Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey

1. We have investigated the mechanism of a directional deficit in vertical pursuit eye movements in a monkey that was unable to match upward eye speed to target speed but that had pursuit within the normal range for downward or horizontal target motion. Except for a difference in the axis of deficient pursuit, the symptoms in this monkey were similar to those seen with lesions in the frontal or parietal lobes of the cerebral cortex in humans or monkeys. Our evaluation of vertical pursuit in this monkey suggests a new interpretation for the role of the frontal and parietal lobes in pursuit. 2. The up/down asymmetry was most pronounced for target motion at speeds greater than or equal to 2 degree/s. For target motion at 15 or 30 degree/s, upward step-ramp target motion evoked a brief upward smooth eye acceleration, followed by tracking that consisted largely of saccades. Downward step-ramp target motion evoked a prolonged smooth eye acceleration, followed by smooth, accurate tracking. 3. Varying the amplitude of the target step revealed that the deficit was similar for targets moving across all locations of the visual field. Eye acceleration in the interval 0-20 ms after the onset of pursuit was independent of initial target position and was symmetrical for upward and downward target motion. Eye acceleration in the interval 60-80 ms after the onset of pursuit showed a large asymmetry. For upward target motion, eye acceleration in this interval was small and did not depend on initial target position. For downward target motion, eye acceleration depended strongly on initial target position and was large when the target started close to the position of fixation. 4. We next attempted to understand the mechanism of the up/down asymmetry by evaluating the monkey's vertical motion processing and vertical eye movements under a variety of tracking conditions. For spot targets, the response to upward image motion was similar to that in normal monkeys if the image motion was presented during downward pursuit. In addition, the monkey with deficient upward pursuit was able to use upward image motion to make accurate saccades to moving targets. We conclude that the visual processing of upward image motion was normal in this monkey and that an asymmetry in visual motion processing could not account for the deficit in his upward pursuit. 5. Upward smooth eye acceleration was normal when the spot target was moved together with a large textured pattern.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Topographic and directional organization of visual motion inputs for the initiation of horizontal and vertical smooth-pursuit eye movements in monkeys

Journal of Neurophysiology ◽

10.1152/jn.1989.61.1.173 ◽

1989 ◽

Vol 61 (1) ◽

pp. 173-185 ◽

Cited By ~ 46

Author(s):

S. G. Lisberger ◽

T. A. Pavelko

Keyword(s):

Eye Movements ◽

Visual Field ◽

Visual Motion ◽

Target Position ◽

Target Motion ◽

Visual Signals ◽

Motion Processing ◽

Pursuit Eye Movements ◽

Visual Inputs ◽

Initial Target

1. The goal of our study was to determine the properties of the visual inputs for pursuit eye movements. In a previous study we presented horizontal target motion along the horizontal meridian and showed that targets were more effective if they moved across the center of the visual field. We have now analyzed the topographic weighting of the inputs for pursuit in greater detail, using targets that moved in all directions and across a wide area of the visual field. 2. Monkeys were rewarded for tracking targets that started at 48 positions in the visual field. The initial positions were spaced equally around 4 circles that were centered at the position of fixation and had radii of 3, 6, 9, and 12 degrees. Targets moved horizontally or vertically at 30 degrees/s. We measured the smooth eye acceleration in the first 80 ms after the initiation of pursuit, before there had been time for visual feedback to affect the position or velocity of the retinal images from the target. 3. For both horizontal and vertical target motion, there were major differences between the early and late intervals in the first 80 ms of pursuit. In the first 20 ms eye acceleration was largely independent of initial target position. In later intervals eye acceleration decreased sharply as a function of initial target eccentricity. The later intervals also showed a pronounced toward/away asymmetry such that the initiation of pursuit was more vigorous for target motion toward than for motion away from the horizontal or vertical meridian. 4. Comparison of the topographic organization of the middle temporal visual area (MT) with our data on pursuit suggests that the topography of cortical maps is smoothed when the visual signals are transmitted to the pursuit system. For example, the superior visual hemifield is underrepresented in cortical motion processing areas, but target motion in the superior and inferior visual hemifields is equally effective for the initiation of pursuit. 5. We investigated the directional organization of the visual inputs for pursuit by presenting targets that started at 6 degrees eccentric and moved in 16 different directions. Horizontal target motion always evoked larger eye accelerations than did vertical target motion. Target motion in oblique directions evoked intermediate values of eye acceleration. 6. Our data show two classes of variation in pursuit performance. First, some subjects showed ideosyncratic variations that were restricted to one hemifield or one direction of target motion. We attribute these variations to differences among subjects in the physiology of visual pathways.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Visual motion processing for the initiation of smooth-pursuit eye movements in humans

