Eye Movements In Monkeys Research Articles

Sensorimotor-linked reward modulates smooth pursuit eye movements in monkeys.

Reward is essential for shaping behavior. Using sensory cues to imply forthcoming rewards, previous studies have demonstrated powerful effects of rewards on behavior. Nevertheless, the impact of reward on the sensorimotor transformation, particularly when reward is linked to behavior remains uncertain. In this study, we investigated how reward modulates smooth pursuit eye movements in monkeys. Three distinct associations between reward and eye movements were conducted in independent blocks. Results indicated that reward increased eye velocity during the steady-state pursuit, rather than during the initiation. The influence depended on the particular association between behavior and reward: a faster eye velocity was linked with reward. Neither rewarding slower eye movements nor randomizing rewards had a significant effect on behavior. The findings support the existence of distinct mechanisms involved in the initiation and steady-state phases of pursuit, and contribute to a deeper understanding of how reward interacts with these two periods of pursuit.

Decoding effects of psychoactive drugs in a high-dimensional space of eye movements in monkeys.

Oculomotor behavior has been shown to be correlated with mental disorders in clinics, making it promising for disease diagnosis. Here we developed a thorough oculomotor test toolkit, involving saccade, smooth pursuit, and fixation, allowing the examination of multiple oculomotor parameters in monkey models induced by psychoactive drugs. Eye movements were recorded after daily injections of phencyclidine (PCP) (3.0mg/kg), ketamine (0.8mg/kg) or controlled saline in two macaque monkeys. Both drugs led to robust reduction in accuracy and increment in reaction time during high cognitive-demanding tasks. Saccades, smooth pursuit, and fixation stability were also significantly impaired. During fixation, the involuntary microsaccades exhibited increased amplitudes and were biased toward the lower visual field. Pupillary response was reduced during cognitive tasks. Both drugs also increased sensitivity to auditory cues as reflected in auditory evoked potentials (AEPs). Thus, our animal model induced by psychoactive drugs produced largely similar abnormalities to that in patients with schizophrenia. Importantly, a classifier based on dimension reduction and machine learning could reliably identify altered states induced by different drugs (PCP, ketamine and saline, accuracy=93%). The high performance of the classifier was reserved even when data from one monkey were used for training and testing the other subject (averaged classification accuracy=90%). Thus, despite heterogeneity in baseline oculomotor behavior between the two monkeys, our model allows data transferability across individuals, which could be beneficial for future evaluation of pharmaceutical or physical therapy validity.

Microsaccades are directed toward the midpoint between targets in a variably cued attention task

Reliable, noninvasive biomarkers that reveal the internal state of a subject are an invaluable tool for neurological diagnoses. Small fixational eye movements, called microsaccades, are a candidate biomarker thought to reflect a subject's focus of attention [Z. M. Hafed, J. J. Clark, VisionRes. 42, 2533-2545 (2002); R. Engbert, R. Kliegl, VisionRes. 43, 1035-1045 (2003)]. The linkage between the direction of microsaccades and attention has mainly been demonstrated using explicit and unambiguous attentional cues. However, the natural world is seldom predictable and rarely provides unambiguous information. Thus, a useful biomarker must be robust to such changes in environmental statistics. To determine how well microsaccades reveal visual-spatial attention across behavioral contexts, we analyzed these fixational eye movements in monkeys performing a conventional change detection task. The task included two stimulus locations and variable cue validities across blocks of trials. Subjects were adept at the task, showing precise and graded modulations of visual attention for subtle target changes and performing better and faster when the cue was more reliable [J. P. Mayo, J. H. R. Maunsell, J. Neurosci.36, 5353 (2016)]. However, over tens of thousands of microsaccades, we found no difference in microsaccade direction between cued locations when cue variability was high nor between hit and miss trials. Instead, microsaccades were made toward the midpoint of the two target locations, not toward individual targets. Our results suggest that the direction of microsaccades should be interpreted with caution and may not be a reliable measure of covert spatial attention in more complex viewing conditions.

Multiple components in direction learning in smooth pursuit eye movements of monkeys.

