Preparatory Gain Modulation of Visuomotor Transmission for Smooth Pursuit Eye Movements in Monkeys

2006 ◽  
Vol 96 (6) ◽  
pp. 3051-3063 ◽  
Author(s):  
Hiromitsu Tabata ◽  
Kenichiro Miura ◽  
Masakatsu Taki ◽  
Kiyoto Matsuura ◽  
Kenji Kawano
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Response Amplitude ◽  
Target Velocity ◽  
Recent Experience ◽  
Gain Modulation ◽  
Visuomotor Processing ◽  
Pursuit Velocity ◽  
Eye Velocity ◽  
Plateau Level

It has been reported that the visuomotor processing underlying the initiation of smooth pursuit eye movement is modulated in relation to the recent experience of eye movements: the initial pursuit eye velocity is larger after experiencing repeated pursuits than saccades. To assess which parameters of the previously executed pursuits play an essential role in modulating the gain of visuomotor transmission, we recorded the ocular responses of monkeys to a brief perturbing motion of the tracking target injected before the start of the eye movements. First, we compared the perturbation responses among the blocks in which the duration of executing pursuit was varied. We found that the response amplitude increased with the increase of the pursuit duration and it reached a plateau level at 100–200 ms of the duration. Second, a comparison of the perturbation responses in the blocks in which target velocity was different showed a gradual increase of the response as a function of the required pursuit velocity. Third, when the animals repeatedly performed pursuits, the response amplitude gradually increased with increasing interval between the appearance of the target and the onset of perturbation. On the other hand, such an increase was not observed when the animals repeatedly performed saccades. These results suggest that before initiating eye movements, the pursuit system modulates the gain of visuomotor transmission so as to be closely related to the properties of the repeatedly experienced eye movements and this gain modulation is triggered by the target’s appearance.

scholarly journals The vestibular-related frontal cortex and its role in smooth-pursuit eye movements and vestibular-pursuit interactions

2006 ◽  
Vol 16 (1-2) ◽  
pp. 1-22 ◽  
Author(s):  
Junko Fukushima ◽  
Teppei Akao ◽  
Sergei Kurkin ◽  
Chris R.S. Kaneko ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Frontal Cortex ◽  
Smooth Pursuit ◽  
Vestibular Stimulation ◽  
Target Motion ◽  
Head Movements ◽  
Image Motion ◽  
Target Velocity ◽  
Eye Velocity ◽  
Pursuit Neurons

In order to see clearly when a target is moving slowly, primates with high acuity foveae use smooth-pursuit and vergence eye movements. The former rotates both eyes in the same direction to track target motion in frontal planes, while the latter rotates left and right eyes in opposite directions to track target motion in depth. Together, these two systems pursue targets precisely and maintain their images on the foveae of both eyes. During head movements, both systems must interact with the vestibular system to minimize slip of the retinal images. The primate frontal cortex contains two pursuit-related areas; the caudal part of the frontal eye fields (FEF) and supplementary eye fields (SEF). Evoked potential studies have demonstrated vestibular projections to both areas and pursuit neurons in both areas respond to vestibular stimulation. The majority of FEF pursuit neurons code parameters of pursuit such as pursuit and vergence eye velocity, gaze velocity, and retinal image motion for target velocity in frontal and depth planes. Moreover, vestibular inputs contribute to the predictive pursuit responses of FEF neurons. In contrast, the majority of SEF pursuit neurons do not code pursuit metrics and many SEF neurons are reported to be active in more complex tasks. These results suggest that FEF- and SEF-pursuit neurons are involved in different aspects of vestibular-pursuit interactions and that eye velocity coding of SEF pursuit neurons is specialized for the task condition.

scholarly journals Evidence for Object Permanence in the Smooth-Pursuit Eye Movements of Monkeys

