Target Selection for Saccadic Eye Movements: Prelude Activity in the Superior Colliculus During a Direction-Discrimination Task

2001 ◽  
Vol 86 (5) ◽  
pp. 2543-2558 ◽  
Author(s):  
Gregory D. Horwitz ◽  
William T. Newsome
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Discrimination Task ◽  
Target Selection ◽  
Saccadic Eye Movements ◽  
Saccade Target ◽  
Visual Responses ◽  
Direction Discrimination ◽  
Motion Signal ◽  
Movement Field

We investigated the role of the superior colliculus (SC) in saccade target selection while macaque monkeys performed a direction-discrimination task. The monkeys selected one of two possible saccade targets based on the direction of motion in a stochastic random-dot display; the difficulty of the task was varied by adjusting the strength of the motion signal in the display. One of the two saccade targets was positioned within the movement field of the SC neuron under study while the other target was positioned well outside the movement field. Approximately 30% of the neurons in the intermediate and deep layers of the SC discharged target-specific preludes of activity that “predicted” target choices well before execution of the saccadic eye movement. Across the population of neurons, the strength of the motion signal in the display influenced the intensity of this “predictive” prelude activity: SC activity signaled the impending saccade more reliably when the motion signal was strong than when it was weak. The dependence of neural activity on motion strength could not be explained by small variations in the metrics of the saccadic eye movements. Predictive activity was particularly strong in a subpopulation of neurons with directional visual responses that we have described previously. For a subset of SC neurons, therefore, prelude activity reflects the difficulty of the direction discrimination in addition to the target of the impending saccade. These results are consistent with the notion that a restricted network of SC neurons plays a role in the process of saccade target selection.

Target Selection for Saccadic Eye Movements: Direction-Selective Visual Responses in the Superior Colliculus

2001 ◽  
Vol 86 (5) ◽  
pp. 2527-2542 ◽  
Author(s):  
Gregory D. Horwitz ◽  
William T. Newsome
Keyword(s):  
Superior Colliculus ◽  
Eye Movement ◽  
Discrimination Task ◽  
Visual Motion ◽  
Target Selection ◽  
Small Population ◽  
Saccade Target ◽  
Visual Responses ◽  
Direction Discrimination ◽  
Deep Layers

We investigated the role of the superior colliculus (SC) in saccade target selection in rhesus monkeys who were trained to perform a direction-discrimination task. In this task, the monkey discriminated between opposed directions of visual motion and indicated its judgment by making a saccadic eye movement to one of two visual targets that were spatially aligned with the two possible directions of motion in the display. Thus the neural circuits that implement target selection in this task are likely to receive directionally selective visual inputs and be closely linked to the saccadic system. We therefore studied prelude neurons in the intermediate and deep layers of the SC that can discharge up to several seconds before an impending saccade, indicating a relatively high-level role in saccade planning. We used the direction-discrimination task to identify neurons whose prelude activity “predicted” the impending perceptual report several seconds before the animal actually executed the operant eye movement; these “choice predicting” cells comprised ∼30% of the neurons we encountered in the intermediate and deep layers of the SC. Surprisingly, about half of these prelude cells yielded direction-selective responses to our motion stimulus during a passive fixation task. In general, these neurons responded to motion stimuli in many locations around the visual field including the center of gaze where the visual discriminanda were positioned during the direction-discrimination task. Preferred directions generally pointed toward the location of the movement field of the SC neuron in accordance with the sensorimotor demands of the discrimination task. Control experiments indicate that the directional responses do not simply reflect covertly planned saccades. Our results indicate that a small population of SC prelude neurons exhibits properties appropriate for linking stimulus cues to saccade target selection in the context of a visual discrimination task.

Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements

1995 ◽  
Vol 73 (5) ◽  
pp. 1988-2003 ◽  
Author(s):  
M. F. Walker ◽  
E. J. Fitzgibbon ◽  
M. E. Goldberg
Keyword(s):  
Receptive Field ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Receptive Fields ◽  
Saccadic Eye Movements ◽  
Superficial Layer ◽  
Saccade Target ◽  
Visual Response ◽  
Intermediate Layers ◽  
Movement Field

