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)

Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements

1976 ◽  
Vol 39 (4) ◽  
pp. 722-744 ◽  
Author(s):  
C. W. Mohler ◽  
R. H. Wurtz
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Intermediate Layer ◽  
Visual Fields ◽  
Saccadic Eye Movements ◽  
Superficial Layer ◽  
Cell Discharge ◽  
Intermediate Layers ◽  
Dorsal Edge

1. We investigated the characteristics of cells in the intermediate layers of the superior colliculus that increase their rate of discharge before saccadic eye movements. Eye movements were repeatedly elicited by training rhesus monkeys to fixate on a spot of light and to make saccades to other spots of light when the fixation spot was turned off. 2. The eye movement cells showed consistent variations with their depth within the colliculus. The onset of the cell discharge led the eye movement by less time and the duration of the discharge was shorter as the cell was located closer to the dorsal edge of the intermediate layers. The movements fields (that area of the visual field where a saccade into the area is preceded by a burst of cell discharges) of each successive cell also became smaller as the cells were located more dorsally. The profile of peak discharge frequency remained fairly flat throughout the movement field of the cells regardless of depth of the cell within the colliculus. 3. A new type of eye movement-related cell has been found which usually lies at the border between the superficial and intermediate layers. This cell type, the visually triggered movement cell, increased its rate of discharge before saccades made to a visual stimulus but not before spontaneous saccades of equal amplitude made in the light or the dark. A vigorous discharge of these cells before an eye movement was dependent on the presence of a visual target; the cells seemed to combine the visual input of superficial layer cells and the movement-related input of the intermediate layer cells. The size of the movement fields of these cells were about the same size as the visual fields of superficial layer cells just above them...

Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey

1994 ◽  
Vol 72 (6) ◽  
pp. 2754-2770 ◽  
Author(s):  
E. L. Keller ◽  
J. A. Edelman
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Temporal Dynamics ◽  
Saccadic Eye Movements ◽  
Eye Position ◽  
Visual Response ◽  
Intermediate Layers ◽  
Saccade Onset ◽  
Spatial And Temporal Dynamics ◽  
Motor Error

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons (SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it has a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Modulation of Presaccadic Activity in the Frontal Eye Field by the Superior Colliculus

2009 ◽  
Vol 101 (6) ◽  
pp. 2934-2942 ◽  
Author(s):  
Rebecca A. Berman ◽  
Wilsaan M. Joiner ◽  
James Cavanaugh ◽  
Robert H. Wurtz
Keyword(s):  
Cerebral Cortex ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Frontal Eye Field ◽  
Visual Response ◽  
Saccadic Eye Movement ◽  
Reversible Inactivation ◽  
Intermediate Layers ◽  
Eye Field ◽  
Neuronal Processing

A cascade of neuronal signals precedes each saccadic eye movement to targets in the visual scene. In the cerebral cortex, this neuronal processing culminates in the frontal eye field (FEF), where neurons have bursts of activity before the saccade. This presaccadic activity is typically considered to drive downstream activity in the intermediate layers of the superior colliculus (SC), which receives direct projections from FEF. Consequently, the FEF activity is thought to be determined solely by earlier cortical processing and unaffected by activity in the SC. Recent evidence of an ascending path from the SC to FEF raises the possibility, however, that presaccadic activity in the FEF may also depend on input from the SC. Here we tested this possibility by recording from single FEF neurons during the reversible inactivation of SC. Our results indicate that presaccadic activity in the FEF does not require SC input: we never observed a significant reduction in FEF presaccadic activity when the SC was inactivated. Unexpectedly, in a third of experiments, SC inactivation elicited a significant increase in FEF presaccadic activity. The passive visual response of FEF neurons, in contrast, was virtually unaffected by inactivation of the SC. These findings show that presaccadic activity in the FEF does not originate in the SC but nevertheless may be influenced by modulatory signals ascending from the SC.

scholarly journals Polar-angle representation of saccadic eye movements in human superior colliculus

2017 ◽  
Author(s):  
Ricky R Savjani ◽  
Elizabeth Halfen ◽  
Jung Hwan Kim ◽  
David Ress
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Visual Stimulation ◽  
Polar Angle ◽  
Saccadic Eye Movements ◽  
List Type ◽  
Saccadic Eye Movement ◽  
Intermediate Layers ◽  
Retinotopic Organization

