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

2009 ◽  
Vol 102 (4) ◽  
pp. 2013-2025 ◽  
Author(s):  
Leslie C. Osborne ◽  
Stephen G. Lisberger

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.

1994 ◽  
Vol 11 (3) ◽  
pp. 411-424 ◽  
Author(s):  
Joshua D. Schwartz ◽  
Stephen G. Lisberger

AbstractSmooth pursuit eye movements allow primates to keep gaze pointed at small objects moving across stationary surroundings. In monkeys trained to track a small moving target, we have injected brief perturbations of target motion under different initial conditions as probes to read out the state of the visuo-motor pathways that guide pursuit. A large eye movement response was evoked if the perturbation was applied to a moving target the monkey was tracking. A small response was evoked if the same perturbation was applied to a stationary target the monkey was fixating. The gain of the response to the perturbation increased as a function of the initial speed of target motion and as a function of the interval from the onset of target motion to the time of the perturbation. The response to the perturbation also was direction selective. Gain was largest if the perturbation was along the axis of ongoing target motion and smallest if the perturbation was orthogonal to the axis of target motion. We suggest that two parallel sets of visual motion pathways through the extrastriate visual cortex may mediate, respectively, the visuo-motor processing for pursuit and the modulation of the gain of transmission through those pathways.


1998 ◽  
Vol 79 (4) ◽  
pp. 1918-1930 ◽  
Author(s):  
Stephen G. Lisberger

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.


1999 ◽  
Vol 81 (2) ◽  
pp. 596-610 ◽  
Author(s):  
William K. Page ◽  
Charles J. Duffy

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.


2019 ◽  
Vol 7 (14) ◽  
Author(s):  
Seiji Ono ◽  
Kenichiro Miura ◽  
Takashi Kawamura ◽  
Tomohiro Kizuka

2020 ◽  
Vol 123 (3) ◽  
pp. 1265-1276 ◽  
Author(s):  
Stuart Behling ◽  
Stephen G. Lisberger

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.


2011 ◽  
Vol 106 (2) ◽  
pp. 741-753 ◽  
Author(s):  
Yu-Qiong Niu ◽  
Stephen G. Lisberger

We have investigated how visual motion signals are integrated for smooth pursuit eye movements by measuring the initiation of pursuit in monkeys for pairs of moving stimuli of the same or differing luminance. The initiation of pursuit for pairs of stimuli of the same luminance could be accounted for as a vector average of the responses to the two stimuli singly. When stimuli comprised two superimposed patches of moving dot textures, the brighter stimulus suppressed the inputs from the dimmer stimulus, so that the initiation of pursuit became winner-take-all when the luminance ratio of the two stimuli was 8 or greater. The dominance of the brighter stimulus could be not attributed to either the latency difference or the ratio of the eye accelerations for the bright and dim stimuli presented singly. When stimuli comprised either spot targets or two patches of dots moving across separate locations in the visual field, the brighter stimulus had a much weaker suppressive influence; the initiation of pursuit could be accounted for by nearly equal vector averaging of the responses to the two stimuli singly. The suppressive effects of the brighter stimulus also appeared in human perceptual judgments, but again only for superimposed stimuli. We conclude that one locus of the interaction of two moving visual stimuli is shared by perception and action and resides in local inhibitory connections in the visual cortex. A second locus resides deeper in sensory-motor processing and may be more closely related to action selection than to stimulus selection.


2015 ◽  
Vol 113 (10) ◽  
pp. 3954-3960 ◽  
Author(s):  
Jude F. Mitchell ◽  
Nicholas J. Priebe ◽  
Cory T. Miller

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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