We analyzed behavioral features of smooth pursuit eye movements to characterize the course of acquisition and expression of multiple neural components of motor learning. Monkeys tracked a target that began to move in an initial "pursuit" direction and suddenly, but predictably, changed direction after a fixed interval of 250 ms. As the trial is repeated, monkeys learn to make eye movements that predict the change in target direction. Quantitative analysis of the learned response revealed evidence for multiple, dynamic, parallel processes at work during learning. 1) The overall learning followed at least two trial courses: a fast component grew and saturated rapidly over tens of trials, and a slow component grew steadily over up to 1,000 trials. 2) The temporal specificity of the learned response within each trial was crude during the first 100 trials but then improved gradually over the remaining trials. 3) External influences on the gain of pursuit initiation modulate the expression but probably not the acquisition of learning. The gain of pursuit initiation and the expression of the learned response decreased in parallel, both gradually through a 1,000-trial learning block and immediately between learning trials with different gains in the initiation of pursuit. We conclude that at least two distinct neural mechanisms drive the acquisition of pursuit learning over 100 to 1,000 trials (3 to 30 min). Both mechanisms generate underlying memory traces that are modulated in relation to the gain of pursuit initiation before expression in the final motor output. NEW & NOTEWORTHY We show that cerebellum-dependent direction learning in smooth pursuit eye movements grows in at least two components over 1,100 behavioral learning repetitions. One component grows over tens of trials and the other over hundreds. Within trials, learned temporal specificity gradually improves over hundreds of trials. The expression of each learning component on a given trial can be modified by external factors that do not affect the underlying memory trace.

Smooth Pursuit Eye Movement of Monkeys Naive to Laboratory Setups With Pictures and Artificial Stimuli.

When animal behavior is studied in a laboratory environment, the animals are often extensively trained to shape their behavior. A crucial question is whether the behavior observed after training is part of the natural repertoire of the animal or represents an outlier in the animal’s natural capabilities. This can be investigated by assessing the extent to which the target behavior is manifested during the initial stages of training and the time course of learning. We explored this issue by examining smooth pursuit eye movements in monkeys naïve to smooth pursuit tasks. We recorded the eye movements of monkeys from the 1st days of training on a step-ramp paradigm. We used bright spots, monkey pictures and scrambled versions of the pictures as moving targets. We found that during the initial stages of training, the pursuit initiation was largest for the monkey pictures and in some direction conditions close to target velocity. When the pursuit initiation was large, the monkeys mostly continued to track the target with smooth pursuit movements while correcting for displacement errors with small saccades. Two weeks of training increased the pursuit eye velocity in all stimulus conditions, whereas further extensive training enhanced pursuit slightly more. The training decreased the coefficient of variation of the eye velocity. Anisotropies that grade pursuit across directions were observed from the 1st day of training and mostly persisted across training. Thus, smooth pursuit in the step-ramp paradigm appears to be part of the natural repertoire of monkeys’ behavior and training adjusts monkeys’ natural predisposed behavior.

Selective reward affects the rate of saccade adaptation

In this study we tested whether a selective reward could affect the adaptation of saccadic eye movements in monkeys. We induced the adaptation of saccades by displacing the target of a horizontal saccade vertically as the eye moved toward it, thereby creating an apparent vertical dysmetria. The repeated upward target displacement caused the originally horizontal saccade to gradually deviate upward over the course of several hundred trials. We induced this directional adaptation in both right- and leftward saccades in every experiment (n=20). In half of the experiments (n=10), we rewarded monkeys only when they made leftward saccades and in the other half (n=10) only for rightward saccades. The reaction time of saccades in the rewarded direction was shorter and we, like others, interpreted this change as a sign of the reward’s preferential effect in that direction. Saccades in the rewarded direction showed more rapid adaptation of their directions than did saccades in the non-rewarded direction, indicating that the selective reward increased the speed of saccade adaptation. The differences in adaptation speed were reflected in changes in saccade metrics, which were usually more noticeable in the deceleration phases of saccades than in their acceleration phases. Because previous studies have shown that the oculomotor cerebellum is involved with saccade deceleration and also participates in saccade adaptation, it is possible that selective reward could influence cerebellar plasticity.

Modulation of Complex-Spike Duration and Probability during Cerebellar Motor Learning in Visually Guided Smooth-Pursuit Eye Movements of Monkeys.

