Contrast and assimilation in visual motion processing for perception and smooth pursuit eye movements

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.

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Memory and Decision Making in the Frontal Cortex during Visual Motion Processing for Smooth Pursuit Eye Movements

Neuron ◽

10.1016/j.neuron.2009.05.010 ◽

2009 ◽

Vol 62 (5) ◽

pp. 717-732 ◽

Cited By ~ 42

Author(s):

Natsuko Shichinohe ◽

Teppei Akao ◽

Sergei Kurkin ◽

Junko Fukushima ◽

Chris R.S. Kaneko ◽

...

Keyword(s):

Decision Making ◽

Eye Movements ◽

Frontal Cortex ◽

Smooth Pursuit ◽

Visual Motion ◽

Motion Processing ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Visual Motion Processing

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Visual Motion Processing and Sensory-Motor Integration for Smooth Pursuit Eye Movements

Annual Review of Neuroscience ◽

10.1146/annurev.ne.10.030187.000525 ◽

1987 ◽

Vol 10 (1) ◽

pp. 97-129 ◽

Cited By ~ 412

Author(s):

S G Lisberger ◽

E J Morris ◽

L Tychsen

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Visual Motion ◽

Motion Processing ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Visual Motion Processing ◽

Sensory Motor

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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.

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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.

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

Journal of Neurophysiology ◽

10.1152/jn.00611.2009 ◽

2009 ◽

Vol 102 (4) ◽

pp. 2013-2025 ◽

Cited By ~ 8

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.

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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)

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MST Neuronal Responses to Heading Direction During Pursuit Eye Movements

Journal of Neurophysiology ◽

10.1152/jn.1999.81.2.596 ◽

1999 ◽

Vol 81 (2) ◽

pp. 596-610 ◽

Cited By ~ 66

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.

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