2003 ◽  
Vol 90 (4) ◽  
pp. 2205-2218 ◽  
Author(s):  
Mark M. Churchland ◽  
I-Han Chou ◽  
Stephen G. Lisberger
Keyword(s):  
Steady State ◽  
Eye Movements ◽  
Computer Simulations ◽  
Smooth Pursuit ◽  
Constant Velocity ◽  
Object Permanence ◽  
Target Velocity ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Eye Velocity

We recorded the smooth-pursuit eye movements of monkeys in response to targets that were extinguished (blinked) for 200 ms in mid-trajectory. Eye velocity declined considerably during the target blinks, even when the blinks were completely predictable in time and space. Eye velocity declined whether blinks were presented during steady-state pursuit of a constant-velocity target, during initiation of pursuit before target velocity was reached, or during eye accelerations induced by a change in target velocity. When a physical occluder covered the trajectory of the target during blinks, creating the impression that the target moved behind it, the decline in eye velocity was reduced or abolished. If the target was occluded once the eye had reached target velocity, pursuit was only slightly poorer than normal, uninterrupted pursuit. In contrast, if the target was occluded during the initiation of pursuit, while the eye was accelerating toward target velocity, pursuit during occlusion was very different from normal pursuit. Eye velocity remained relatively stable during target occlusion, showing much less acceleration than normal pursuit and much less of a decline than was produced by a target blink. Anticipatory or predictive eye acceleration was typically observed just prior to the reappearance of the target. Computer simulations show that these results are best understood by assuming that a mechanism of eye-velocity memory remains engaged during target occlusion but is disengaged during target blinks.

scholarly journals Motion dependence of smooth pursuit eye movements in the marmoset

2015 ◽  
Vol 113 (10) ◽  
pp. 3954-3960 ◽  
Author(s):  
Jude F. Mitchell ◽  
Nicholas J. Priebe ◽  
Cory T. Miller
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Genetic Model ◽  
Mental Disease ◽  
Target Velocity ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Slow Moving ◽  
Eye Velocity

Smooth pursuit eye movements stabilize slow-moving objects on the retina by matching eye velocity with target velocity. Two critical components are required to generate smooth pursuit: first, because it is a voluntary eye movement, the subject must select a target to pursue to engage the tracking system; and second, generating smooth pursuit requires a moving stimulus. We examined whether this behavior also exists in the common marmoset, a New World primate that is increasingly attracting attention as a genetic model for mental disease and systems neuroscience. We measured smooth pursuit in two marmosets, previously trained to perform fixation tasks, using the standard Rashbass step-ramp pursuit paradigm. We first measured the aspects of visual motion that drive pursuit eye movements. Smooth eye movements were in the same direction as target motion, indicating that pursuit was driven by target movement rather than by displacement. Both the open-loop acceleration and closed-loop eye velocity exhibited a linear relationship with target velocity for slow-moving targets, but this relationship declined for higher speeds. We next examined whether marmoset pursuit eye movements depend on an active engagement of the pursuit system by measuring smooth eye movements evoked by small perturbations of motion from fixation or during pursuit. Pursuit eye movements were much larger during pursuit than from fixation, indicating that pursuit is actively gated. Several practical advantages of the marmoset brain, including the accessibility of the middle temporal (MT) area and frontal eye fields at the cortical surface, merit its utilization for studying pursuit movements.

Postsaccadic Enhancement of Initiation of Smooth Pursuit Eye Movements in Monkeys

1998 ◽  
Vol 79 (4) ◽  
pp. 1918-1930 ◽  
Author(s):  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Target Position ◽  
Target Motion ◽  
Target Velocity ◽  
Smooth Pursuit Eye Movements ◽  
Motor Pathways ◽  
Pursuit Eye Movements ◽  
Eye Velocity