1. Previous experiments have shown that visual neurons in the lateral intraparietal area (LIP) respond predictively to stimuli outside their classical receptive fields when an impending saccade will bring those stimuli into their receptive fields. Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demonstrate similar predictive responses in the monkey colliculus. 2. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. Each of these neurons did not respond to the stimulus unless an eye movement brought it into its receptive field, nor did it discharge in association with the eye movement unless it brought a stimulus into its receptive field. 4. These neurons were located in the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. 5. The predictive responses of most of these neurons (16/18, 89%) did not require that the stimulus be relevant to the monkey's rewarded behavior. However, for some neurons the predictive response was enhanced when the stimulus was the target of a subsequent saccade into the neuron's movement field. 6. Most neurons with predictive responses responded with a similar magnitude and latency to a continuous stimulus that remained on after the saccade, and to the same stimulus when it was only flashed for 50 ms coincident with the onset of the saccade target and thus never appeared within the cell's classical receptive field. 7. The visual response of neurons in the intermediate layers of the colliculus is suppressed during the saccade itself. Neurons that showed predictive responses began to discharge before the saccade, were suppressed during the saccade, and usually resumed discharging after the saccade. 8. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelevant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would not be brought into their receptive fields by a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus

1985 ◽  
Vol 53 (1) ◽  
pp. 266-291 ◽  
Author(s):  
O. Hikosaka ◽  
R. H. Wurtz
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Injection Site ◽  
Saccadic Eye Movements ◽  
Contralateral Side ◽  
Slow Phase ◽  
Gamma Aminobutyric Acid ◽  
Affected Area ◽  
Related Substances ◽  
Movement Field

Our previous observations led to the hypothesis that cells in the substantia nigra pars reticulata (SNr) tonically inhibit saccade-related cells in the intermediate layers of the superior colliculus (SC). Before saccades to visual or remembered targets, cells in SNr briefly reduce that inhibition, allowing a burst of spikes of SC cells that, in turn, leads to the initiation of a saccadic eye movement. Since this inhibition is likely to be mediated by gamma-aminobutyric acid (GABA), we tested this hypothesis by injecting a GABA agonist (muscimol) or a GABA antagonist (bicuculline) into the superior colliculus and measured the effects on saccadic eye movements made to visual or remembered targets. An injection of muscimol selectively suppressed saccades to the movement field of the cells near the injection site. The affected area expanded over time, thus suggesting the diffusion of muscimol in the SC; the area never included the other hemifield, suggesting that the diffusion was limited to one SC. One of the monkeys became unable to make any saccades to the affected area. Saccades to visual targets following injection of muscimol had longer latency and slightly shorter amplitudes that were corrected by subsequent saccades. The most striking change was a decrease in the peak velocity of the saccade, frequently to less than half the preinjection value. Saccades to remembered targets following injection of muscimol also showed an increase in latency and decrease in velocity, but in addition, showed a striking decrease in the accuracy of the saccades. The trajectories of saccades became distorted as if they were deflected away from the affected area. After muscimol injection, the area over which spontaneous eye movements were made shifted toward the side ipsilateral to the injection. Saccades toward the contralateral side were less frequent and slower. In nystagmus, which developed later, the slow phase was toward the contralateral side. In contrast to muscimol, injection of bicuculline facilitated the initiation of saccades. Injection was followed almost immediately by stereotyped and apparently irrepressible saccades made toward the center of the movement field of the SC cells at the injection site. The monkeys became unable to fixate during the tasks; the fixation was interrupted by saccadic jerks made to the affected area of the visual field and then back to the fixation point.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Vision as oculomotor reward: cognitive contributions to the dynamic control of saccadic eye movements

2021 ◽  
Author(s):  
Christian Wolf ◽  
Markus Lappe
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Visual System ◽  
Dynamic Control ◽  
Saccadic Eye Movements ◽  
Saccade Target ◽  
Cognitive Mechanisms ◽  
Foveal Vision ◽  
Subsequent Behavior ◽  
High Level

AbstractHumans and other primates are equipped with a foveated visual system. As a consequence, we reorient our fovea to objects and targets in the visual field that are conspicuous or that we consider relevant or worth looking at. These reorientations are achieved by means of saccadic eye movements. Where we saccade to depends on various low-level factors such as a targets’ luminance but also crucially on high-level factors like the expected reward or a targets’ relevance for perception and subsequent behavior. Here, we review recent findings how the control of saccadic eye movements is influenced by higher-level cognitive processes. We first describe the pathways by which cognitive contributions can influence the neural oculomotor circuit. Second, we summarize what saccade parameters reveal about cognitive mechanisms, particularly saccade latencies, saccade kinematics and changes in saccade gain. Finally, we review findings on what renders a saccade target valuable, as reflected in oculomotor behavior. We emphasize that foveal vision of the target after the saccade can constitute an internal reward for the visual system and that this is reflected in oculomotor dynamics that serve to quickly and accurately provide detailed foveal vision of relevant targets in the visual field.

