scholarly journals A circuit for saccadic suppression in the primate brain

2017 ◽  
Vol 117 (4) ◽  
pp. 1720-1735 ◽  
Author(s):  
Rebecca A. Berman ◽  
James Cavanaugh ◽  
Kerry McAlonan ◽  
Robert H. Wurtz
Keyword(s):  
Eye Movements ◽  
Corollary Discharge ◽  
Saccadic Suppression ◽  
Visual Signals ◽  
Visual Responses ◽  
Visual Neuroscience ◽  
Primate Brain ◽  
Complete Circuit ◽  
Visual Area Mt ◽  
Visual Hemifields

Saccades should cause us to see a blur as the eyes sweep across a visual scene. Specific brain mechanisms prevent this by producing suppression during saccades. Neuronal correlates of such suppression were first established in the visual superficial layers of the superior colliculus (SC) and subsequently have been observed in cortical visual areas, including the middle temporal visual area (MT). In this study, we investigated suppression in a recently identified circuit linking visual SC (SCs) to MT through the inferior pulvinar (PI). We examined responses to visual stimuli presented just before saccades to reveal a neuronal correlate of suppression driven by a copy of the saccade command, referred to as a corollary discharge. We found that visual responses were similarly suppressed in SCs, PI, and MT. Within each region, suppression of visual responses occurred with saccades into both visual hemifields, but only in the contralateral hemifield did this suppression consistently begin before the saccade (~100 ms). The consistency of the signal along the circuit led us to hypothesize that the suppression in MT was influenced by input from the SC. We tested this hypothesis in one monkey by inactivating neurons within the SC and found evidence that suppression in MT depends on corollary discharge signals from motor SC (SCi). Combining these results with recent findings in rodents, we propose a complete circuit originating with corollary discharge signals in SCi that produces suppression in visual SCs, PI, and ultimately, MT cortex. NEW & NOTEWORTHY A fundamental puzzle in visual neuroscience is that we frequently make rapid eye movements (saccades) but seldom perceive the visual blur accompanying each movement. We investigated neuronal correlates of this saccadic suppression by recording from and perturbing a recently identified circuit from brainstem to cortex. We found suppression at each stage, with evidence that it was driven by an internally generated signal. We conclude that this circuit contributes to neuronal suppression of visual signals during eye movements.

Discharge Characteristics of Pursuit Neurons in MST During Vergence Eye Movements

2005 ◽  
Vol 93 (5) ◽  
pp. 2415-2434 ◽  
Author(s):  
Teppei Akao ◽  
Michael J. Mustari ◽  
Junko Fukushima ◽  
Sergei Kurkin ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Visual Motion ◽  
Significant Proportion ◽  
Visual Signals ◽  
Visual Responses ◽  
Discharge Characteristics ◽  
Temporal Area ◽  
Mst Neurons ◽  
Pursuit Neurons ◽  
Vergence Tracking

For small objects moving smoothly in space close to the observer, smooth pursuit and vergence eye movements maintain target images near the foveae to insure high-resolution processing of visual signals about moving objects. Signals for both systems must be synthesized for pursuit-in-three-dimensions (3D). Recent studies have shown that responses of the majority of pursuit neurons in the frontal eye fields (FEF) code pursuit-in-3D. This area is known to have reciprocal connections with the medial superior temporal area (MST) where frontal pursuit neurons are found. To examine whether pursuit-in-3D signals are already present in MST and how MST neurons discharge during vergence-tracking induced by a small spot, we examined discharge of MST pursuit neurons in 2 monkeys. Of a total of 219 pursuit neurons examined during both frontal pursuit and vergence-tracking, 61% discharged only for frontal pursuit, 18% only for vergence-tracking, and 21% for both. A majority of vergence-related MST neurons exhibited sensitivity to vergence eye velocity. Their discharge was maintained during brief blanking of a vergence target. About 1/3 of vergence-related MST neurons exhibited visual responses to spot motion in depth. The preferred directions for visual motion and vergence-tracking were similar in half of our population. Some of the remaining neurons showed opposite preferred directions. A significant proportion (29%) of vergence-related neurons discharged before onset of eye movements with lead times longer than 20 ms. The results in this and previous studies indicate differences in discharge characteristics of FEF and MST pursuit neurons, suggesting different roles for the two in pursuit-in-3D.