Lisberger, Stephen G. Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. J. Neurophysiol. 79: 1918–1930, 1998. Step-ramp target motion evokes a characteristic sequence of presaccadic smooth eye movement in the direction of the target ramp, catch-up targets to bring eye position close to the position of the moving target, and postsaccadic eye velocities that nearly match target velocity. I have analyzed this sequence of eye movements in monkeys to reveal a strong postsaccadic enhancement of pursuit eye velocity and to document the conditions that lead to that enhancement. Smooth eye velocity was measured in the last 10 ms before and the first 10 ms after the first saccade evoked by step-ramp target motion. Plots of eye velocity as a function of time after the onset of the target ramp revealed that eye velocity at a given time was much higher if measured after versus before the saccade. Postsaccadic enhancement of pursuit was recorded consistently when the target stepped 3° eccentric on the horizontal axis and moved upward, downward, or away from the position of fixation. To determine whether postsaccadic enhancement of pursuit was invoked by smear of the visual scene during a saccade, I recorded the effect of simulated saccades on the presaccadic eye velocity for step-ramp target motion. The 3° simulated saccade, which consisted of motion of a textured background at 150°/s for 20 ms, failed to cause any enhancement of presaccadic eye velocity. By using a strategically selected set of oblique target steps with horizontal ramp target motion, I found clear enhancement for saccades in all directions, even those that were orthogonal to target motion. When the size of the target step was varied by up to 15° along the horizontal meridian, postsaccadic eye velocity did not depend strongly either on the initial target position or on whether the target moved toward or away from the position of fixation. In contrast, earlier studies and data in this paper show that presaccadic eye velocity is much stronger when the target is close to the center of the visual field and when the target moves toward versus away from the position of fixation. I suggest that postsaccadic enhancement of pursuit reflects activation, by saccades, of a switch that regulates the strength of transmission through the visual-motor pathways for pursuit. Targets can cause strong visual motion signals but still evoke low presaccadic eye velocities if they are ineffective at activating the pursuit system.

Smooth-Pursuit Eye-Movement-Related Neuronal Activity in Macaque Nucleus Reticularis Tegmenti Pontis

2003 ◽  
Vol 89 (4) ◽  
pp. 2146-2158 ◽  
Author(s):  
David A. Suzuki ◽  
Tetsuto Yamada ◽  
Robert D. Yee
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Response Amplitude ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Average Sensitivity ◽  
Nucleus Reticularis Tegmenti Pontis ◽  
Pursuit Eye Movements ◽  
Nucleus Reticularis ◽  
Eye Velocity

Neuronal responses that were observed during smooth-pursuit eye movements were recorded from cells in rostral portions of the nucleus reticularis tegmenti pontis (rNRTP). The responses were categorized as smooth-pursuit eye velocity (78%) or eye acceleration (22%). A separate population of rNRTP cells encoded static eye position. The sensitivity to pursuit eye velocity averaged 0.81 spikes/s per °/s, whereas the average sensitivity to pursuit eye acceleration was 0.20 spikes/s per °/s2. Of the eye-velocity cells with horizontal preferences for pursuit responses, 56% were optimally responsive to contraversive smooth-pursuit eye movements and 44% preferred ipsiversive pursuit. For cells with vertical pursuit preferences, 61% preferred upward pursuit and 39% preferred downward pursuit. The direction selectivity was broad with 50% of the maximal response amplitude observed for directions of smooth pursuit up to ±85° away from the optimal direction. The activities of some rNRTP cells were linearly related to eye position with an average sensitivity of 2.1 spikes/s per deg. In some cells, the magnitude of the response during smooth-pursuit eye movements was affected by the position of the eyes even though these cells did not encode eye position. On average, pursuit centered to one side of screen center elicited a response that was 73% of the response amplitude obtained with tracking centered at screen center. For pursuit centered on the opposite side, the average response was 127% of the response obtained at screen center. The results provide a neuronal rationale for the slow, pursuit-like eye movements evoked with rNRTP microstimulation and for the deficits in smooth-pursuit eye movements observed with ibotenic acid injection into rNRTP. More globally, the results support the notion of a frontal and supplementary eye field-rNRTP-cerebellum pathway involved with controlling smooth-pursuit eye movements.

