Facilitation of Smooth Pursuit Initiation by Electrical Stimulation in the Supplementary Eye Fields

2001 ◽  
Vol 86 (5) ◽  
pp. 2413-2425 ◽  
Author(s):  
M. Missal ◽  
S. J. Heinen
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Electrical Microstimulation ◽  
Pursuit Initiation ◽  
Fixation Task ◽  
Catch Up ◽  
Eye Velocity ◽  
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 ∼20%. At most sites, the threshold for a significant facilitation was 50 μA 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.

Role of Retinal Slip in the Prediction of Target Motion During Smooth and Saccadic Pursuit

2001 ◽  
Vol 86 (2) ◽  
pp. 550-558 ◽  
Author(s):  
Sophie de Brouwer ◽  
Marcus Missal ◽  
Philippe Lefèvre
Keyword(s):  
Steady State ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Target Motion ◽  
Target Velocity ◽  
Retinal Slip ◽  
Average Gain ◽  
Pursuit Initiation ◽  
Catch Up

Visual tracking of moving targets requires the combination of smooth pursuit eye movements with catch-up saccades. In primates, catch-up saccades usually take place only during pursuit initiation because pursuit gain is close to unity. This contrasts with the lower and more variable gain of smooth pursuit in cats, where smooth eye movements are intermingled with catch-up saccades during steady-state pursuit. In this paper, we studied in detail the role of retinal slip in the prediction of target motion during smooth and saccadic pursuit in the cat. We found that the typical pattern of pursuit in the cat was a combination of smooth eye movements with saccades. During smooth pursuit initiation, there was a correlation between peak eye acceleration and target velocity. During pursuit maintenance, eye velocity oscillated at ∼3 Hz around a steady-state value. The average gain of smooth pursuit was ∼0.5. Trained cats were able to continue pursuing in the absence of a visible target, suggesting a role of the prediction of future target motion in this species. The analysis of catch-up saccades showed that the smooth-pursuit motor command is added to the saccadic command during catch-up saccades and that both position error and retinal slip are taken into account in their programming. The influence of retinal slip on catch-up saccades showed that prediction about future target motion is used in the programming of catch-up saccades. Altogether, these results suggest that pursuit systems in primates and cats are qualitatively similar, with a lower average gain in the cat and that prediction affects both saccades and smooth eye movements during pursuit.

scholarly journals Role of Primate Cerebellar Hemisphere in Voluntary Eye Movement Control Revealed by Lesion Effects

2009 ◽  
Vol 101 (2) ◽  
pp. 934-947 ◽  
Author(s):  
Masafumi Ohki ◽  
Hiromasa Kitazawa ◽  
Takahito Hiramatsu ◽  
Kimitake Kaga ◽  
Taiko Kitamura ◽  
...  
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Movement Control ◽  
Cerebellar Hemisphere ◽  
Target Velocity ◽  
Eye Movement Control ◽  
Pursuit Eye Movements ◽  
Catch Up

The anatomical connection between the frontal eye field and the cerebellar hemispheric lobule VII (H-VII) suggests a potential role of the hemisphere in voluntary eye movement control. To reveal the involvement of the hemisphere in smooth pursuit and saccade control, we made a unilateral lesion around H-VII and examined its effects in three Macaca fuscata that were trained to pursue visually a small target. To the step (3°)-ramp (5–20°/s) target motion, the monkeys usually showed an initial pursuit eye movement at a latency of 80–140 ms and a small catch-up saccade at 140–220 ms that was followed by a postsaccadic pursuit eye movement that roughly matched the ramp target velocity. After unilateral cerebellar hemispheric lesioning, the initial pursuit eye movements were impaired, and the velocities of the postsaccadic pursuit eye movements decreased. The onsets of 5° visually guided saccades to the stationary target were delayed, and their amplitudes showed a tendency of increased trial-to-trial variability but never became hypo- or hypermetric. Similar tendencies were observed in the onsets and amplitudes of catch-up saccades. The adaptation of open-loop smooth pursuit velocity, tested by a step increase in target velocity for a brief period, was impaired. These lesion effects were recognized in all directions, particularly in the ipsiversive direction. A recovery was observed at 4 wk postlesion for some of these lesion effects. These results suggest that the cerebellar hemispheric region around lobule VII is involved in the control of smooth pursuit and saccadic eye movements.

