scholarly journals Motion direction representation in multivariate electroencephalography activity for smooth pursuit eye movements

2019 ◽  
Author(s):  
Joonyeol Lee ◽  
Woojae Jeong ◽  
Seolmin Kim ◽  
Yee-Joon Kim

AbstractVisually-guided smooth pursuit eye movements are composed of initial open-loop and later steady-state periods. Feedforward sensory information dominates the motor behavior during the open-loop pursuit, and a more complex feedback loop regulates the steady-state pursuit. To understand the neural representations of motion direction during open-loop and steady-state smooth pursuits, we recorded electroencephalography (EEG) responses from human observers while they tracked random dot kinematograms as pursuit targets. We estimated population direction tuning curves from multivariate EEG activity using an inverted encoding model. We found significant direction tuning curves as early as 20 ms from motion onset. Direction tuning responses were generalized to later times during the open-loop smooth pursuit, but they became more dynamic during the later steady-state pursuit. The encoding quality of retinal motion direction information estimated from the early direction tuning curves was predictive of trial-by-trial variation in initial pursuit directions. These results suggest that the movement directions of open-loop smooth pursuit are guided by the representation of the retinal motion present in the multivariate EEG activity.

1999 ◽  
Vol 88 (3) ◽  
pp. 209-219 ◽  
Author(s):  
Gunvant K. Thaker ◽  
David E. Ross ◽  
Robert W. Buchanan ◽  
Helene M. Adami ◽  
Deborah R. Medoff

2003 ◽  
Vol 90 (4) ◽  
pp. 2205-2218 ◽  
Author(s):  
Mark M. Churchland ◽  
I-Han Chou ◽  
Stephen G. Lisberger

We recorded the smooth-pursuit eye movements of monkeys in response to targets that were extinguished (blinked) for 200 ms in mid-trajectory. Eye velocity declined considerably during the target blinks, even when the blinks were completely predictable in time and space. Eye velocity declined whether blinks were presented during steady-state pursuit of a constant-velocity target, during initiation of pursuit before target velocity was reached, or during eye accelerations induced by a change in target velocity. When a physical occluder covered the trajectory of the target during blinks, creating the impression that the target moved behind it, the decline in eye velocity was reduced or abolished. If the target was occluded once the eye had reached target velocity, pursuit was only slightly poorer than normal, uninterrupted pursuit. In contrast, if the target was occluded during the initiation of pursuit, while the eye was accelerating toward target velocity, pursuit during occlusion was very different from normal pursuit. Eye velocity remained relatively stable during target occlusion, showing much less acceleration than normal pursuit and much less of a decline than was produced by a target blink. Anticipatory or predictive eye acceleration was typically observed just prior to the reappearance of the target. Computer simulations show that these results are best understood by assuming that a mechanism of eye-velocity memory remains engaged during target occlusion but is disengaged during target blinks.


2005 ◽  
Vol 93 (3) ◽  
pp. 1710-1717 ◽  
Author(s):  
Babatunde Adeyemo ◽  
Dora E. Angelaki

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.


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.


2015 ◽  
Vol 113 (5) ◽  
pp. 1377-1399 ◽  
Author(s):  
T. Scott Murdison ◽  
Guillaume Leclercq ◽  
Philippe Lefèvre ◽  
Gunnar Blohm

Smooth pursuit eye movements are driven by retinal motion and enable us to view moving targets with high acuity. Complicating the generation of these movements is the fact that different eye and head rotations can produce different retinal stimuli but giving rise to identical smooth pursuit trajectories. However, because our eyes accurately pursue targets regardless of eye and head orientation (Blohm G, Lefèvre P. J Neurophysiol 104: 2103–2115, 2010), the brain must somehow take these signals into account. To learn about the neural mechanisms potentially underlying this visual-to-motor transformation, we trained a physiologically inspired neural network model to combine two-dimensional (2D) retinal motion signals with three-dimensional (3D) eye and head orientation and velocity signals to generate a spatially correct 3D pursuit command. We then simulated conditions of 1) head roll-induced ocular counterroll, 2) oblique gaze-induced retinal rotations, 3) eccentric gazes (invoking the half-angle rule), and 4) optokinetic nystagmus to investigate how units in the intermediate layers of the network accounted for different 3D constraints. Simultaneously, we simulated electrophysiological recordings (visual and motor tunings) and microstimulation experiments to quantify the reference frames of signals at each processing stage. We found a gradual retinal-to-intermediate-to-spatial feedforward transformation through the hidden layers. Our model is the first to describe the general 3D transformation for smooth pursuit mediated by eye- and head-dependent gain modulation. Based on several testable experimental predictions, our model provides a mechanism by which the brain could perform the 3D visuomotor transformation for smooth pursuit.