Visual tracking in monkeys: evidence for short-latency suppression of the vestibuloocular reflex

1990 ◽  
Vol 63 (4) ◽  
pp. 676-688 ◽  
Author(s):  
S. G. Lisberger
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Initial Conditions ◽  
Short Latency ◽  
Target Motion ◽  
Head Motion ◽  
Target Velocity ◽  
Vestibuloocular Reflex ◽  
Pursuit Eye Movements ◽  
Eye Velocity

1. Monkeys normally use a combination of smooth head and eye movements to keep the eyes pointed at a slowly moving object. The visual inputs from target motion evoke smooth pursuit eye movements, whereas the vestibular inputs from head motion evoke a vestibuloocular reflex (VOR). Our study asks how the eye movements of pursuit and the VOR interact. Is there a linear addition of independent commands for pursuit and the VOR? Or does the interaction of visual and vestibular stimuli cause momentary, "parametric" modulation of transmission through VOR pathways? 2. We probed for the state of the VOR and pursuit by presenting transient perturbations of target and/or head motion under different steady-state tracking conditions. Tracking conditions included fixation at straight-ahead gaze, in which both the head and the target were stationary; "times-zero (X0) tracking," in which the target and head moved in the same direction at the same speed; and "times-two (X2) tracking," in which the target and head moved in opposite directions at the same speed. 3. Comparison of the eye velocities evoked by changes in the direction of X0 versus X2 tracking revealed two components of the tracking response. The earliest component, which we attribute to the VOR, had a latency of 14 ms and a trajectory that did not depend on initial tracking conditions. The later component had a latency of 70 ms or less and a trajectory that did depend on tracking conditions. 4. To probe the latency of pursuit eye movements, we imposed perturbations of target velocity imposed during X0 and X2 tracking. The resulting changes in eye velocity had latencies of at least 100 ms. We conclude that the effects of initial tracking conditions on eye velocity at latencies of less than 70 ms cannot be caused by visual feedback through the smooth-pursuit system. Instead, there must be another mechanism for short-latency control over the VOR; we call this component of the response "short-latency tracking." 5. Perturbations of head velocity or head and target velocity during X0 and X2 tracking showed that short-latency tracking depended only on the tracking conditions at the time the perturbation was imposed. The VOR appeared to be suppressed when the initial conditions were X0 tracking. 6. The magnitude of short-latency tracking depended on the speed of initial head and target movement. During X0 tracking at 15 deg/s, short-latency tracking was modest. When the initial speed of head and target motion was 60 deg/s, the amplitude of short-latency tracking was quite large and its latency became as short as 36 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals The effect of a temporary absence of target velocity information on visual tracking

2010 ◽  
Vol 3 (4) ◽  
Author(s):  
Patricia M. Cisarik ◽  
Sanjeev Kasthurirangan ◽  
Frank E. Visco Jr. ◽  
Harold E. Bedell ◽  
Scott B. Stevenson ◽  
...  
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Target Velocity ◽  
Laser Target ◽  
Position Information ◽  
Saccade Programming ◽  
Velocity Information ◽  
Behavioral Evidence ◽  
Pursuit Velocity ◽  
Made In

Experiments with the Rashbass ‘step-ramp’ paradigm have revealed that the initial catchup saccade that occurs near pursuit onset uses target velocity as well as position information in its programming. Information about both position and motion also influences smooth pursuit. To investigate the timing of velocity sampling near the initiation of saccades and smooth pursuit, we analyzed the eye movements made in nine ‘step-ramp’ conditions, produced by combining –2, 0 and +2 deg steps with –8, 0 and +8 deg/s ramps. Each trial had either no temporal gap or a 50-ms gap during which the laser target was extinguished, beginning 25, 50, 75 or 100 ms after the step. Six subjects repeated each of the resulting 45 conditions 25 times. With no temporal gap, saccades were larger in the step-ramp-away’ than the ‘step-only’ condition, confirming that saccade programming incorporates ramp velocity information. A temporal gap had no effect on the accuracy of saccades on ‘step-only’ trials, but often caused undershoots in ‘step-ramp’ trials. A 50-ms gap within the first 100 ms also increased the latency of the initial saccade. Although initial pursuit velocity was unaffected by a temporal gap, a gap that started at 25 ms reliably delayed pursuit onset for ramp motion of the target toward the fovea. Later gaps had a minimal effect on initial pursuit latency. The similar timing of the temporal gaps in target motion information that affect the initiation of saccades and pursuit provides further behavioral evidence that the two types of eye movements share pre-motor neural mechanisms.