SummaryThe superior colliculus (SC) is a layered midbrain structure involved in directing eye movements and coordinating visual attention. Electrical stimulation and neuronal recordings in the intermediate layers of monkey SC have shown a retinotopic organization for the mediation of saccadic eye-movements. However, in human SC the topography of saccades is unknown. Here, a novel experimental paradigm and highresolution (1.2-mm) functional magnetic resonance imaging methods were used to measure activity evoked by saccadic eye movements within SC. Results provide three critical observations about the topography of the human SC: (1) saccades along the superior-inferior visual axis are mapped across the medial-lateral anatomy of the SC; (2) the saccadic eye-movement representation is in register with the retinotopic organization of visual stimulation; and (3) activity evoked by saccades occurs deeper within SC than that evoked by visual stimulation. These approaches lay the foundation for studying the organization of human subcortical eye-movement mechanisms.HighlightsHigh-resolution functional MRI enabled imaging from intermediate layers of human SCSaccades along superior-inferior visual field are mapped across medial-lateral SCSaccadic eye movement maps lie deeper in SC and are in alignment with retinotopyeTOC BlurbSavjani et al. found the polar angle representation of saccadic eye movements in human SC. The topography is similar in monkey SC, is in register with the retinotopic organization evoked by visual stimulation, but lies within deeper layers. These methods enable investigation of human subcortical eye-movement organization and visual function.

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.

Organization of monkey superior colliculus: enhanced visual response of superficial layer cells

1976 ◽  
Vol 39 (4) ◽  
pp. 745-765 ◽  
Author(s):  
R. H. Wurtz ◽  
C. W. Mohler
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Receptive Field ◽  
Eye Movement ◽  
Superficial Layer ◽  
Enhancement Effect ◽  
Visual Response ◽  
Related Activity ◽  
A Cell ◽  
Hand Response

1. Cells in the superficial layers of monkey superior colliculus respond more vigorously to a spot of light falling in their receptive fields when the monkey uses that spot of light as the target for a saccadic eye movement. Our purpose in these experiments was to investigate the characteristics of this enhancement effect. While monkeys fixated, we determined the response of a cell to a stimulus falling in its receptive field. Then we determined the response of the cell to the same stimulus when the monkey made a saccade to the stimulus or near to it. 2. The enhancement of the visual response is spatially limited. The receptive field of a cell always shows enhancement throughout its extent and frequently shows a slight expansion. Saccades made near to a stimulus in the visual receptive field, but not to it, also lead to an enhancement of that visual stimulus; an area around the excitatory center of the receptive field where such enhancement occurs was referred to as the enhancement field of the cell. An enhanced response in one part of the visual field was not accompanied by depressed responses associated with saccades to other parts of the visual field. 3. The enhancement effect is temporally limited; it begins 200-300 ms before the eye movement, as determined by the increasing response to 50-ms light pulses presented at varying intervals before the eye movement. The degree of enhancement intensifies when the visual stimulus is turned on closer in time to the onset of the saccade. A buildup of the enhancement also occurs on successive trials as does the response of eye movement-related cells in the intermediate layers. 4. The enhancement response is not present in the upper quarter-millimeter of the superficial layers, suggesting that the effect is not present in retinal afferents which terminate primarily in this area of the superficial layers. The enhancement effect is seen throughout the visual field; the foveal area was not tested. 5. In order to determine the relation of the enhancement effect to the monkey's behavioral response, we required the monkey to make a hand response rather than an eye movement-response to the visual stimuli. Cells did not show a clear enhancement with such a hand response. Results of these experiments indicate that the enhancement effect is dependent on the type of response the monkey makes to the stimulus and is probably specifically related to eye movements. Since the enhancement of visual response seems likely to be related specifically to eye movements both on physiological and behavioral grounds, the response-free term "attention" is probably inappropriate for the phenomenon. 6. The hypothesis advanced in the preceding paper that eye movement-related activity from intermediate and deep colliculus layers is directed upward to converge with visually related activity in the superficial layers is extended to include an input from cells in these deeper layers (or their afferents) to the superficial layer cells...

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.

Context dependence of receptive field remapping in superior colliculus

2011 ◽  
Vol 106 (4) ◽  
pp. 1862-1874 ◽  
Author(s):  
Jan Churan ◽  
Daniel Guitton ◽  
Christopher C. Pack
Keyword(s):  
Receptive Field ◽  
Superior Colliculus ◽  
Visual Stimulation ◽  
Receptive Fields ◽  
Spatial Location ◽  
Macaque Monkey ◽  
Visual Signals ◽  
Perceptual Stability ◽  
Visual Background ◽  
The Brain

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.

