Cancellation of self-induced retinal image motion during smooth pursuit eye movements

Anatomical and physiological studies have shown that the “frontal pursuit area” (FPA) in the arcuate cortex of monkeys is involved in the control of smooth pursuit eye movements. To further analyze the signals carried by the FPA, we examined the activity of pursuit-related neurons recorded from a discrete region near the arcuate spur during a variety of oculomotor tasks. Pursuit neurons showed direction tuning with a wide range of preferred directions and a mean full width at half-maximum of 129°. Analysis of latency using the “receiver operating characteristic” to compare responses to target motion in opposite directions showed that the directional response of 58% of FPA neurons led the initiation of pursuit, while 19% led by 25 ms or more. Analysis of neuronal responses during pursuit of a range of target velocities revealed that the sensitivity to eye velocity was larger during the initiation of pursuit than during the maintenance of pursuit, consistent with two components of firing related to image motion and eye motion. FPA neurons showed correlates of two behavioral features of pursuit documented in prior reports. 1) Eye acceleration at the initiation of pursuit declines as a function of the eccentricity of the moving target. FPA neurons show decreased firing at the initiation of pursuit in parallel with the decline in eye acceleration. This finding is consistent with prior suggestions that the FPA plays a role in modulating the gain of visual-motor transmission for pursuit. 2) A stationary eccentric cue evokes a smooth eye movement opposite in direction to the cue and enhances the pursuit evoked by subsequent target motions. Many pursuit neurons in the FPA showed weak, phasic visual responses for stationary targets and were tuned for the positions about 4° eccentric on the side opposite to the preferred pursuit direction. However, few neurons (12%) responded during the preparation or execution of saccades. The responses to the stationary target could account for the behavioral effects of stationary, eccentric cues. Further analysis of the relationship between firing rate and retinal position error during pursuit in the preferred and opposite directions failed to provide evidence for a large contribution of image position to the firing of FPA neurons. We conclude that FPA processes information in terms of image and eye velocity and that it is functionally separate from the saccadic frontal eye fields, which processes information in terms of retinal image position.

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Illusory bending of a rigidly moving line segment: Effects of image motion and smooth pursuit eye movements

Journal of Vision ◽

10.1167/7.6.9 ◽

2007 ◽

Vol 7 (6) ◽

pp. 9 ◽

Cited By ~ 2

Author(s):

Lore Thaler ◽

James T. Todd ◽

Miriam Spering ◽

Karl R. Gegenfurtner

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Line Segment ◽

Image Motion ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Moving Line

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Partial Ablations of the Flocculus and Ventral Paraflocculus in Monkeys Cause Linked Deficits in Smooth Pursuit Eye Movements and Adaptive Modification of the VOR

Journal of Neurophysiology ◽

10.1152/jn.00768.2000 ◽

2002 ◽

Vol 87 (2) ◽

pp. 912-924 ◽

Cited By ~ 139

Author(s):

H. Rambold ◽

A. Churchland ◽

Y. Selig ◽

L. Jasmin ◽

S. G. Lisberger

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Large Fraction ◽

Head Rotation ◽

Head Movements ◽

Image Motion ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Vor Adaptation ◽

Ventral Paraflocculus

The vestibuloocular reflex (VOR) generates compensatory eye movements to stabilize visual images on the retina during head movements. The amplitude of the reflex is calibrated continuously throughout life and undergoes adaptation, also called motor learning, when head movements are persistently associated with image motion. Although the floccular-complex of the cerebellum is necessary for VOR adaptation, it is not known whether this function is localized in its anterior or posterior portions, which comprise the ventral paraflocculus and flocculus, respectively. The present paper reports the effects of partial lesions of the floccular-complex in five macaque monkeys, made either surgically or with stereotaxic injection of 3-nitropropionic acid (3-NP). Before and after the lesions, smooth pursuit eye movements were tested during sinusoidal and step-ramp target motion. Cancellation of the VOR was tested by moving a target exactly with the monkey during sinusoidal head rotation. The control VOR was tested during sinusoidal head rotation in the dark and during 30°/s pulses of head velocity. VOR adaptation was studied by having the monkeys wear ×2 or ×0.25 optics for 4–7 days. In two monkeys, bilateral lesions removed all of the flocculus except for parts of folia 1 and 2 but did not produce any deficits in smooth pursuit, VOR adaptation, or VOR cancellation. We conclude that the flocculus alone probably is not necessary for either pursuit or VOR learning. In two monkeys, unilateral lesions including a large fraction of the ventral paraflocculus produced small deficits in horizontal and vertical smooth pursuit, and mild impairments of VOR adaptation and VOR cancellation. We conclude that the ventral paraflocculus contributes to both behaviors. In one monkey, a bilateral lesion of the flocculus and ventral paraflocculus produced severe deficits smooth pursuit and VOR cancellation, and a complete loss of VOR adaptation. Considering all five cases together, there was a strong correlation between the size of the deficits in VOR learning and pursuit. We found the strongest correlation between the behavior deficits and the size of the lesion of the ventral paraflocculus, a weaker but significant correlation for the full floccular complex, and no correlation with the size of the lesion of the flocculus. We conclude that 1) lesions of the floccular complex cause linked deficits in smooth pursuit and VOR adaptation, and 2) the relevant portions of the structure are primarily in the ventral paraflocculus, although the flocculus may participate.