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.

Neuronal Responses Related to Smooth Pursuit Eye Movements in the Periarcuate Cortical Area of Monkeys

1998 ◽  
Vol 80 (1) ◽  
pp. 28-47 ◽  
Author(s):  
Masaki Tanaka ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Cortical Area ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Neuronal Responses ◽  
Stationary Target ◽  
Pursuit Eye Movements ◽  
Preferred Direction ◽  
Eye Velocity

Tanaka, Masaki and Kikuro Fukushima. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80: 28–47, 1998. To examine how the periarcuate area is involved in the control of smooth pursuit eye movements, we recorded 177 single neurons while monkeys pursued a moving target in the dark. The majority (52%, 92/177) of task-related neurons responded to pursuit but had little or no response to saccades. Histological reconstructions showed that these neurons were located mainly in the posterior bank of the arcuate sulcus near the sulcal spur. Twenty-seven percent (48/177) changed their activity at the onset of saccades. Of these, 36 (75%) showed presaccadic burst activity with strong preference for contraversive saccades. Eighteen (10%, 18/177) were classified as eye-position–related neurons, and 11% (19/177) were related to other aspects of the stimuli or response. Among the 92 neurons that responded to pursuit, 85 (92%) were strongly directional with uniformly distributed preferred directions. Further analyses were performed in these directionally sensitive pursuit-related neurons. For 59 neurons that showed distinct changes in activity around the initiation of pursuit, the median latency from target motion was 96 ms and that preceding pursuit was −12 ms, indicating that these neuron can influence the initiation of pursuit. We tested some neurons by briefly extinguishing the tracking target ( n = 39) or controlling its movement with the eye position signal ( n = 24). The distribution of the change in pursuit-related activity was similar to previous data for the dorsomedial part of the medial superior temporal neurons ( Newsome et al. 1988) , indicating that pursuit-related neurons in the periarcuate area also carry extraretinal signals. For 22 neurons, we examined the responses when the animals reversed pursuit direction to distinguish the effects of eye acceleration in the preferred direction from oppositely directed eye velocity. Almost all neurons discharged before eye velocity reached zero, however, only nine neurons discharged before the eyes were accelerated in the preferred direction. The delay in neuronal responses relative to the onset of eye acceleration in these trials might be caused by suppression from oppositely directed pursuit velocity. The results suggest that the periarcuate neurons do not participate in the earliest stage of eye acceleration during the change in pursuit direction, although most of them may participate in the early stages of pursuit initiation in the ordinary step-ramp pursuit trials. Some neurons changed their activity when the animals fixated a stationary target, and this activity could be distinguished easily from the strong pursuit-related responses. Our results suggest that the periarcuate pursuit area carries extraretinal signals and affects the premotor circuitry for smooth pursuit.

Quantitative Analysis of Abducens Neuron Discharge Dynamics During Saccadic and Slow Eye Movements

1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Eye Movement ◽  
Neuronal Activity ◽  
Smooth Pursuit ◽  
Slow Phase ◽  
Vestibular Nystagmus ◽  
Firing Rates ◽  
Rapid Eye Movements ◽  
Eye Velocity

The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement–based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + rE˙, where FR is firing rate, E and E˙ are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or “slide” (FR = b + kE + rE˙ + uË − c[Formula: see text]), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients ( r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias ( b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.

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