Suppression of smooth pursuit eye movements induced by electrical stimulation of the monkey frontal eye field

2011 ◽  
Vol 106 (5) ◽  
pp. 2675-2687 ◽  
Author(s):  
Yoshiko Izawa ◽  
Hisao Suzuki ◽  
Yoshikazu Shinoda
Keyword(s):  
Electrical Stimulation ◽  
Smooth Pursuit ◽  
Suppressive Effect ◽  
Frontal Eye Field ◽  
Pursuit Eye Movements ◽  
Physiological Properties ◽  
Eye Field ◽  
Catch Up ◽  
Stimulation Of

This study was performed to characterize the properties of the suppression of smooth pursuit eye movement induced by electrical stimulation of the frontal eye field (FEF) in trained monkeys. At the stimulation sites tested, we first determined the threshold for generating electrically evoked saccades (Esacs). We then examined the suppressive effects of stimulation on smooth pursuit at intensities that were below the threshold for eliciting Esacs. We observed that FEF stimulation induced a clear deceleration of pursuit at pursuit initiation and also during the maintenance of pursuit at subthreshold intensities. The suppression of pursuit occurred even in the absence of catch-up saccades during pursuit, indicating that suppression influenced pursuit per se. We mapped the FEF area that was associated with the suppressive effect of stimulation on pursuit. In a wide area in the FEF, suppressive effects were observed for ipsiversive, but not contraversive, pursuit. In contrast, we observed the bilateral suppression of both ipsiversive and contraversive pursuit in a localized area in the FEF. This area coincided with the area in which we have previously shown that stimulation suppressed the generation of saccades in bilateral directions and also where fixation neurons that discharged during fixation were concentrated. On the basis of these results, we compared the FEF suppression of pursuit with that of saccades with regard to several physiological properties and then discussed the role of the FEF in the suppression of both pursuit and saccades, and particularly in the maintenance of visual fixation.

scholarly journals Stopping smooth pursuit

2017 ◽  
Vol 372 (1718) ◽  
pp. 20160200 ◽  
Author(s):  
Marcus Missal ◽  
Stephen J. Heinen
Keyword(s):  
Smooth Pursuit ◽  
Neural Control ◽  
Inhibitory Neurons ◽  
Image Motion ◽  
Visual Object ◽  
Passive Response ◽  
Eye Velocity ◽  
Supplementary Eye Fields ◽  
Omnipause Neurons

If a visual object of interest suddenly starts to move, we will try to follow it with a smooth movement of the eyes. This smooth pursuit response aims to reduce image motion on the retina that could blur visual perception. In recent years, our knowledge of the neural control of smooth pursuit initiation has sharply increased. However, stopping smooth pursuit eye movements is less well understood and will be discussed in this paper. The most straightforward way to study smooth pursuit stopping is by interrupting image motion on the retina. This causes eye velocity to decay exponentially towards zero. However, smooth pursuit stopping is not a passive response, as shown by behavioural and electrophysiological evidence. Moreover, smooth pursuit stopping is particularly influenced by active prediction of the upcoming end of the target. Here, we suggest that a particular class of inhibitory neurons of the brainstem, the omnipause neurons, could play a central role in pursuit stopping. Furthermore, the role of supplementary eye fields of the frontal cortex in smooth pursuit stopping is also discussed. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.

scholarly journals Different mechanisms for modulation of the initiation and steady-state of smooth pursuit eye movements