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Smooth pursuitlike eye movements evoked by microstimulation in macaque nucleus reticularis tegmenti pontis

Journal of Neurophysiology ◽

10.1152/jn.1996.76.5.3313 ◽

1996 ◽

Vol 76 (5) ◽

pp. 3313-3324 ◽

Cited By ~ 30

Author(s):

T. Yamada ◽

D. A. Suzuki ◽

R. D. Yee

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Current Intensity ◽

Image Motion ◽

Eye Position ◽

Smooth Pursuit Eye Movements ◽

Pontine Nucleus ◽

Nucleus Reticularis Tegmenti Pontis ◽

Pursuit Eye Movements ◽

Nucleus Reticularis

1. Smooth pursuitlike eye movements were evoked with low current microstimulation delivered to rostral portions of the nucleus reticularis tegmenti pontis (rNRTP) in alert macaques. Microstimulation sites were selected by the observation of modulations in single-cell firing rates that were correlated with periodic smoothpursuit eye movements. Current intensities ranged from 10 to 120 microA and were routinely < 40 microA. Microstimulation was delivered either in the dark with no fixation, 100 ms after a fixation target was extinguished, or during maintained fixation of a stationary or moving target. Evoked eye movements also were studied under open-loop conditions with the target image stabilized on the retina. 2. Eye movements evoked in the absence of a target rapidly accelerated to a constant velocity that was maintained for the duration of the microstimulation. Evoked eye speeds ranged from 3.7 to 23 deg/s and averaged 11 deg/s. Evoked eye speed appeared to be linearly related to initial eye position with a sensitivity to initial eye position that averaged 0.23 deg.s-1.deg-1. While some horizontal and oblique smooth eye movements were elicited, microstimulation resulted in upward eye movements in 89% of the sites. 3. Evoked eye speed was found to be dependent on microstimulation pulse frequency and current intensity. Within limits, evoked eye speed increased with increases in stimulation frequency or current intensity. For stimulation frequencies < 300–400 Hz, only smooth pursuit-like eye movements were evoked. At higher stimulation frequencies, accompanying saccades consistently were elicited. 4. Feedback of retinal image motion interacted with the evoked eye movements to decrease eye speed if the visual motion was in the opposite direction as the evoked, pursuit-like eye movements. 5. The results implicate rNRTP as part of the neuronal substrate that controls smooth-pursuit eye movements. NRTP appears to be divided functionally into a rostral, pursuit-related portion and a caudal, saccade-related area. rNRTP is a component of a corticopontocerebellar circuit that presumably involves the pursuit area of the frontal eye field and that parallels the middle and medial superior temporal cerebral cortical/dorsalateral pontine nucleus (MT/MST-DLPN-cerebellum) pathway known to be involved also with regulating smooth-pursuit eye movements.

