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

2003 ◽  
Vol 90 (3) ◽  
pp. 1489-1502 ◽  
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.

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

1996 ◽  
Vol 76 (5) ◽  
pp. 3313-3324 ◽  
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.

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.

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

10.1167/7.6.9 ◽  
2007 ◽  
Vol 7 (6) ◽  
pp. 9 ◽  
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

A Control Systems Model of Smooth Pursuit Eye Movements with Realistic Emergent Properties

1989 ◽  
Vol 1 (1) ◽  
pp. 116-122 ◽  
Author(s):  
R. J. Krauzlis ◽  
S. G. Lisberger
Keyword(s):  
Eye Movements ◽  
Visual Tracking ◽  
Smooth Pursuit ◽  
Oculomotor System ◽  
Difficult Problem ◽  
Visual Signals ◽  
Emergent Properties ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Systems Model

Visual tracking of objects in a noisy environment is a difficult problem that has been solved by the primate oculomotor system, but remains unsolved in robotics. In primates, smooth pursuit eye movements match eye motion to target motion to keep the eye pointed at smoothly moving targets. We have used computer models as a tool to investigate possible computational strategies underlying this behavior. Here, we present a model based upon behavioral data from monkeys. The model emphasizes the variety of visual signals available for pursuit and, in particular, includes a sensitivity to the acceleration of retinal images. The model was designed to replicate the initial eye velocity response observed during pursuit of different target motions. The strength of the model is that it also exhibits a number of emergent properties that are seen in the behavior of both humans and monkeys. This suggests that the elements in the model capture important aspects of the mechanism of visual tracking by the primate smooth pursuit system.

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

2002 ◽  
Vol 87 (2) ◽  
pp. 912-924 ◽  
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.

scholarly journals Responses of Purkinje cells in the oculomotor vermis of monkeys during smooth pursuit eye movements and saccades: comparison with floccular complex

2017 ◽  
Vol 118 (2) ◽  
pp. 986-1001 ◽  
Author(s):  
Ramanujan T. Raghavan ◽  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Purkinje Cells ◽  
Smooth Pursuit ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Oculomotor Vermis

The midline oculomotor cerebellum plays a different role in smooth pursuit eye movements compared with the lateral, floccular complex and appears to be much less involved in direction learning in pursuit. The output from the oculomotor vermis during pursuit lies along a null-axis for saccades and vice versa. Thus the vermis can play independent roles in the two kinds of eye movement.

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.

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.

Ablation of the pursuit area in the frontal cortex of the primate degrades foveal but not optokinetic smooth eye movements

1996 ◽  
Vol 76 (1) ◽  
pp. 637-641 ◽  
Author(s):  
E. G. Keating ◽  
A. Pierre ◽  
S. Chopra
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Frontal Cortex ◽  
Frontal Lobe ◽  
Relative Motion ◽  
Smooth Pursuit ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Motion Detectors ◽  
Do So

1. Neural pathology which impairs foveal smooth pursuit eye movements typically also degrades optokinetic pursuit of large textures, suggesting that the two kinds of pursuit share a common circuit. This study reports an exception. After sequential bilateral ablation of the pursuit area in the frontal lobe three monkeys displayed degraded pursuit of a small foveal target but performed normally on identical measures of optokinetic pursuit. 2. A related experiment in one subject demonstrated a pursuit deficit when the foveal target moved relative to the background, but not when background and target moved together. The frontal pursuit area may specifically control pursuit of relative motion, and do so by receiving signals primarily from motion detectors in the macular part of the visual field.

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