Spatial determinants of multisensory integration in cat superior colliculus neurons

1996 ◽  
Vol 75 (5) ◽  
pp. 1843-1857 ◽  
Author(s):  
M. A. Meredith ◽  
B. E. Stein
Keyword(s):  
Receptive Field ◽  
Superior Colliculus ◽  
Neuronal Response ◽  
Receptive Fields ◽  
Spatial Relationship ◽  
Physiological Role ◽  
Extracellular Recording ◽  
Average Proportion ◽  
Relationship Of ◽  
High Degree

1. Although a representation of multisensory space is contained in the superior colliculus, little is known about the spatial requirements of multisensory stimuli that influence the activity of neurons here. Critical to this problem is an assessment of the registry of the different receptive fields within individual multisensory neurons. The present study was initiated to determine how closely the receptive fields of individual multisensory neurons are aligned, the physiological role of that alignment, and the possible functional consequences of inducing receptive-field misalignment. 2. Individual multisensory neurons in the superior colliculus of anesthetized, paralyzed cats were studied with the use of standard extracellular recording techniques. The receptive fields of multisensory neurons were large, as reported previously, but exhibited a surprisingly high degree of spatial coincidence. The average proportion of receptive-field overlap was 86% for the population of visual-auditory neurons sampled. 3. Because of this high degree of intersensory receptive-field correspondence, combined-modality stimuli that were coincident in space tended to fall within the excitatory regions of the receptive fields involved. The result was a significantly enhanced neuronal response in 88% of the multisensory neurons studied. If stimuli were spatially disparate, so that one fell outside its receptive field, either a decreased response occurred (56%), or no intersensory effect was apparent (44%). 4. The normal alignment of the different receptive fields of a multisensory neuron could be disrupted by passively displacing the eyes, pinnae, or limbs/body. In no case was a shift in location or size observed in a neuron's other receptive field(s) to compensate for this displacement. The physiological result of receptive-field misalignment was predictable and based on the location of the stimuli relative to the new positions of their respective receptive fields. Now, for example, one component of a spatially coincident pair of stimuli might fall outside its receptive field and inhibit the other's effects. 5. These data underscore the dependence of multisensory integrative responses on the relationship of the different stimuli to their corresponding receptive fields rather than to the spatial relationship of the stimuli to one another. Apparently, the alignment of different receptive fields for individual multisensory neurons ensures that responses to combinations of stimuli derived from the same event are integrated to increase the salience of that event. Therefore the maintenance of receptive-field alignment is critical for the appropriate integration of converging sensory signals and, ultimately, elicitation of adaptive behaviors.

Dependence of Saccade-Related Activity in the Primate Superior Colliculus on Visual Target Presence

2001 ◽  
Vol 86 (2) ◽  
pp. 676-691 ◽  
Author(s):  
Jay A. Edelman ◽  
Michael E. Goldberg
Keyword(s):  
Superior Colliculus ◽  
Visual Target ◽  
Visual Response ◽  
Target Presence ◽  
Related Activity ◽  
Intermediate Layers ◽  
Saccade Velocity ◽  
Trial Basis ◽  
Visual Targets ◽  
Extracellular Activity

Neurons in the intermediate layers of the superior colliculus respond to visual targets and/or discharge immediately before and during saccades. These visual and motor responses have generally been considered independent, with the visual response dependent on the nature of the stimulus, and the saccade-related activity related to the attributes of the saccade, but not to how the saccade was elicited. In these experiments we asked whether saccade-related discharge in the superior colliculus depended on whether the saccade was directed to a visual target. We recorded extracellular activity of neurons in the intermediate layers of the superior colliculus of three rhesus monkeys during saccades in tasks in which we varied the presence or absence of a visual target and the temporal delays between the appearance and disappearance of a target and saccade initiation. Across our sample of neurons ( n = 64), discharge was highest when a saccade was made to a still-present visual target, regardless of whether the target had recently appeared or had been present for several hundred milliseconds. Discharge was intermediate when the target had recently disappeared and lowest when the target had never appeared during that trial. These results are consistent with the hypothesis that saccade-related discharge decreases as the time between the target disappearance and saccade initiation increases. Saccade velocity was also higher for saccades to visual targets, and correlated on a trial-by-trial basis with perisaccadic discharge for many neurons. However, discharge of many neurons was dependent on task but independent of saccade velocity, and across our sample of neurons, saccade velocity was higher for saccades made immediately after target appearance than would be predicted by discharge level. A tighter relationship was found between saccade precision and perisaccadic discharge. These findings suggest that just as the purpose of the saccadic system in primates is to drive the fovea to a visual target, presaccadic motor activity in the superior colliculus is most intense when such a target is actually present. This enhanced activity may, itself, contribute to the enhanced performance of the saccade system when the saccade is made to a real visual target.

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