Journal of Neurophysiology ◽

10.1152/jn.1986.56.4.953 ◽

1986 ◽

Vol 56 (4) ◽

pp. 953-968 ◽

Cited By ~ 150

Author(s):

L. Tychsen ◽

S. G. Lisberger

Keyword(s):

Eye Movements ◽

Visual Field ◽

Functional Organization ◽

Target Motion ◽

Motion Processing ◽

Lower Visual Field ◽

Pursuit Eye Movements ◽

Pursuit Initiation ◽

Visual Motion Processing ◽

Visual Properties

We have used the initiation of pursuit eye movements as a tool to reveal properties of motion processing in the neural pathways that provide inputs to the human pursuit system. Horizontal and vertical eye position were recorded with a magnetic search coil in six normal adults. Stimuli were provided by individual trials of ramp target motion. Analysis was restricted to the first 100 ms of eye movement, which precedes the onset of corrective feedback. By recording the transient response to target motion at speeds the pursuit motor system can achieve, we investigated the visual properties of images that initiate pursuit. We have found effects of varying the retinal location, the direction, the velocity, the intensity, and the size of the stimulus. Eye acceleration in the first 100 ms of pursuit depended on both the direction of target motion and the initial position of the moving target. For horizontal target motion, eye acceleration was highest if the stimulus was close to the center of the visual field and moved toward the vertical meridian. For vertical target motion, eye acceleration was highest when the stimulus moved upward or downward within the lower visual field. The shape of the relationship between eye acceleration and initial target position was similar for target velocities ranging from 1.0 to 45 degrees/s. The initiation of pursuit showed two components that had different visual properties and were expressed early and late in the first 100 ms of pursuit. In the first 20 ms, instantaneous eye acceleration was in the direction of target motion but did not depend on other visual properties of the stimulus. At later times (e.g., 80-100 ms after pursuit initiation), instantaneous eye acceleration was strongly dependent on each property we tested. Targets that started close to and moved toward the position of fixation evoked the highest eye accelerations. For high-intensity targets, eye acceleration increased steadily as target velocity increased. For low-intensity targets, eye acceleration was selective for target velocities of 30-45 degrees/s. The properties of pursuit initiation in humans, including the differences between the early and late components, are remarkably similar to those reported by Lisberger and Westbrook (12) in monkeys. Our data provide evidence that the cell populations responsible for motion processing are similar in humans and monkeys and imply that the functional organization of the visual cortex is similar in the two species.

Download Full-text

Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST

Journal of Neurophysiology ◽

10.1152/jn.1988.60.3.940 ◽

1988 ◽

Vol 60 (3) ◽

pp. 940-965 ◽

Cited By ~ 213

Author(s):

M. R. Dursteler ◽

R. H. Wurtz

Keyword(s):

Eye Movements ◽

Visual Field ◽

Visual Motion ◽

Ibotenic Acid ◽

Motion Processing ◽

Temporal Area ◽

Target Speed ◽

Pursuit Eye Movements ◽

Medial Superior Temporal ◽

Visual Motion Processing

1. Previous experiments have shown that punctate chemical lesions within the middle temporal area (MT) of the superior temporal sulcus (STS) produce deficits in the initiation and maintenance of pursuit eye movements (10, 34). The present experiments were designed to test the effect of such chemical lesions in an area within the STS to which MT projects, the medial superior temporal area (MST). 2. We injected ibotenic acid into localized regions of MST, and we observed two deficits in pursuit eye movements, a retinotopic deficit and a directional deficit. 3. The retinotopic deficit in pursuit initiation was characterized by the monkey's inability to match eye speed to target speed or to adjust the amplitude of the saccade made to acquire the target to compensate for target motion. This deficit was related to the initiation of pursuit to targets moving in any direction in the visual field contralateral to the side of the brain with the lesion. This deficit was similar to the deficit we found following damage to extrafoveal MT except that the affected area of the visual field frequently extended throughout the entire contralateral visual field tested. 4. The directional deficit in pursuit maintenance was characterized by a failure to match eye speed to target speed once the fovea had been brought near the moving target. This deficit occurred only when the target was moving toward the side of the lesion, regardless of whether the target began to move in the ipsilateral or contralateral visual field. There was no deficit in the amplitude of saccades made to acquire the target, or in the amplitude of the catch-up saccades made to compensate for the slowed pursuit. The directional deficit is similar to the one we described previously following chemical lesions of the foveal representation in the STS. 5. Retinotopic deficits resulted from any of our injections in MST. Directional deficits resulted from lesions limited to subregions within MST, particularly lesions that invaded the floor of the STS and the posterior bank of the STS just lateral to MT. Extensive damage to the densely myelinated area of the anterior bank or to the posterior parietal area on the dorsal lip of the anterior bank produced minimal directional deficits. 6. We conclude that damage to visual motion processing in MST underlies the retinotopic pursuit deficit just as it does in MT. MST appears to be a sequential step in visual motion processing that occurs before all of the visual motion information is transmitted to the brainstem areas related to pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