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

Journal of Neurophysiology ◽

10.1152/jn.00786.2016 ◽

2017 ◽

Vol 117 (5) ◽

pp. 1987-2003 ◽

Cited By ~ 4

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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Choosing a foveal goal recruits the saccadic system during smooth pursuit

Journal of Neurophysiology ◽

10.1152/jn.00418.2017 ◽

2018 ◽

Vol 120 (2) ◽

pp. 489-496 ◽

Cited By ~ 4

Author(s):

Stephen J. Heinen ◽

Jeremy B. Badler ◽

Scott N. J. Watamaniuk

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Retinal Image ◽

Central Element ◽

Central Feature ◽

Smooth Pursuit Eye Movements ◽

Large Object ◽

Pursuit Eye Movements ◽

Saccadic System ◽

Catch Up

Models of smooth pursuit eye movements stabilize an object’s retinal image, yet pursuit is peppered with small, destabilizing “catch-up” saccades. Catch-up saccades might help follow a small, spot stimulus used in most pursuit experiments, since fewer of them occur with large stimuli. However, they can return when a large stimulus has a small central feature. It may be that a central feature on a large object automatically recruits the saccadic system. Alternatively, a cognitive choice is made that the feature is the pursuit goal, and the saccadic system is then recruited to pursue it. Observers pursued a 5-dot stimulus composed of a central dot surrounded by four peripheral dots arranged as a diamond. An attention task specified the pursuit goal as either the central element, or the diamond gestalt. Fewer catch-up saccades occurred with the Gestalt goal than with the central goal, although the additional saccades with the central goal neither enhanced nor impeded pursuit. Furthermore, removing the central element from the diamond goal further reduced catch-up saccade frequency, indicating that the central element automatically triggered some saccades. Higher saccade frequency was not simply due to narrowly focused attention, since attending a small peripheral diamond during pursuit elicited fewer saccades than attending the diamond positioned foveally. The results suggest some saccades are automatically elicited by a small central element, but when it is chosen as the pursuit goal the saccadic system is further recruited to pursue it. NEW & NOTEWORTHY Smooth-pursuit eye movements stabilize retinal image motion to prevent blur. Curiously, smooth pursuit is frequently supplemented by small catchup saccades that could reduce image clarity. Catchup saccades might only be needed to pursue small laboratory stimuli, as they are infrequent during large object pursuit. Yet large objects with central features revive them. Here, we show that voluntarily selecting a feature as the pursuit goal elicits saccades that do not help pursuit.

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Visual Tracking Neurons in Primate Area MST Are Activated by Smooth-Pursuit Eye Movements of an “Imaginary” Target

Journal of Neurophysiology ◽

10.1152/jn.00272.2003 ◽

2003 ◽

Vol 90 (3) ◽

pp. 1489-1502 ◽

Cited By ~ 64

Author(s):

Uwe J. Ilg ◽

Peter Thier

Keyword(s):

Eye Movements ◽

Visual Field ◽

Eye Movement ◽

Visual Tracking ◽

Smooth Pursuit ◽

Rhesus Monkeys ◽

Image Motion ◽

Eye Position ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements

Because smooth-pursuit eye movements (SPEM) can be executed only in the presence of a moving target, it has been difficult to attribute the neuronal activity observed during the execution of these eye movements to either sensory processing or to motor preparation or execution. Previously, we showed that rhesus monkeys can be trained to perform SPEM directed toward an “imaginary” target defined by visual cues confined to the periphery of the visual field. The pursuit of an “imaginary” target provides the opportunity to elicit SPEM without stimulating visual receptive fields confined to the center of the visual field. Here, we report that a subset of neurons [85 “ imaginary” visual tracking (iVT)-neurons] in area MST of 3 rhesus monkeys were identically activated during pursuit of a conventional, foveal dot target and the “imaginary” target. Because iVT-neurons did not respond to the presentation of a moving “imaginary” target during fixation of a stationary dot, we are able to exclude that responses to pursuit of the “imaginary” target were artifacts of stimulation of the visual field periphery. Neurons recorded from the representation of the central parts of the visual field in neighboring area MT, usually vigorously discharging during pursuit of foveal targets, in no case responded to pursuit of the “imaginary” target. This dissociation between MT and MST neurons supports the view that pursuit responses of MT neurons are the result of target image motion, whereas those of iVT-neurons in area MST reflect an eye movement–related signal that is nonretinal in origin. iVT-neurons fell into two groups, depending on the properties of the eye movement–related signal. Whereas most of them (71%) encoded eye velocity, a minority showed responses determined by eye position, irrespective of whether eye position was changed by smooth pursuit or by saccades. Only the former group exhibited responses that led the eye movement, which is a prerequisite for a causal role in the generation of SPEM.

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