scholarly journals A test of spatial temporal decoding mechanisms in the superior colliculus

2012 ◽  
Vol 107 (9) ◽  
pp. 2442-2452 ◽  
Author(s):  
Husam A. Katnani ◽  
A. J. Van Opstal ◽  
Neeraj J. Gandhi
Keyword(s):  
Nervous System ◽  
Motor Control ◽  
Eye Movements ◽  
Superior Colliculus ◽  
Motor Behavior ◽  
Saccadic Eye Movements ◽  
Population Coding ◽  
Population Activity ◽  
Low Levels

Population coding is a ubiquitous principle in the nervous system for the proper control of motor behavior. A significant amount of research is dedicated to studying population activity in the superior colliculus (SC) to investigate the motor control of saccadic eye movements. Vector summation with saturation (VSS) has been proposed as a mechanism for how population activity in the SC can be decoded to generate saccades. Interestingly, the model produces different predictions when decoding two simultaneous populations at high vs. low levels of activity. We tested these predictions by generating two simultaneous populations in the SC with high or low levels of dual microstimulation. We also combined varying levels of stimulation with visually induced activity. We found that our results did not perfectly conform to the predictions of the VSS scheme and conclude that the simplest implementation of the model is incomplete. We propose that additional parameters to the model might account for the results of this investigation.

Distributed spatial coding in the superior colliculus: A review

1991 ◽  
Vol 6 (1) ◽  
pp. 3-13 ◽  
Author(s):  
James T. McIlwain
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Receptive Fields ◽  
Saccadic Eye Movements ◽  
Visual Direction ◽  
Saccade Amplitude ◽  
Spatial Coding ◽  
Distributed Coding

AbstractThis paper reviews evidence that the superior colliculus (SC) of the midbrain represents visual direction and certain aspects of saccadic eye movements in the distribution of activity across a population of cells. Accurate and precise eye movements appear to be mediated, in part at least, by cells of the SC that have large sensory receptive fields and/or discharge in association with a range of saccades. This implies that visual points or saccade targets are represented by patches rather than points of activity in the SC. Perturbation of the pattern of collicular discharge by focal inactivation modifies saccade amplitude and direction in a way consistent with distributed coding. Several models have been advanced to explain how such a code might be implemented in the colliculus. Evidence related to these hypotheses is examined and continuing uncertainties are identified.

scholarly journals Normal correspondence of tectal maps for saccadic eye movements in strabismus

2016 ◽  
Vol 116 (6) ◽  
pp. 2541-2549 ◽  
Author(s):  
John R. Economides ◽  
Daniel L. Adams ◽  
Jonathan C. Horton
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Superior Colliculus ◽  
Saccadic Eye Movements ◽  
Systematic Change ◽  
Free Viewing ◽  
Pattern Deviation ◽  
Ocular Deviation ◽  
The Right ◽  
Stem Structure

The superior colliculus is a major brain stem structure for the production of saccadic eye movements. Electrical stimulation at any given point in the motor map generates saccades of defined amplitude and direction. It is unknown how this saccade map is affected by strabismus. Three macaques were raised with exotropia, an outwards ocular deviation, by detaching the medial rectus tendon in each eye at age 1 mo. The animals were able to make saccades to targets with either eye and appeared to alternate fixation freely. To probe the organization of the superior colliculus, microstimulation was applied at multiple sites, with the animals either free-viewing or fixating a target. On average, microstimulation drove nearly conjugate saccades, similar in both amplitude and direction but separated by the ocular deviation. Two monkeys showed a pattern deviation, characterized by a systematic change in the relative position of the two eyes with certain changes in gaze angle. These animals' saccades were slightly different for the right eye and left eye in their amplitude or direction. The differences were consistent with the animals' underlying pattern deviation, measured during static fixation and smooth pursuit. The tectal map for saccade generation appears to be normal in strabismus, but saccades may be affected by changes in the strabismic deviation that occur with different gaze angles.

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.

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