The effect of a moving distractor on the initiation of smooth-pursuit eye movements

Visual Neuroscience ◽

10.1017/s0952523800011457 ◽

1997 ◽

Vol 14 (2) ◽

pp. 323-338 ◽

Cited By ~ 28

Author(s):

Vincent P. Ferrera ◽

Stephen G. Lisberger

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Smooth Pursuit ◽

Visual Motion ◽

Target Selection ◽

Motion Processing ◽

Smooth Pursuit Eye Movements ◽

Response Preparation ◽

Pursuit Eye Movements ◽

Visual Motion Processing

AbstractAs a step toward understanding the mechanism by which targets are selected for smooth-pursuit eye movements, we examined the behavior of the pursuit system when monkeys were presented with two discrete moving visual targets. Two rhesus monkeys were trained to select a small moving target identified by its color in the presence of a moving distractor of another color. Smooth-pursuit eye movements were quantified in terms of the latency of the eye movement and the initial eye acceleration profile. We have previously shown that the latency of smooth pursuit, which is normally around 100 ms, can be extended to 150 ms or shortened to 85 ms depending on whether there is a distractor moving in the opposite or same direction, respectively, relative to the direction of the target. We have now measured this effect for a 360 deg range of distractor directions, and distractor speeds of 5–45 deg/s. We have also examined the effect of varying the spatial separation and temporal asynchrony between target and distractor. The results indicate that the effect of the distractor on the latency of pursuit depends on its direction of motion, and its spatial and temporal proximity to the target, but depends very little on the speed of the distractor. Furthermore, under the conditions of these experiments, the direction of the eye movement that is emitted in response to two competing moving stimuli is not a vectorial combination of the stimulus motions, but is solely determined by the direction of the target. The results are consistent with a competitive model for smooth-pursuit target selection and suggest that the competition takes place at a stage of the pursuit pathway that is between visual-motion processing and motor-response preparation.

Download Full-text

Effect of changing feedback delay on spontaneous oscillations in smooth pursuit eye movements of monkeys

Journal of Neurophysiology ◽

10.1152/jn.1992.67.3.625 ◽

1992 ◽

Vol 67 (3) ◽

pp. 625-638 ◽

Cited By ~ 77

Author(s):

D. Goldreich ◽

R. J. Krauzlis ◽

S. G. Lisberger

Keyword(s):

Eye Movements ◽

Visual Feedback ◽

Target Motion ◽

Image Motion ◽

Target Velocity ◽

Feedback Delay ◽

Total Delay ◽

Internal Feedback ◽

Pursuit Eye Movements ◽

Eye Velocity

1. Our goal was to discriminate between two classes of models for pursuit eye movements. The monkey's pursuit system and both classes of model exhibit oscillations around target velocity during tracking of ramp target motion. However, the mechanisms that determine the frequency of oscillations differ in the two classes of model. In "internal feedback" models, oscillations are controlled by internal feedback loops, and the frequency of oscillation does not depend strongly on the delay in visual feedback. In "image motion" models, oscillations are controlled by visual feedback, and the frequency of oscillation does depend on the delay in visual feedback. 2. We measured the frequency of oscillation during pursuit of ramp target motion as a function of the total delay for visual feedback. For the shortest feedback delays of approximately 70 ms, the frequency of oscillation was between 6 and 7 Hz. Increases in feedback delay caused decreases in the frequency of oscillation. The effect of increasing feedback delay was similar, whether the increases were produced naturally by dimming and decreasing the size of the tracking target or artificially with the computer. We conclude that the oscillations in eye velocity during pursuit of ramp target motion are controlled by visual inputs, as suggested by the image motion class of models. 3. Previous experiments had suggested that the visuomotor pathways for pursuit are unable to respond well to frequencies as high as the 6-7 Hz at which eye velocity oscillates in monkeys. We therefore tested the response to target vibration at an amplitude of +/- 8 degrees/s and frequencies as high as 15 Hz. For target vibration at 6 Hz, the gain of pursuit, defined as the amplitude of eye velocity divided by the amplitude of target velocity, was as high as 0.65. We conclude that the visuomotor pathways for pursuit are capable of processing image motion at high temporal frequencies. 4. The gain of pursuit was much larger when the target vibrated around a constant speed of 15 degrees/s than when it vibrated around a stationary position. This suggests that the pursuit pathways contain a switch that must be closed to allow the visuomotor pathways for pursuit to operate at their full gain. The switch apparently remains open for target vibration around a stationary position. 5. The responses to target vibration revealed a frequency at which eye velocity lagged target velocity by 180 degrees and at which one monkey showed a local peak in the gain of pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque

