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.

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

2020 ◽  
Vol 123 (3) ◽  
pp. 1265-1276 ◽  
Author(s):  
Stuart Behling ◽  
Stephen G. Lisberger
Keyword(s):  
Steady State ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Smooth Pursuit Eye Movements ◽  
Target Speed ◽  
Pursuit Eye Movements ◽  
Visual Motor ◽  
State Tracking ◽  
Eye Velocity

Smooth 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 toward 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 allows us to observe evidence for separate modulations of the gain of visual-motor transmission during pursuit initiation and of the motor corollary discharges that comprise eye velocity memory and support steady-state tracking. NEW & NOTEWORTHY We exploit low-coherence patches of dots to control the initiation and steady state of smooth pursuit eye movements and show that these two phases of movement are modulated separately by the reliability of visual motion signals. We conclude that the neural circuit for pursuit includes separate modulation of the strength of visual-motor transmission for movement initiation and of eye velocity positive feedback to support steady-state tracking.

scholarly journals Spatial and Temporal Integration of Visual Motion Signals for Smooth Pursuit Eye Movements in Monkeys

2009 ◽  
Vol 102 (4) ◽  
pp. 2013-2025 ◽  
Author(s):  
Leslie C. Osborne ◽  
Stephen G. Lisberger
Keyword(s):  
Random Walk ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Target Motion ◽  
Linear Filter ◽  
Smooth Pursuit Eye Movements ◽  
Spatial Averaging ◽  
Spatial Integration ◽  
Pursuit Eye Movements

To probe how the brain integrates visual motion signals to guide behavior, we analyzed the smooth pursuit eye movements evoked by target motion with a stochastic component. When each dot of a texture executed an independent random walk such that speed or direction varied across the spatial extent of the target, pursuit variance increased as a function of the variance of visual pattern motion. Noise in either target direction or speed increased the variance of both eye speed and direction, implying a common neural noise source for estimating target speed and direction. Spatial averaging was inefficient for targets with >20 dots. Together these data suggest that pursuit performance is limited by the properties of spatial averaging across a noisy population of sensory neurons rather than across the physical stimulus. When targets executed a spatially uniform random walk in time around a central direction of motion, an optimized linear filter that describes the transformation of target motion into eye motion accounted for ∼50% of the variance in pursuit. Filters had widths of ∼25 ms, much longer than the impulse response of the eye, and filter shape depended on both the range and correlation time of motion signals, suggesting that filters were products of sensory processing. By quantifying the effects of different levels of stimulus noise on pursuit, we have provided rigorous constraints for understanding sensory population decoding. We have shown how temporal and spatial integration of sensory signals converts noisy population responses into precise motor responses.

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.

Evidence for a retinal velocity memory underlying the direction of anticipatory smooth pursuit eye movements

2013 ◽  
Vol 110 (3) ◽  
pp. 732-747 ◽  
Author(s):  
T. Scott Murdison ◽  
Chanel A. Paré-Bingley ◽  
Gunnar Blohm
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Target Velocity ◽  
Smooth Pursuit Eye Movements ◽  
Ocular Torsion ◽  
Pursuit Eye Movements ◽  
Ocular Counterroll ◽  
In Series ◽  
Head Roll ◽  
Directional Component

To compute spatially correct smooth pursuit eye movements, the brain uses both retinal motion and extraretinal signals about the eyes and head in space ( Blohm and Lefèvre 2010 ). However, when smooth eye movements rely solely on memorized target velocity, such as during anticipatory pursuit, it is unknown if this velocity memory also accounts for extraretinal information, such as head roll and ocular torsion. To answer this question, we used a novel behavioral updating paradigm in which participants pursued a repetitive, spatially constant fixation-gap-ramp stimulus in series of five trials. During the first four trials, participants' heads were rolled toward one shoulder, inducing ocular counterroll (OCR). With each repetition, participants increased their anticipatory pursuit gain, indicating a robust encoding of velocity memory. On the fifth trial, they rolled their heads to the opposite shoulder before pursuit, also inducing changes in ocular torsion. Consequently, for spatially accurate anticipatory pursuit, the velocity memory had to be updated across changes in head roll and ocular torsion. We tested how the velocity memory accounted for head roll and OCR by observing the effects of changes to these signals on anticipatory trajectories of the memory decoding (fifth) trials. We found that anticipatory pursuit was updated for changes in head roll; however, we observed no evidence of compensation for OCR, representing the absence of ocular torsion signals within the velocity memory. This indicated that the directional component of the memory must be coded retinally and updated to account for changes in head roll, but not OCR.