Activation of an inferior olivary neuron powerfully excites Purkinje cells via its climbing fiber input and triggers a characteristic high-frequency burst, known as the complex spike (CS). The theory of cerebellar learning postulates that the CS induces long-lasting depression of the strength of synapses from active parallel fibers onto Purkinje cells, and that synaptic depression leads to changes in behavior. Prior reports showed that a CS on one learning trial is linked to a properly timed depression of simple spikes on the subsequent trial, as well as a learned change in pursuit eye movement. Further, the duration of a CS is a graded instruction for single-trial plasticity and behavioral learning. We now show across multiple learning paradigms that both the probability and duration of CS responses are correlated with the magnitudes of neural and behavioral learning in awake behaving monkeys. When the direction of the instruction for learning repeatedly was in the same direction or alternated directions, the duration and probability of CS responses decreased over a learning block along with the magnitude of trial-over-trial neural learning. When the direction of the instruction was randomized, CS duration, CS probability, and neural and behavioral learning remained stable across time. In contrast to depression, potentiation of simple-spike firing rate for ON-direction learning instructions follows a longer time course and plays a larger role as depression wanes. Computational analysis provides a model that accounts fully for the detailed statistics of a complex set of data.

Differential Contribution of Low- and High-level Image Content to Eye Movements in Monkeys and Humans.

Oculomotor selection exerts a fundamental impact on our experience of the environment. To better understand the underlying principles, researchers typically rely on behavioral data from humans, and electrophysiological recordings in macaque monkeys. This approach rests on the assumption that the same selection processes are at play in both species. To test this assumption, we compared the viewing behavior of 106 humans and 11 macaques in an unconstrained free-viewing task. Our data-driven clustering analyses revealed distinct human and macaque clusters, indicating species-specific selection strategies. Yet, cross-species predictions were found to be above chance, indicating some level of shared behavior. Analyses relying on computational models of visual saliency indicate that such cross-species commonalities in free viewing are largely due to similar low-level selection mechanisms, with only a small contribution by shared higher level selection mechanisms and with consistent viewing behavior of monkeys being a subset of the consistent viewing behavior of humans.

Loss of Afferent Vestibular Input Produces Central Adaptation and Increased Gain of Vestibular Prosthetic Stimulation.

Implanted vestibular neurostimulators are effective in driving slow phase eye movements in monkeys and humans. Furthermore, increases in slow phase velocity and electrically evoked compound action potential (vECAP) amplitudes occur with increasing current amplitude of electrical stimulation. In intact monkeys, protracted intermittent stimulation continues to produce robust behavioral responses and preserved vECAPs. In lesioned monkeys, shorter duration studies show preserved but with somewhat lower or higher velocity behavioral responses. It has been proposed that such changes are due to central adaptive changes in the electrically elicited vestibulo-ocular reflex (VOR). It is equally possible that these differences are due to changes in the vestibular periphery in response to activation of the vestibular efferent system. In order to investigate the site of adaptive change in response to electrical stimulation, we performed transtympanic gentamicin perfusions to induce rapid changes in vestibular input in monkeys with long-standing stably functioning vestibular neurostimulators, disambiguating the effects of implantation from the effects of ototoxic lesion. Gentamicin injection was effective in producing a large reduction in natural VOR only when it was performed in the non-implanted ear, suggesting that the implanted ear contributed little to the natural rotational response before injection. Injection of the implanted ear produced a reduction in the vECAP responses in that ear, suggesting that the intact hair cells in the non-functional ipsilateral ear were successfully lesioned by gentamicin, reducing the efficacy of stimulation in that ear. Despite this, injection of both ears produced central plastic changes that resulted in a dramatically increased slow phase velocity nystagmus elicited by electrical stimulation. These results suggest that loss of vestibular afferent activity, and a concurrent loss of electrically elicited vestibular input, produces an increase in the efficacy of a vestibular neurostimulator by eliciting centrally adapted behavioral responses without concurrent adaptive increase of galvanic afferent activation in the periphery.