scholarly journals Modulation of Visual Signals in Macaque MT and MST Neurons During Pursuit Eye Movement

2009 ◽  
Vol 102 (6) ◽  
pp. 3225-3233 ◽  
Author(s):  
Leanne Chukoskie ◽  
J. Anthony Movshon
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Retinal Image ◽  
Visual Motion ◽  
Single Cells ◽  
Response Amplitude ◽  
Visual Signals ◽  
Image Motion ◽  
Visual Responses ◽  
Retinal Image Motion

Retinal image motion is produced with each eye movement, yet we usually do not perceive this self-produced “reafferent” motion, nor are motion judgments much impaired when the eyes move. To understand the neural mechanisms involved in processing reafferent motion and distinguishing it from the motion of objects in the world, we studied the visual responses of single cells in middle temporal (MT) and medial superior temporal (MST) areas during steady fixation and smooth-pursuit eye movements in awake, behaving macaques. We measured neuronal responses to random-dot patterns moving at different speeds in a stimulus window that moved with the pursuit target and the eyes. This allowed us to control retinal image motion at all eye velocities. We found the expected high proportion of cells selective for the direction of visual motion. Pursuit tracking changed both response amplitude and preferred retinal speed for some cells. The changes in preferred speed were on average weakly but systematically related to the speed of pursuit for area MST cells, as would be expected if the shifts in speed selectivity were compensating for reafferent input. In area MT, speed tuning did not change systematically during pursuit. Many cells in both areas also changed response amplitude during pursuit; the most common form of modulation was response suppression when pursuit was opposite in direction to the cell's preferred direction. These results suggest that some cells in area MST encode retinal image motion veridically during eye movements, whereas others in both MT and MST contribute to the suppression of visual responses to reafferent motion.

scholarly journals Disparity Sensitivity of Frontal Eye Field Neurons

2000 ◽  
Vol 83 (1) ◽  
pp. 625-629 ◽  
Author(s):  
Stefano Ferraina ◽  
Martin Paré ◽  
Robert H. Wurtz
Keyword(s):  
Eye Movements ◽  
Dimensional Space ◽  
Visual Stimuli ◽  
Three Dimensional ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Motor Processes ◽  
Uncrossed Disparity ◽  
Eye Field ◽  
Three Dimensional Space

Information about depth is necessary to generate saccades to visual stimuli located in three-dimensional space. To determine whether monkey frontal eye field (FEF) neurons play a role in the visuo-motor processes underlying this behavior, we studied their visual responses to stimuli at different disparities. Disparity sensitivity was tested from 3° of crossed disparity (near) to 3° degrees of uncrossed disparity (far). The responses of about two thirds of FEF visual and visuo-movement neurons were sensitive to disparity and showed a broad tuning in depth for near or far disparities. Early phasic and late tonic visual responses often displayed different disparity sensitivity. These findings provide evidence of depth-related signals in FEF and suggest a role for FEF in the control of disconjugate as well as conjugate eye movements.

