooth eye movements to RDCs and single spot targets, we find that both targets generate similar responses confirming that the signal supplied to the smooth pursuit system can result from a spatial integration of motion information. In addition, the change in directional precision of smooth eye movements to RDCs with different amounts of directional noise was similar to that found for psychophysical direction discrimination. These results imply that the motion processing system responsible for psychophysical performance may also provide input to the oculomotor system.

Spatial integration in human smooth pursuit.

When viewing a moving object, details may appear blurred if the object's motion is not compensated for by the eyes. Smooth pursuit is a voluntary eye movement that is used to stabilize a moving object. Most studies of smooth pursuit have used small, foveal targets as stimuli (e.g. Lisberger SG and Westbrook LE. J Neurosci 1985;5:1662-1673.). However, in the laboratory, smooth pursuit is poorer when a small object is tracked across a background, presumably due to a conflict between the primitive optokinetic reflex and smooth pursuit. Functionally, this could occur if the motion signal arising from the target and its surroundings were averaged, resulting in a smaller net motion signal. We asked if the smooth pursuit system could spatially summate coherent motion, i.e. if its response would improve when motion in the peripheral retina was in the same direction as motion in the fovea. Observers tracked random-dot cinematograms (RDC) which were devoid of consistent position cues to isolate the motion response. Either the height or the density of the display was systematically varied. Eye speed at the end of the open-loop period was greater for cinematograms than for a single spot. In addition, eye acceleration increased and latency decreased as the size of the aperture increased. Changes in the density produced similar but smaller effects on both acceleration and latency. The improved pursuit for larger motion stimuli suggests that neuronal mechanisms subserving smooth pursuit spatially average motion information to obtain a stronger motion signal.

Single-neuron activity in the dorsomedial frontal cortex during smooth-pursuit eye movements to predictable target motion.

A region of dorsomedial frontal cortex (DMFC) has been implicated in planning and executing saccadic eye movements; hence it has been referred to as a supplementary eye field (SEF). Recently, activity related to executing smooth-pursuit eye movements has been recorded from the DMFC, and microstimulation here has been shown to evoke smooth eye movements. This report documents neuronal activity present in smooth-pursuit tasks where the predictability of target motion was manipulated. The activity of many neurons in the DMFC reached a peak when a predictable change in target motion occurred. Furthermore, the peak activity of some cells was systematically shifted by manipulating the duration of the target event, indicating that the network these neurons were in could learn the temporal characteristics of new target motion. Finally, the activity of most neurons tested was greater when target motion was predictable than when it was unpredictable. The results suggest that the DMFC participates in planning smooth-pursuit eye movements based on past stimulus history.

The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects.

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.

Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements.

This report describes the behavior of neurons in the dorsomedial frontal cortex during smooth pursuit eye movements. Single neurons were recorded from monkeys while they tracked a small target that moved from the center of a screen outward. The firing rate of most cells was modulated during smooth pursuit eye movements, and often the activity peaked around pursuit initiation. Visual motion of the small target with the eyes fixed could activate pursuit neurons, but did not account for the total pursuit response. Neurons were also selective for the direction in which the animal was tracking, indicating that they were linked to the generation of the eye movements, and not to non-specific arousal effects. The results suggest that the dorsomedial frontal cortex participates in initiating smooth pursuit. It is proposed that the dorsomedial frontal cortex is part of a partial alternative path to the classic pursuit pathway that might be used to facilitate the initiation or control of eye movements beyond a simple reflexive response to retinal slip.

Adaptation of saccades and fixation to bilateral foveal lesions in adult monkey.

Bilateral foveal lesions were made by laser photocoagulation in adult monkeys. One day post-lesion, animals fixated with a new retinal locus inferior to the fovea (in the visual field) that they used permanently. Fixation stability improved modestly over two days. Initially, saccades maladaptively brought the lesioned foveae to visual targets. Over at least several weeks, saccade trajectories gradually changed bringing targets to intact retina, although some animals never totally adapted. The slow time course of saccadic adaptation to foveal loss suggests a mechanism different from that documented in other studies of saccadic adaptation and from that used by the fixation system.

Characteristics of nystagmus evoked by electrical stimulation of the uvular/nodular lobules of the cerebellum in monkey.

Electrical stimulation in the monkey vestibulocerebellum has previously been shown to produce ocular nystagmus, but large stimulating current values were used. Using long duration (< or = 10-second) stimulus pulse trains and low current values (< 50 microA), we studied the nystagmus evoked by microstimulation in the uvular/nodular regions of the cerebellum. In doing this, we found quantitative differences in the nystagmus evoked from these two regions. Stimulation of the nodulus typically produced a vigorous nystagmus with a contralateral slow phase and a prolonged afternystagmus in the same direction. In contrast, stimulation of the uvula typically produced a regular ipsilateral nystagmus pattern with a very short, if any, afternystagmus in the same direction. In addition, at some stimulation sites in the uvula we observed an adaptation in the slow phase eye velocity during the time that the stimulation remained on. This effect could result in a secondary nystagmus, with a slow phase velocity direction opposite to that first evoked by the stimulation, followed by a prolonged afternystagmus in the direction of the secondary nystagmus at stimulus offset. The nystagmus evoked by these cerebellar stimulations differs from both natural nystagmus produced by large field visual motion and from the nystagmus produced by electrical stimulation of the nucleus of the optic tract. The nystagmus produced by uvular and nodular stimulation shows a shorter latency and a more rapid slow phase eye velocity buildup. The uvula stimulations also showed a much shorter afternystagmus. Also, the same nystagmus was evoked whether the animal was in a lighted or dark surround. These characteristics and recent single-unit recording studies in the uvula seem to suggest that the uvula acts not as a direct input to the velocity storage mechanism, but instead perhaps as part of an internal regulator for balance between the bilateral vestibular nuclei which are normally part of the nystagmus response. On the other hand, the nodulus, with its prolonged afternystagmus in the same direction as the evoked nystagmus, may be involved as a part of the velocity storage mechanism.

Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways.

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.

Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey.

Cells in the foveal representation of V1 cortex of adult primates became visually responsive after normal sensory input was removed. Immediately after fovea were lesioned bilaterally, a region was found where no cells' activity could be modulated by visual stimulation. Recordings made in that deafferented zone at greater than 2.5 months after lesions revealed that activity of over half of the cells could be modulated by visual stimuli presented to intact peripheral retina. Although response characteristics made cells with recovered driving quite unlike normal cells, the result suggests a level of visual cortical reorganization previously observed only in immature animals.