Supplementary Eye Fields Stimulation Facilitates Anticipatory Pursuit

2004 ◽  
Vol 92 (2) ◽  
pp. 1257-1262 ◽  
Author(s):  
M. Missal ◽  
S. J. Heinen

Anticipatory movements are motor responses occurring before likely sensory events in contrast to reflexive actions. Anticipatory movements are necessary to compensate for delays present in sensory and motor systems. Smooth pursuit eye movements are often used as a paradigmatic example for the study of anticipation. However, the neural control of anticipatory pursuit is unknown. A previous study suggested that the supplementary eye fields (SEFs) could play a role in the guidance of smooth pursuit to predictable target motion. In this study, we favored anticipatory responses in monkeys by making the parameters of target motion highly predictable and electrically stimulated the SEF before and during this behavior. Stimulation sites were restricted to regions of the SEF where saccades could not be evoked at the same low currents. We found that electrical microstimulation in the SEF increased the velocity of anticipatory pursuit movements and decreased their latency. These effects will be referred to as anticipatory pursuit facilitation. The degree of facilitation was the largest if the stimulation train was delivered near the end of the fixation period, before the moment when anticipatory pursuit usually begins. No anticipatory smooth eye movements could be evoked during fixation without an expectation of target motion. These results suggest that the SEF pursuit area might be involved in the process of guiding anticipatory pursuit.

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.


2002 ◽  
Vol 88 (4) ◽  
pp. 1880-1892 ◽  
Author(s):  
M. Missal ◽  
E. L. Keller

The premotor pathways subserving saccades and smooth-pursuit eye movements are usually thought to be different. Indeed, saccade and smooth-pursuit eye movements have different dynamics and functions. In particular, a group of midline cells in the pons called omnipause neurons (OPNs) are considered to be part of the saccadic system only. It has been established that OPNs keep premotor neurons for saccades under constant inhibition during fixation periods. Saccades occur only when the activity of OPNs has completely stopped or paused. Accordingly, electrical stimulation in the region of OPNs inhibits premotor neurons and interrupts saccades. The premotor relay for smooth pursuit is thought to be organized differently and omnipause neurons are not supposed to be involved in smooth-pursuit eye movements. To investigate this supposition, OPNs were recorded during saccades and during smooth pursuit in the monkey ( Macaca mulatta). Unexpectedly, we found that neuronal activity of OPNs decreased during smooth pursuit. The resulting activity reduction reached statistical significance in ∼50% of OPNs recorded during pursuit of a target moving at 40°/s. On average, activity was reduced by 34% but never completely stopped or paused. The onset of activity reduction coincided with the onset of smooth pursuit. The duration of activity reduction was correlated with pursuit duration and its intensity was correlated with eye velocity. Activity reduction was observed even in the absence of catch-up saccades that frequently occur during pursuit. Electrical microstimulation in the OPNs' area induced a strong deceleration of the eye during smooth pursuit. These results suggest that OPNs form an inhibitory mechanism that could control the time course of smooth pursuit. This inhibitory mechanism is part of the fixation system and is probably needed to avoid reflexive eye movements toward targets that are not purposefully selected. This study shows that saccades and smooth pursuit, although they are different kinds of eye movements, are controlled by the same inhibitory system.


1997 ◽  
Vol 14 (5) ◽  
pp. 853-865 ◽  
Author(s):  
S. J. Heinen ◽  
M. Liu

AbstractA region of dorsomedial frontal cortex (DMFC) has been implicated in planning and executing saccadic eye movements; hence it has been referred to as a supplementary eye field (SEF). Recently, activity related to executing smooth-pursuit eye movements has been recorded from the DMFC, and microstimulation here has been shown to evoke smooth eye movements. This report documents neuronal activity present in smooth-pursuit tasks where the predictability of target motion was manipulated. The activity of many neurons in the DMFC reached a peak when a predictable change in target motion occurred. Furthermore, the peak activity of some cells was systematically shifted by manipulating the duration of the target event, indicating that the network these neurons were in could learn the temporal characteristics of new target motion. Finally, the activity of most neurons tested was greater when target motion was predictable than when it was unpredictable. The results suggest that the DMFC participates in planning smooth-pursuit eye movements based on past stimulus history.


2004 ◽  
Vol 91 (2) ◽  
pp. 623-631 ◽  
Author(s):  
Megan R. Carey ◽  
Stephen G. Lisberger

The generation of primate smooth pursuit eye movements involves two processes. One process transforms the direction and speed of target motion into a motor command and the other regulates the strength, or “gain,” of the visual-motor transformation. We have conducted a behavioral analysis to identify the signals that modulate the internal gain of pursuit. To test whether the modulatory signals are related to eye velocity in the orbit or in the world (gaze velocity), we used brief perturbations of target motion to probe the gain of pursuit during tracking conditions that used head rotation to dissociate eye and gaze velocity. We found that the responses to perturbations varied primarily as a function of gaze velocity. To further understand the gaze velocity signals that control internal pursuit gain, we used adaptive modification of the gain of the vestibulo-ocular reflex (VOR) to dissociate physical gaze velocity from the component of gaze velocity that is driven by visual inputs. After VOR adaptation, perturbation responses were altered; the smallest perturbation responses now occurred during tracking conditions that required nonzero physical gaze velocity. However, perturbation responses during tracking conditions that mimicked the modified VOR were still enhanced relative to those obtained during fixation. We conclude that the signals that modulate the internal gain of pursuit are modified by VOR adaptation so that they are rendered intermediate between physical and visually driven gaze velocity. Similar changes in the gaze velocity signal have been reported in the cerebellar floccular complex following adaptive modification of the VOR and could be present in other brain areas that carry putative gaze velocity signals.


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.


2019 ◽  
Vol 5 (1) ◽  
pp. 223-246 ◽  
Author(s):  
Eileen Kowler ◽  
Jason F. Rubinstein ◽  
Elio M. Santos ◽  
Jie Wang

Smooth pursuit eye movements maintain the line of sight on smoothly moving targets. Although often studied as a response to sensory motion, pursuit anticipates changes in motion trajectories, thus reducing harmful consequences due to sensorimotor processing delays. Evidence for predictive pursuit includes ( a) anticipatory smooth eye movements (ASEM) in the direction of expected future target motion that can be evoked by perceptual cues or by memory for recent motion, ( b) pursuit during periods of target occlusion, and ( c) improved accuracy of pursuit with self-generated or biologically realistic target motions. Predictive pursuit has been linked to neural activity in the frontal cortex and in sensory motion areas. As behavioral and neural evidence for predictive pursuit grows and statistically based models augment or replace linear systems approaches, pursuit is being regarded less as a reaction to immediate sensory motion and more as a predictive response, with retinal motion serving as one of a number of contributing cues.


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.


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