A Control Systems Model of Smooth Pursuit Eye Movements with Realistic Emergent Properties

1989 ◽  
Vol 1 (1) ◽  
pp. 116-122 ◽  
Author(s):  
R. J. Krauzlis ◽  
S. G. Lisberger
Keyword(s):  
Eye Movements ◽  
Visual Tracking ◽  
Smooth Pursuit ◽  
Oculomotor System ◽  
Difficult Problem ◽  
Visual Signals ◽  
Emergent Properties ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Systems Model

Visual tracking of objects in a noisy environment is a difficult problem that has been solved by the primate oculomotor system, but remains unsolved in robotics. In primates, smooth pursuit eye movements match eye motion to target motion to keep the eye pointed at smoothly moving targets. We have used computer models as a tool to investigate possible computational strategies underlying this behavior. Here, we present a model based upon behavioral data from monkeys. The model emphasizes the variety of visual signals available for pursuit and, in particular, includes a sensitivity to the acceleration of retinal images. The model was designed to replicate the initial eye velocity response observed during pursuit of different target motions. The strength of the model is that it also exhibits a number of emergent properties that are seen in the behavior of both humans and monkeys. This suggests that the elements in the model capture important aspects of the mechanism of visual tracking by the primate smooth pursuit system.

Visual responses of pulvinar and collicular neurons during eye movements of awake, trained macaques

1991 ◽  
Vol 66 (2) ◽  
pp. 485-496 ◽  
Author(s):  
D. L. Robinson ◽  
J. W. McClurkin ◽  
C. Kertzman ◽  
S. E. Petersen
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Visual Stimulation ◽  
Receptive Fields ◽  
Visual Responses ◽  
Stimulus Motion ◽  
Stimulus Movement ◽  
Pursuit Eye Movements ◽  
Extraretinal Signal ◽  
Wide Range

1. We recorded from single neurons in awake, trained rhesus monkeys in a lighted environment and compared responses to stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested. 2. Cells in PI and PL respond to stimulus movement over a wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial layers of the superior colliculus have similar properties to those in PI and PL. 3. When tested in the dark to reduce visual stimulation from the background, cells in PI and PL still do not respond to motion generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements. 4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units above background illumination evoke responses from cells in PI and PL. The suppression appears stronger in the superior colliculus than in PI and PL. 5. These experiments demonstrate that many cells in PI and PL have a suppression of their responses to stimuli that cross their receptive fields during eye movements. These cells are probably suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.

scholarly journals A neural locus for spatial-frequency specific saccadic suppression in visual-motor neurons of the primate superior colliculus

2017 ◽  
Vol 117 (4) ◽  
pp. 1657-1673 ◽  
Author(s):  
Chih-Yang Chen ◽  
Ziad M. Hafed
Keyword(s):  
Spatial Frequency ◽  
Superior Colliculus ◽  
Motor Neurons ◽  
Motor Command ◽  
Visual Sensitivity ◽  
Saccadic Suppression ◽  
Behavioral Measure ◽  
Visual Responses ◽  
Spatial Frequencies ◽  
Visual Motor

Saccades cause rapid retinal-image shifts that go perceptually unnoticed several times per second. The mechanisms for saccadic suppression have been controversial, in part because of sparse understanding of neural substrates. In this study we uncovered an unexpectedly specific neural locus for spatial frequency-specific saccadic suppression in the superior colliculus (SC). We first developed a sensitive behavioral measure of suppression in two macaque monkeys, demonstrating selectivity to low spatial frequencies similar to that observed in earlier behavioral studies. We then investigated visual responses in either purely visual SC neurons or anatomically deeper visual motor neurons, which are also involved in saccade generation commands. Surprisingly, visual motor neurons showed the strongest visual suppression, and the suppression was dependent on spatial frequency, as in behavior. Most importantly, suppression selectivity for spatial frequency in visual motor neurons was highly predictive of behavioral suppression effects in each individual animal, with our recorded population explaining up to ~74% of behavioral variance even on completely different experimental sessions. Visual SC neurons had mild suppression, which was unselective for spatial frequency and thus only explained up to ~48% of behavioral variance. In terms of spatial frequency-specific saccadic suppression, our results run contrary to predictions that may be associated with a hypothesized SC saccadic suppression mechanism, in which a motor command in the visual motor and motor neurons is first relayed to the more superficial purely visual neurons, to suppress them and to then potentially be fed back to cortex. Instead, an extraretinal modulatory signal mediating spatial-frequency-specific suppression may already be established in visual motor neurons. NEW & NOTEWORTHY Saccades, which repeatedly realign the line of sight, introduce spurious signals in retinal images that normally go unnoticed. In part, this happens because of perisaccadic suppression of visual sensitivity, which is known to depend on spatial frequency. We discovered that a specific subtype of superior colliculus (SC) neurons demonstrates spatial-frequency-dependent suppression. Curiously, it is the neurons that help mediate the saccadic command itself that exhibit such suppression, and not the purely visual ones.