2019 ◽  
Author(s):  
Stuart Behling ◽  
Stephen G. Lisberger
Keyword(s):  
Steady State ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Smooth Pursuit Eye Movements ◽  
Target Speed ◽  
Pursuit Eye Movements ◽  
Pursuit Initiation ◽  
Visual Motor ◽  
State Tracking ◽  
Eye Velocity

AbstractSmooth pursuit eye movements are used by primates to track moving objects. They are initiated by sensory estimates of target speed represented in the middle temporal (MT) area of extrastriate visual cortex and then supported by motor feedback to maintain steady-state eye speed at target speed. Here, we show that reducing the coherence in a patch of dots for a tracking target degrades the eye speed both at the initiation of pursuit and during steady-state tracking, when eye speed reaches an asymptote well below target speed. The deficits are quantitatively different between the motor-supported steady-state of pursuit and the sensory-driven initiation of pursuit, suggesting separate mechanisms. The deficit in visually-guided pursuit initiation could not explain the deficit in steady-state tracking. Pulses of target speed during steady-state tracking revealed lower sensitivities to image motion across the retina for lower values of dot coherence. However, sensitivity was not zero, implying that visual motion should still be driving eye velocity towards target velocity. When we changed dot coherence from 100% to lower values during accurate steady-state pursuit, we observed larger eye decelerations for lower coherences, as expected if motor feedback was reduced in gain. A simple pursuit model accounts for our data based on separate modulation of the strength of visual-motor transmission and motor feedback. We suggest that reduced dot coherence creates less reliable target motion that impacts pursuit initiation by changing the gain of visual-motor transmission and perturbs steady-state tracking by modulation of the motor corollary discharges that comprise eye velocity memory.

scholarly journals Role of Arcuate Frontal Cortex of Monkeys in Smooth Pursuit Eye Movements. II. Relation to Vector Averaging Pursuit

2002 ◽  
Vol 87 (6) ◽  
pp. 2700-2714 ◽  
Author(s):  
Masaki Tanaka ◽  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Gain Control ◽  
Image Motion ◽  
Internal Gain ◽  
Vector Averaging ◽  
A Site ◽  
Eye Velocity ◽  
The Brain

When monkeys view two targets moving in different directions and are given no cues about which to track, the initiation of smooth pursuit is a vector average of the response evoked by each target singly. In the present experiments, double-target stimuli consisted of two identical targets moving in opposite directions along the preferred axis of pursuit for the neuron under study for 200 ms, followed by the continued motion for 800 ms of one target chosen randomly. Among the neurons that showed directional modulation during pursuit, recordings revealed three groups. The majority (32/60) showed responses that were intermediate to, and statistically different from, the responses to either target presented alone. Another large group (22/60) showed activity that was statistically indistinguishable from the response to the target moving in the preferred ( n = 15) or opposite ( n = 7) direction of the neuron under study. The minority (6/60) showed statistically higher firing during averaging pursuit than for either target presented singly. We conclude that many pursuit-related neurons in the frontal pursuit area (FPA) carry signals related to the motor output during averaging pursuit, while others encode the motion of one target or the other. Microstimulation with 200-ms trains of pulses at 50 μA while monkeys performed the same double-target tasks biased the averaging eye velocity in the direction of evoked eye movements during fixation. The effect of stimulation was compared with the predictions of three different models that placed the site of vector averaging upstream from, at, or downstream from the sites where the FPA regulates the gain of pursuit. The data were most consistent with a site for pursuit averaging downstream from the gain control, both for double-target stimuli that presented motion in opposite directions and in orthogonal directions. Thus the recording and stimulation data suggest that the FPA is both downstream and upstream from the sites of vector averaging. We resolve this paradox by suggesting that the site of averaging is really downstream from the site of gain control, while feedback of the eye velocity command from the brain stem and/or cerebellum is responsible for the firing of FPA neurons in relation to the averaged eye velocity. We suggest that eye velocity feedback allows FPA neurons to continue firing during accurate tracking, when image motion is small, and that the persistent output from the FPA is necessary to keep the internal gain of pursuit high and permit accurate pursuit.

