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 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 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 Gain Control in Human Smooth-Pursuit Eye Movements

2002 ◽  
Vol 87 (6) ◽  
pp. 2936-2945 ◽  
Author(s):  
Anne K. Churchland ◽  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Gain Control ◽  
Sine Wave ◽  
Target Motion ◽  
Smooth Pursuit Eye Movements ◽  
Target Speed ◽  
Pursuit Eye Movements ◽  
On Line ◽  
Visual Motor

In previous experiments, on-line modulation of the gain of visual-motor transmission for pursuit eye movements was demonstrated in monkeys by showing that the response to a brief perturbation of target motion was strongly enhanced during pursuit relative to during fixation. The present paper elaborates the properties of on-line gain control by recording the smooth-pursuit eye movements of human subjects during tracking of a spot target. When perturbations consisted of one cycle of a 5-Hz sine wave, responses were significantly larger during pursuit than during fixation. Furthermore, responses grew as a function of eye/target velocity at the time of the perturbation and of perturbation amplitude. Thus human pursuit, like monkey pursuit, is modulated by on-line gain control. For larger perturbations consisting of a single sine wave at 2.8 Hz, ±19°/s, the degree of enhancement depended strongly on the phase of the perturbation. Enhancement was present when “peak-first” perturbations caused the target speed to increase first and was attenuated when “peak-last” perturbations caused target speed to decrease first. This effect was most profound when the perturbation was 2.8 Hz, ±19°/s but was also present when the amplitude of the peak-last perturbation was ±5o/s. For peak-last perturbations, the eye velocity evoked by the later peak of the perturbation was inversely related to that evoked by the preceding trough of the perturbation. We interpret these effects of perturbation phase as evidence that peak-last perturbations cause a decrease in the on-line gain of visual-motor transmission for pursuit. We conclude that gain control is modulated dynamically as behavioral conditions change. Finally, when perturbations were presented as a sequence of three large, peak-last sine waves starting at the onset of target motion at 10°/s, repeating the conditions used in prior studies on humans, we were able to replicate the prior finding that the response to the perturbations was equal during pursuit and fixation. We conclude that on-line gain control modulates human pursuit and that it can be probed most reliably with small, brief perturbations that do not affect the on-line gain themselves.

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.

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 Objective Dynamic Visual Acuity Assessment Method Based on Steady-State Visual Evoked Potentials with Smooth-Pursuit Eye Movements Recording

2021 ◽  
Vol 21 (9) ◽  
pp. 2452
Author(s):  
Chenghang Du ◽  
GUANGHUA XU ◽  
XIAOWEI ZHENG ◽  
KAI ZHANG ◽  
PEIYUAN TIAN ◽  
...  
Keyword(s):  
Visual Acuity ◽  
Steady State ◽  
Eye Movements ◽  
Evoked Potentials ◽  
Visual Evoked Potentials ◽  
Smooth Pursuit ◽  
Assessment Method ◽  
Smooth Pursuit Eye Movements ◽  
Dynamic Visual Acuity ◽  
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.

scholarly journals Scaling of anticipatory smooth pursuit eye movements with target speed probability

2010 ◽  
Vol 8 (6) ◽  
pp. 665-665 ◽  
Author(s):  
D. Souto ◽  
A. Montagnini ◽  
G. S. Masson
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Smooth Pursuit Eye Movements ◽  
Target Speed ◽  
Pursuit Eye Movements

Similar Kinematic Properties for Ocular Following and Smooth Pursuit Eye Movements

2005 ◽  
Vol 93 (3) ◽  
pp. 1710-1717 ◽  
Author(s):  
Babatunde Adeyemo ◽  
Dora E. Angelaki
Keyword(s):  
Steady State ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Eye Position ◽  
Vestibuloocular Reflex ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Initial Fixation ◽  
Ocular Following ◽  
Kinematic Properties

Ocular following (OFR) is a short-latency visual stabilization response to the optic flow experienced during self-motion. It has been proposed that it represents the early component of optokinetic nystagmus (OKN) and that it is functionally linked to the vestibularly driven stabilization reflex during translation (translational vestibuloocular reflex, TVOR). Because no single eye movement can eliminate slip from the whole retina during translation, the OFR and the TVOR appear to be functionally related to maintaining visual acuity on the fovea. Other foveal-specific eye movements, like smooth pursuit and saccades, exhibit an eye-position-dependent torsional component, as dictated by what is known as the “half-angle rule” of Listing's law. In contrast, eye movements that stabilize images on the whole retina, such as the rotational vestibuloocular reflex (RVOR) and steady-state OKN do not. Consistent with the foveal stabilization hypothesis, it was recently shown that the TVOR is indeed characterized by an eye-position-dependent torsion, similar to pursuit eye movements. Here we have investigated whether the OFR exhibits three-dimensional kinematic properties consistent with a foveal response (i.e., similar to the TVOR and smooth pursuit eye movements) or with a whole-field stabilization function (similar to steady-state OKN). The OFR was elicited using 100-ms ramp motion of a full-field random dot pattern that moved horizontally at 20, 62, or 83°/s. To study if an eye-position-dependent torsion is generated during the OFR, we varied the initial fixation position vertically within a range of ±20°. As a control, horizontal smooth pursuit eye movements were also elicited using step-ramp target motion (10, 20, or 30°/s) at similar eccentric positions. We found that the OFR followed kinematic properties similar to those seen in pursuit and the TVOR with the eye-position-dependent torsional tilt of eye velocity having slopes that averaged 0.73 ± 0.16 for OFR and 0.57 ± 0.12 (means ± SD) for pursuit. These findings support the notion that the OFR, like the TVOR and pursuit, are foveal image stabilization systems.

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.

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