Effects of Phosphor Persistence on Perception and the Control of Eye Movements

Perception ◽  
1989 ◽  
Vol 18 (2) ◽  
pp. 257-264 ◽  
Author(s):  
Catherine Neary ◽  
Arnold J Wilkins
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
The Other ◽  
Saccadic Suppression ◽  
Rapid Eye Movement ◽  
Physiological Basis ◽  
Cathode Ray Tube ◽  
Ghost Image ◽  
Corrective Saccades

When a rapid eye movement (saccade) is made across material displayed on cathode ray tube monitors with short-persistence phosphors, various perceptual phenomena occur. The phenomena do not occur when the monitor has a long-persistence phosphor. These phenomena were observed for certain spatial arrays, their possible physiological basis noted, and their effect on the control of eye movements examined. When the display consisted simply of two dots, and a saccade was made from one to the other, a transient ghost image was seen just beyond the destination target. When the display consisted of vertical lines, tilting and displacement of the lines occurred. The phenomena were more intrusive for the latter display and there was a significant increase in the number of corrective saccades. These results are interpreted in terms of the effects of fluctuating illumination (and hence phosphor persistence) on saccadic suppression.

Visual Responses of the Human Superior Colliculus: A High-Resolution Functional Magnetic Resonance Imaging Study

2005 ◽  
Vol 94 (4) ◽  
pp. 2491-2503 ◽  
Author(s):  
Keith A. Schneider ◽  
Sabine Kastner
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
High Resolution ◽  
Superior Colliculus ◽  
Visual Fields ◽  
Visual Response ◽  
Visual Responses ◽  
Subcortical Structures ◽  
Stimulus Motion ◽  
Low Contrast

The superior colliculus (SC) is a multimodal laminar structure located on the roof of the brain stem. The SC is a key structure in a distributed network of areas that mediate saccadic eye movements and shifts of attention across the visual field and has been extensively studied in nonhuman primates. In humans, it has proven difficult to study the SC with functional MRI (fMRI) because of its small size, deep location, and proximity to pulsating vascular structures. Here, we performed a series of high-resolution fMRI studies at 3 T to investigate basic visual response properties of the SC. The retinotopic organization of the SC was determined using the traveling wave method with flickering checkerboard stimuli presented at different polar angles and eccentricities. SC activations were confined to stimulation of the contralateral hemifield. Although a detailed retinotopic map was not observed, across subjects, the upper and lower visual fields were represented medially and laterally, respectively. Responses were dominantly evoked by stimuli presented along the horizontal meridian of the visual field. We also measured the sensitivity of the SC to luminance contrast, which has not been previously reported in primates. SC responses were nearly saturated by low contrast stimuli and showed only small response modulation with higher contrast stimuli, indicating high sensitivity to stimulus contrast. Responsiveness to stimulus motion in the SC was shown by robust activations evoked by moving versus static dot stimuli that could not be attributed to eye movements. The responses to contrast and motion stimuli were compared with those in the human lateral geniculate nucleus. Our results provide first insights into basic visual responses of the human SC and show the feasibility of studying subcortical structures using high-resolution fMRI.

scholarly journals Corollary discharge circuits in the primate brain

2008 ◽  
Vol 18 (6) ◽  
pp. 552-557 ◽  
Author(s):  
Trinity B Crapse ◽  
Marc A Sommer
Keyword(s):  
Corollary Discharge ◽  
Primate Brain
Sign in / Sign up

Export Citation Format

Share Document