A physiological perspective on fixational eye movements

For a behavioral neuroscientist, fixational eye movements are a double-edged sword. On one edge, they make control of visual stimuli difficult, but on the other edge they provide insight into the ways the visual system acquires information from the environment. We have studied macaque monkeys as models for human visual systems. Fixational eye movements of monkeys are similar to those of humans but they are more often vertically biased and spatially more dispersed. Eye movements scatter stimuli from their intended retinal locations, increase variability of neuronal responses, inflate estimates of receptive field size, and decrease measures of response amplitude. They also bias against successful stimulation of extremely selective cells. Compensating for eye movements reduced these errors and revealed a fine-grained motion pathway from V1 feeding the cortical ventral stream. Compensation is a useful tool for the experimenter, but rather than compensating for eye movements, the brain utilizes them as part of its input. The saccades and drifts that occur during fixation selectively activate different types of V1 neurons. Cells that prefer slower speeds respond during the drift periods with maintained discharges and tend to have smaller receptive fields that are selective for sign of contrast. They are well suited to code small details of the image and to enable our fine detailed vision. Cells that prefer higher speeds fire transient bursts of spikes when the receptive field leaves, crosses, or lands on a stimulus, but only the most transient ones (about one-third of our sample) failed to respond during drifts. Voluntary and fixational saccades had very similar effects, including the presence of a biphasic extraretinal modulation that interacted with stimulus-driven responses. Saccades evoke synchronous bursts that can enhance visibility but these bursts may also participate in the visual masking that contributes to saccadic suppression. Study of the small eye movements of fixation may illuminate some of the big problems in vision.

Role of plasticity at different sites across the time course of cerebellar motor learning.

Learning comprises multiple components that probably involve cellular and synaptic plasticity at multiple sites. Different neural sites may play their largest roles at different times during behavioral learning. We have used motor learning in smooth pursuit eye movements of monkeys to determine how and when different components of learning occur in a known cerebellar circuit. The earliest learning occurs when one climbing-fiber response to a learning instruction causes simple-spike firing rate of Purkinje cells in the floccular complex of the cerebellum to be depressed transiently at the time of the instruction on the next trial. Trial-over-trial depression and the associated learning in eye movement are forgotten in <6 s, but facilitate long-term behavioral learning over a time scale of ∼5 min. During 100 repetitions of a learning instruction, simple-spike firing rate becomes progressively depressed in Purkinje cells that receive climbing-fiber inputs from the instruction. In Purkinje cells that prefer the opposite direction of pursuit and therefore do not receive climbing-fiber inputs related to the instruction, simple-spike responses undergo potentiation, but more weakly and more slowly. Analysis of the relationship between the learned changes in simple-spike firing and learning in eye velocity suggests an orderly progression of plasticity: first on Purkinje cells with complex-spike (CS) responses to the instruction, later on Purkinje cells with CS responses to the opposite direction of instruction, and last in sites outside the cerebellar cortex. Climbing-fiber inputs appear to play a fast and primary, but nonexclusive, role in pursuit learning.

Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning

Motor learning occurs through interactions between the cerebellar circuit and cellular plasticity at different sites. Previous work has established plasticity in brain slices and suggested plausible sites of behavioral learning. We now reveal what actually happens in the cerebellum during short-term learning. We monitor the expression of plasticity in the simple-spike firing of cerebellar Purkinje cells during trial-over-trial learning in smooth pursuit eye movements of monkeys. Our findings imply that: 1) a single complex-spike response driven by one instruction for learning causes short-term plasticity in a Purkinje cell's mossy fiber/parallel-fiber input pathways; 2) complex-spike responses and simple-spike firing rate are correlated across the Purkinje cell population; and 3) simple-spike firing rate at the time of an instruction for learning modulates the probability of a complex-spike response, possibly through a disynaptic feedback pathway to the inferior olive. These mechanisms may participate in long-term motor learning. DOI: http://dx.doi.org/10.7554/eLife.01574.001.