MST Neuronal Responses to Heading Direction During Pursuit Eye Movements

1999 ◽  
Vol 81 (2) ◽  
pp. 596-610 ◽  
Author(s):  
William K. Page ◽  
Charles J. Duffy
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Neuronal Population ◽  
Smooth Pursuit Eye Movements ◽  
Neuronal Responses ◽  
Temporal Area ◽  
Pursuit Eye Movements ◽  
Heading Direction ◽  
Monkey Visual Cortex

MST neuronal responses to heading direction during pursuit eye movements. As you move through the environment, you see a radial pattern of visual motion with a focus of expansion (FOE) that indicates your heading direction. When self-movement is combined with smooth pursuit eye movements, the turning of the eye distorts the retinal image of the FOE but somehow you still can perceive heading. We studied neurons in the medial superior temporal area (MST) of monkey visual cortex, recording responses to FOE stimuli presented during fixation and smooth pursuit eye movements. Almost all neurons showed significant changes in their FOE selective responses during pursuit eye movements. However, the vector average of all the neuronal responses indicated the direction of the FOE during both fixation and pursuit. Furthermore, the amplitude of the net vector increased with increasing FOE eccentricity. We conclude that neuronal population encoding in MST might contribute to pursuit-tolerant heading perception.

Role of the Cerebellar Flocculus Region in the Coordination of Eye and Head Movements During Gaze Pursuit

2000 ◽  
Vol 84 (3) ◽  
pp. 1614-1626 ◽  
Author(s):  
Timothy Belton ◽  
Robert A. McCrea
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Head Movements ◽  
Whole Body ◽  
Head Tracking ◽  
Smooth Pursuit Eye Movements ◽  
Body Rotation ◽  
Pursuit Eye Movements ◽  
Smooth Tracking ◽  
Eye Velocity

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive (≈43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.

scholarly journals Asymmetric smooth pursuit eye movements and visual motion reaction time

2019 ◽  
Vol 7 (14) ◽  
Author(s):  
Seiji Ono ◽  
Kenichiro Miura ◽  
Takashi Kawamura ◽  
Tomohiro Kizuka
Keyword(s):  
Eye Movements ◽  
Reaction Time ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements

scholarly journals Temporal dynamics of retinal and extraretinal signals in the FEFsem during smooth pursuit eye movements

2017 ◽  
Vol 117 (5) ◽  
pp. 1987-2003 ◽  
Author(s):  
Leah Bakst ◽  
Jérome Fleuriet ◽  
Michael J. Mustari
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Clustering Algorithm ◽  
Critical Role ◽  
Image Motion ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Eye Field ◽  
Eye Velocity

Neurons in the smooth eye movement subregion of the frontal eye field (FEFsem) are known to play an important role in voluntary smooth pursuit eye movements. Underlying this function are projections to parietal and prefrontal visual association areas and subcortical structures, all known to play vital but differing roles in the execution of smooth pursuit. Additionally, the FEFsem has been shown to carry a diverse array of signals (e.g., eye velocity, acceleration, gain control). We hypothesized that distinct subpopulations of FEFsem neurons subserve these diverse functions and projections, and that the relative weights of retinal and extraretinal signals could form the basis for categorization of units. To investigate this, we used a step-ramp tracking task with a target blink to determine the relative contributions of retinal and extraretinal signals in individual FEFsem neurons throughout pursuit. We found that the contributions of retinal and extraretinal signals to neuronal activity and behavior change throughout the time course of pursuit. A clustering algorithm revealed three distinct neuronal subpopulations: cluster 1 was defined by a higher sensitivity to eye velocity, acceleration, and retinal image motion; cluster 2 had greater activity during blinks; and cluster 3 had significantly greater eye position sensitivity. We also performed a comparison with a sample of medial superior temporal neurons to assess similarities and differences between the two areas. Our results indicate the utility of simple tests such as the target blink for parsing the complex and multifaceted roles of cortical areas in behavior. NEW & NOTEWORTHY The frontal eye field (FEF) is known to play a critical role in volitional smooth pursuit, carrying a variety of signals that are distributed throughout the brain. This study used a novel application of a target blink task during step ramp tracking to determine, in combination with a clustering algorithm, the relative contributions of retinal and extraretinal signals to FEF activity and the extent to which these contributions could form the basis for a categorization of neurons.

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