2019 ◽  
Author(s):  
Stuart Behling ◽  
Stephen G. Lisberger

AbstractSmooth 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 towards 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 creates less reliable target motion that impacts pursuit initiation by changing the gain of visual-motor transmission and perturbs steady-state tracking by modulation of the motor corollary discharges that comprise eye velocity memory.


2010 ◽  
Vol 104 (4) ◽  
pp. 2103-2115 ◽  
Author(s):  
Gunnar Blohm ◽  
Philippe Lefèvre

Smooth pursuit eye movements are driven by retinal motion signals. These retinal motion signals are converted into motor commands that obey Listing's law (i.e., no accumulation of ocular torsion). The fact that smooth pursuit follows Listing's law is often taken as evidence that no explicit reference frame transformation between the retinal velocity input and the head-centered motor command is required. Such eye-position-dependent reference frame transformations between eye- and head-centered coordinates have been well-described for saccades to static targets. Here we suggest that such an eye (and head)-position-dependent reference frame transformation is also required for target motion (i.e., velocity) driving smooth pursuit eye movements. Therefore we tested smooth pursuit initiation under different three-dimensional eye positions and compared human performance to model simulations. We specifically tested if the ocular rotation axis changed with vertical eye position, if the misalignment of the spatial and retinal axes during oblique fixations was taken into account, and if ocular torsion (due to head roll) was compensated for. If no eye-position-dependent velocity transformation was used, the pursuit initiation should follow the retinal direction, independently of eye position; in contrast, a correct visuomotor velocity transformation would result in spatially correct pursuit initiation. Overall subjects accounted for all three components of the visuomotor velocity transformation, but we did observe differences in the compensatory gains between individual subjects. We concluded that the brain does perform a visuomotor velocity transformation but that this transformation was prone to noise and inaccuracies of the internal model.


1988 ◽  
Vol 59 (3) ◽  
pp. 952-977 ◽  
Author(s):  
J. G. May ◽  
E. L. Keller ◽  
D. A. Suzuki

1. Anatomical and single-unit recording studies suggest that the dorsolateral pontine nucleus (DLPN) in monkey is a major link in the projection of descending visual motion information to the cerebellum. Such studies coupled with cortical and cerebellar lesion results suggest a major role for this basilar pontine region in the mediation of smooth-pursuit eye movements. 2. To provide more direct evidence that this pontine region is involved in the control of smooth-pursuit eye movements, focal chemical lesions were made in DLPN in the vicinity of previously recorded visual motion and pursuit-related neurons. Eye movement responses were subsequently recorded in these lesioned animals under several behavioral paradigms. 3. A major deficit in smooth-pursuit performance was produced after unilateral DLPN lesions generated either reversibly with lidocaine or more permanently with ibotenic acid. Pursuit impairments were observed during steady-state tracking of sinusoidal target motion as well as during the initiation of pursuit tracking to sudden ramp target motion. Through the use of the latter technique, initial eye acceleration was reduced to less than one-half of normal for animals with large lesions of the dorsolateral and lateral pontine nuclei. 4. The pursuit deficit in all animals was directional in nature and was not dependent on the visual hemifield in which the motion stimulus occurred. The largest effect for horizontal tracking occurred in all animals for pursuit directed ipsilateral to the lesion. Animals also showed major deficits in one or both directions of vertical pursuit, although the primary direction of the vertical impairment was variable from animal to animal. 5. Chemical lesions in the DLPN also produced comparable deficits in the initiation of optokinetic-induced smooth eye movements in the ipsilateral direction. In contrast to this effect on the initial optokinetic response, in the one lesioned animal studied during prolonged constant velocity optokinetic drum rotation, smooth eye speed increased slowly over a 10- to 15-s period to reach a level that closely matched drum speed. These results suggest that pathways outside the DLPN can generate the steady-state optokinetic response. 6. Saccades to stationary targets were normal after DLPN lesions, but corrective saccades made to targets moving in the direction ipsilateral to the lesion were much more hypometric than similar prelesion control saccades. 7. The pursuit deficits produced by lidocaine injections recovered within 30 min. The ibotenic acid deficits were maximal approximately 1 day after the injection and recovered rapidly thereafter over a time period of 3-7 days.(ABSTRACT TRUNCATED AT 400 WORDS)


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