Journal of Neurophysiology ◽

10.1152/jn.1988.60.2.664 ◽

1988 ◽

Vol 60 (2) ◽

pp. 664-686 ◽

Cited By ~ 94

Author(s):

M. J. Mustari ◽

A. F. Fuchs ◽

J. Wallman

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Visual Sensitivity ◽

Large Field ◽

Motion Processing ◽

Smooth Pursuit Eye Movements ◽

Pontine Nucleus ◽

Stimulus Velocity ◽

Pursuit Eye Movements ◽

Visual Motion Processing

1. The anatomical connections of the dorsolateral pontine nucleus (DLPN) implicate it in the production of smooth-pursuit eye movements. It receives inputs from cortical structures believed to be involved in visual motion processing (middle temporal cortex) or motion execution (posterior parietal cortex) and projects to the flocculus of the cerebellum, which is involved in smooth pursuit. To determine the role of the DLPN in smooth pursuit, we have studied the discharge patterns of 191 DLPN neurons in five monkeys trained to make smooth-pursuit eye movements of a spot moving either across a patterned background or in darkness. 2. Four unit types could be distinguished. Visual units (15%) discharged in response to movement of a large textured pattern, often in a direction-selective fashion but not during smooth pursuit of a spot in the dark. Eye movement neurons (31%) discharged during sinusoidal smooth pursuit in the dark with peak discharge rate either at peak eye position or peak eye velocity, but they showed no response during background movement or during other visual stimulation. These units continued to discharge when the target was extinguished (blanked) briefly, and the monkey continued to make smooth eye movements in the dark. The majority (54%) of our DLPN units discharged during both smooth pursuit in the dark and background movement while the monkey fixated. Blanking the target during smooth pursuit revealed that these units fell into two distinct classes. Visual pursuit units ceased discharging during a blank, suggesting that they had only a visual sensitivity. Pursuit and visual units continued to discharge during the blank, indicating that they had a combined oculomotor and visual sensitivity. 3. Ninety-five percent of the units that discharged during smooth pursuit were direction selective. These units had rather broad directional tuning curves with widths at half height ranging from 65 to 180 degrees. Many preferred directions for DLPN units were observed, although the vertical and near-vertical directions predominated. 4. Most units that responded to large-field background movement were direction selective. During sinusoidal movement of a large-field background, half of them also discharged in relation to stimulus velocity, whereas others did not.

Download Full-text

Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons

Journal of Neurophysiology ◽

10.1152/jn.1988.60.2.580 ◽

1988 ◽

Vol 60 (2) ◽

pp. 580-603 ◽

Cited By ~ 344

Author(s):

H. Komatsu ◽

R. H. Wurtz

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Visual Motion ◽

Receptive Fields ◽

Motion Processing ◽

Temporal Area ◽

Pursuit Eye Movements ◽

Visual Motion Processing ◽

Visual Areas ◽

Visual Properties

1. Among the multiple extrastriate visual areas in monkey cerebral cortex, several areas within the superior temporal sulcus (STS) are selectively related to visual motion processing. In this series of experiments we have attempted to relate this visual motion processing at a neuronal level to a behavior that is dependent on such processing, the generation of smooth-pursuit eye movements. 2. We studied two visual areas within the STS, the middle temporal area (MT) and the medial superior temporal area (MST). For the purposes of this study, MT and MST were defined functionally as those areas within the STS having a high proportion of directionally selective neurons. MST was distinguished from MT by using the established relationship of receptive-field size to eccentricity, with MST having larger receptive fields than MT. 3. A subset of these visually responsive cells within the STS were identified as pursuit cells--those cells that discharge during smooth pursuit of a small target in an otherwise dark room. Pursuit cells were found only in localized regions--in the foveal region of MT (MTf), in a dorsal-medial area of MST on the anterior bank of the STS (MSTd), and in a lateral-anterior area of MST on the floor and the posterior bank of the STS (MST1). 4. Pursuit cells showed two characteristics in common when their visual properties were studied while the monkey was fixating. Almost all cells showed direction selectivity for moving stimuli and included the fovea within their receptive fields. 5. The visual response of pursuit cells in the several areas differed in two ways. Cells in MTf preferred small moving spots of light, whereas cells in MSTd preferred large moving stimuli, such as a pattern of random dots. Cells in MTf had small receptive fields; those in MSTd usually had large receptive fields. Visual responses of pursuit neurons in MST1 were heterogeneous; some resembled those in MTf, whereas others were similar to those in MSTd. This suggests that the pursuit cells in MSTd and MST1 belong to different subregions of MST.

Download Full-text

Postsaccadic Enhancement of Initiation of Smooth Pursuit Eye Movements in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.1998.79.4.1918 ◽

1998 ◽

Vol 79 (4) ◽

pp. 1918-1930 ◽

Cited By ~ 63

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.

Download Full-text