Supplementary Eye Fields Stimulation Facilitates Anticipatory Pursuit

2004 ◽  
Vol 92 (2) ◽  
pp. 1257-1262 ◽  
Author(s):  
M. Missal ◽  
S. J. Heinen
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Neural Control ◽  
Target Motion ◽  
Motor Systems ◽  
Electrical Microstimulation ◽  
Pursuit Eye Movements ◽  
The Moment ◽  
Anticipatory Smooth Eye Movements ◽  
Supplementary Eye Fields

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.

Activity of fixation neurons in the monkey frontal eye field during smooth pursuit eye movements

2014 ◽  
Vol 112 (2) ◽  
pp. 249-262 ◽  
Author(s):  
Yoshiko Izawa ◽  
Hisao Suzuki
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Eye Field ◽  
Catch Up ◽  
Discharge Patterns ◽  
Reduced Activity

We recorded the activity of fixation neurons in the frontal eye field (FEF) in trained monkeys and analyzed their activity during smooth pursuit eye movements. Fixation neurons were densely located in the area of the FEF in the caudal part of the arcuate gyrus facing the inferior arcuate sulcus where focal electrical stimulation suppressed the generation of saccades and smooth pursuit in bilateral directions at an intensity lower than the threshold for eliciting electrically evoked saccades. Whereas fixation neurons discharged tonically during fixation, they showed a variety of discharge patterns during smooth pursuit, ranging from a decrease in activity to an increase in activity. Of these, more than two-thirds were found to show a reduction in activity during smooth pursuit in the ipsilateral and bilateral directions. The reduction in activity of fixation neurons began at pursuit initiation and continued during pursuit maintenance. When catch-up saccades during the initiation of pursuit were eliminated by a step-ramp target routine, the reduced activity of fixation neurons remained. The reduction in activity during pursuit was not dependent on the activity during fixation without a target. Based on these results, we discuss the role of the FEF at maintaining fixation in relation to various other brain areas. We suggest that fixation neurons in the FEF contribute to the suppression of smooth pursuit. These results suggest that FEF fixation neurons are part of a more generalized visual fixation system through which suppressive control is exerted on smooth pursuit, as well as saccades.

scholarly journals Eye-position error influence over “open-loop” smooth pursuit initiation

2018 ◽  
Author(s):  
Antimo Buonocore ◽  
Julianne Skinner ◽  
Ziad M. Hafed
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Open Loop ◽  
Position Error ◽  
Visual Signals ◽  
Error Signal ◽  
Movement Initiation ◽  
Pursuit Eye Movements ◽  
Pursuit Initiation ◽  
Catch Up

AbstractThe oculomotor system integrates a variety of visual signals into appropriate motor plans, but such integration can have widely varying time scales. For example, smooth pursuit eye movements to follow a moving target are slower and longer-lasting than saccadic eye movements, and it has been suggested that initiating a smooth pursuit eye movement involves an obligatory open-loop interval, in which new visual motion signals presumably cannot influence the ensuing motor plan for up to 100 ms after movement initiation. However, this view runs directly contrary to the idea that the oculomotor periphery has privileged access to short-latency visual signals. Here we show that smooth pursuit initiation is sensitive to visual inputs, even in “open-loop” intervals. We instructed male rhesus macaque monkeys to initiate saccade-free smooth pursuit eye movements, and we injected a transient, instantaneous eye position error signal at different times relative to movement initiation. We found robust short-latency modulations in eye velocity and acceleration, starting only ∼50 ms after transient signal occurrence, and even during “open-loop” pursuit initiation. Critically, the spatial direction of the injected position error signal had predictable effects on smooth pursuit initiation, with forward errors increasing eye acceleration and backwards errors reducing it. Catch-up saccade frequencies and amplitudes were also similarly altered ∼50 ms after transient signals, much like well-known effects on microsaccades during fixation. Our results demonstrate that smooth pursuit initiation is highly sensitive to visual signals, and that catch-up saccade generation is reset after a visual transient.

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