Calretinin inputs are confined to motoneurons for upward eye movements in monkey

Motoneurons of extraocular muscles are controlled by different premotor pathways, whose selective damage may cause directionally selective eye movement disorders. The fact that clinical disorders can affect only one direction, e.g., isolated up-/downgaze palsy or up-/downbeat nystagmus, indicates that up- and downgaze pathways are organized separately. Recent work in monkey revealed that a subpopulation of premotor neurons of the vertical eye movement system contains the calcium-binding protein calretinin (CR). With combined tract-tracing and immunofluorescence, the motoneurons of vertically pulling eye muscles in monkey were investigated for the presence of CR-positive afferent terminals. In the oculomotor nucleus, CR was specifically found in punctate profiles contacting superior rectus and inferior oblique motoneurons, as well as levator palpebrae motoneurons, all of which participate in upward eye movements. Double-immunofluorescence labeling revealed that CR-positive terminals lacked the γ-aminobutyric acid (GABA)-synthesizing enzyme glutamate decarboxylase, which is present in inhibitory afferents to all motoneurons mediating vertical eye movements. Therefore, CR-containing afferents are considered to be excitatory. In conclusion, a strong CR input is confined to motoneurons mediating upgaze, which derive from premotor pathways mediating saccades and smooth pursuit, but not from secondary vestibulo-ocular neurons in the magnocellular part of the medial vestibular nucleus. The functional significance of CR in these connections is unclear, but it may serve as a useful marker to locate upgaze pathways in the human brain.

Effects of caudate microstimulation on spontaneous and purposive saccades

Electrical stimulation has been delivered to the basal ganglia (BG) to treat intractable symptoms of a variety of clinical disorders. However, it is still unknown how such treatments improve behavioral symptoms. A difficulty of this problem is that artificial signals created by electrical stimulation interact with intrinsic signals before influencing behavior, thereby making it important to understand how such interactions between artificial and intrinsic signals occur. We addressed this issue by analyzing the effects of electrical stimulation under the following two behavioral conditions that induce different states of intrinsic signals: 1) subjects behave spontaneously without task demands; and 2) subjects perform a behavioral paradigm purposefully. We analyzed saccadic eye movements in monkeys while delivering microstimulation to the head and body of the caudate nucleus, a major input stage of the oculomotor BG. When monkeys generated spontaneous saccades, caudate microstimulation biased saccade vector endpoints toward the contralateral direction of stimulation sites. However, when caudate microstimulation was delivered during a purposive prosaccade (look toward a visual stimulus) or an antisaccade (look away from a stimulus) paradigm, it created overall ipsilateral biases by suppressing contralateral saccades more strongly than ipsilateral saccades. These results suggest that the impact of BG electrical stimulation changes dynamically depending on the state of intrinsic signals that vary under a variety of behavioral demands in everyday life.

The Interaction of Bayesian Priors and Sensory Data and Its Neural Circuit Implementation in Visually Guided Movement

Sensory-motor behavior results from a complex interaction of noisy sensory data with priors based on recent experience. By varying the stimulus form and contrast for the initiation of smooth pursuit eye movements in monkeys, we show that visual motion inputs compete with two independent priors: one prior biases eye speed toward zero; the other prior attracts eye direction according to the past several days' history of target directions. The priors bias the speed and direction of the initiation of pursuit for the weak sensory data provided by the motion of a low-contrast sine wave grating. However, the priors have relatively little effect on pursuit speed and direction when the visual stimulus arises from the coherent motion of a high-contrast patch of dots. For any given stimulus form, the mean and variance of eye speed covary in the initiation of pursuit, as expected for signal-dependent noise. This relationship suggests that pursuit implements a trade-off between movement accuracy and variation, reducing both when the sensory signals are noisy. The tradeoff is implemented as a competition of sensory data and priors that follows the rules of Bayesian estimation. Computer simulations show that the priors can be understood as direction-specific control of the strength of visual-motor transmission, and can be implemented in a neural-network model that makes testable predictions about the population response in the smooth eye movement region of the frontal eye fields.

Residual Attention Guidance in Blindsight Monkeys Watching Complex Natural Scenes

Patients with damage to primary visual cortex (V1) demonstrate residual performance on laboratory visual tasks despite denial of conscious seeing (blindsight) [1]. After a period of recovery, which suggests a role for plasticity [2], visual sensitivity higher than chance is observed in humans and monkeys for simple luminance-defined stimuli, grating stimuli, moving gratings, and other stimuli [3-7]. Some residual cognitive processes including bottom-up attention and spatial memory have also been demonstrated [8-10]. To date, little is known about blindsight with naturalstimuli and spontaneous visual behavior. In particular, is orienting attention toward salient stimuli during free viewing still possible? We used a computational saliency map model to analyze spontaneous eye movements of monkeys with blindsight from unilateral ablation of V1. Despite general deficits in gaze allocation, monkeys were significantly attracted to salient stimuli. The contribution oforientation features to salience was nearly abolished, whereas contributions of motion, intensity, and color features were preserved. Control experiments employing laboratory stimuli confirmed the free-viewing finding that lesioned monkeys retained color sensitivity. Our results show that attention guidance over complex natural scenes is preserved in the absence of V1, thereby directly challenging theories and models that crucially depend on V1 to compute the low-level visual features that guide attention.

Linking visual response properties in the superior colliculus to saccade behavior

Here we examined the influence of the visual response in the superior colliculus (SC) (an oculomotor control structure integrating sensory, motor and cognitive signals) on the development of the motor command that drives saccadic eye movements in monkeys. We varied stimulus luminance to alter the timing and magnitude of visual responses in the SC and examined how these changes correlated with resulting saccade behavior. Increasing target luminance resulted in multiple modulations of the visual response, including increased magnitude and decreased response onset latency. These signal modulations correlated strongly with changes in saccade latency and metrics, indicating that these signal properties carry through to the neural computations that determine when, where and how fast the eyes will move. Thus, components of the earliest part of the visual response in the SC provide important building blocks for the neural basis of the sensory-motor transformation, highlighting a critical link between the properties of the visual response and saccade behavior.

Visual and auditory cue integration for the generation of saccadic eye movements in monkeys and lever pressing in humans

This study examined how effectively visual and auditory cues can be integrated in the brain for the generation of motor responses. The latencies with which saccadic eye movements are produced in humans and monkeys form, under certain conditions, a bimodal distribution, the first mode of which has been termed express saccades. In humans, a much higher percentage of express saccades is generated when both visual and auditory cues are provided compared with the single presentation of these cues [H. C. Hughes et al. (1994) J. Exp. Psychol. Hum. Percept. Perform., 20, 131-153]. In this study, we addressed two questions: first, do monkeys also integrate visual and auditory cues for express saccade generation as do humans and second, does such integration take place in humans when, instead of eye movements, the task is to press levers with fingers? Our results show that (i) in monkeys, as in humans, the combined visual and auditory cues generate a much higher percentage of express saccades than do singly presented cues and (ii) the latencies with which levers are pressed by humans are shorter when both visual and auditory cues are provided compared with the presentation of single cues, but the distribution in all cases is unimodal; response latencies in the express range seen in the execution of saccadic eye movements are not obtained with lever pressing.

Reward Action in the Initiation of Smooth Pursuit Eye Movements

Reward has a powerful influence on motor behavior. To probe how and where reward systems alter motor behavior, we studied smooth pursuit eye movements in monkeys trained to associate the color of a visual cue with the size of the reward to be issued at the end of the target motion. When the tracking task presented two different colored targets that moved orthogonally, monkeys biased the initiation of pursuit toward the direction of motion of the target that led to larger reward. The bias was larger than expected given the modest effects of reward size on tracking of single targets. Experiments with three different reward sizes suggested that the bias afforded a given target depends mainly on the size of the larger reward. To analyze the effect of reward on directional learning in pursuit, monkeys tracked a single moving target that changed direction 250 ms after the onset of motion. Expectation of a larger reward led to a larger learned eye movement during the acquisition of the learned response and during subsequent probes of what had been learned, implying that reward influenced the expression rather than the acquisition of learning. The specific effects of reward size on learning and two-target stimuli imply that the site of reward modulation is at a level where multiple target motions compete for control of eye movement, downstream from sensory processing and learning and upstream from final motor processing.

Saccadic gain adaptation is predicted by the statistics of natural fluctuations in oculomotor function

Due to multiple factors such as fatigue, muscle strengthening, and neural plasticity, the responsiveness of the motor apparatus to neural commands changes over time. To enable precise movements the nervous system must adapt to compensate for these changes. Recent models of motor adaptation derive from assumptions about the way the motor apparatus changes. Characterizing these changes is difficult because motor adaptation happens at the same time, masking most of the effects of ongoing changes. Here, we analyze eye movements of monkeys with lesions to the posterior cerebellar vermis that impair adaptation. Their fluctuations better reveal the underlying changes of the motor system over time. When these measured, unadapted changes are used to derive optimal motor adaptation rules the prediction precision significantly improves. Among three models that similarly fit single-day adaptation results, the model that also matches the temporal correlations of the non-adapting saccades most accurately predicts multiple day adaptation. Saccadic gain adaptation is well matched to the natural statistics of fluctuations of the oculomotor plant.