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

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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Auditory signals evolve from hybrid- to eye-centered coordinates in the primate superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.00706.2011 ◽

2012 ◽

Vol 108 (1) ◽

pp. 227-242 ◽

Cited By ~ 31

Author(s):

Jungah Lee ◽

Jennifer M. Groh

Keyword(s):

Superior Colliculus ◽

Reference Frame ◽

Reference Frames ◽

Visual Response ◽

Response Patterns ◽

Related Activity ◽

Visual Spatial ◽

Auditory Representation ◽

Auditory Signals ◽

Visual Targets

Visual and auditory spatial signals initially arise in different reference frames. It has been postulated that auditory signals are translated from a head-centered to an eye-centered frame of reference compatible with the visual spatial maps, but, to date, only various forms of hybrid reference frames for sound have been identified. Here, we show that the auditory representation of space in the superior colliculus involves a hybrid reference frame immediately after the sound onset but evolves to become predominantly eye centered, and more similar to the visual representation, by the time of a saccade to that sound. Specifically, during the first 500 ms after the sound onset, auditory response patterns ( N = 103) were usually neither head nor eye centered: 64% of neurons showed such a hybrid pattern, whereas 29% were more eye centered and 8% were more head centered. This differed from the pattern observed for visual targets ( N = 156): 86% were eye centered, <1% were head centered, and only 13% exhibited a hybrid of both reference frames. For auditory-evoked activity observed within 20 ms of the saccade ( N = 154), the proportion of eye-centered response patterns increased to 69%, whereas the hybrid and head-centered response patterns dropped to 30% and <1%, respectively. This pattern approached, although did not quite reach, that observed for saccade-related activity for visual targets: 89% were eye centered, 11% were hybrid, and <1% were head centered ( N = 162). The plainly eye-centered visual response patterns and predominantly eye-centered auditory motor response patterns lie in marked contrast to our previous study of the intraparietal cortex, where both visual and auditory sensory and motor-related activity used a predominantly hybrid reference frame ( Mullette-Gillman et al. 2005 , 2009 ). Our present findings indicate that auditory signals are ultimately translated into a reference frame roughly similar to that used for vision, but suggest that such signals might emerge only in motor areas responsible for directing gaze to visual and auditory stimuli.

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Saccade-Related Activity in the Primate Superior Colliculus Depends on the Presence of Local Landmarks at the Saccade Endpoint

Journal of Neurophysiology ◽

10.1152/jn.00016.2003 ◽

2003 ◽

Vol 90 (3) ◽

pp. 1728-1736 ◽

Cited By ~ 14

Author(s):

Jay A. Edelman ◽

Michael E. Goldberg

Keyword(s):

Superior Colliculus ◽

Intermediate Layer ◽

High Contrast ◽

Blank Space ◽

Complete Darkness ◽

Related Activity ◽

Visual Landmarks ◽

Small Spot ◽

Saccade Velocity ◽

Dark Space

Saccade-related discharge in the superior colliculus is greater for saccades made to a spot of light than for saccades in complete darkness. However, it is unclear whether this enhancement is due to the discontinuity of the spot or due to its being a new object of fixation. In these experiments, we examined the saccade-related activity of intermediate-layer neurons in the primate superior colliculus during delayed saccades to the center or corner of a large, bright square, as well as for visual and memory-guided movements to small spots in isolation. The saccade-related discharge for movements made to a local visual landmark present at the time of the saccade, be it a corner of a square or a small spot, was higher than that for saccades made to the center of a square that contained no local visual landmarks within. Moreover, discharge for movements to the center of a square were very similar to that for saccades to blank, dark space. Saccade velocity was similarly dependent on the presence of such a landmark, though less dramatically. The endpoints of saccades directed toward a square's corner were slightly displaced toward the center of the square. Across all neurons, discharge and velocity for saccades to the center of a square increased as the square size was decreased, but were never greater than those for saccades to a small spot of light. These results suggest that both saccade-related discharge in the superior colliculus and saccade metrics are enhanced for movements directed to parts of the visual scene with high contrast, while shifting fixation to a new object is not itself sufficient to elevate discharge and metrics above those of saccades to blank space.

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

Journal of Neurophysiology ◽

10.1152/jn.1994.72.6.2754 ◽

1994 ◽

Vol 72 (6) ◽

pp. 2754-2770 ◽

Cited By ~ 75

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)

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

Journal of Neurophysiology ◽

10.1152/jn.00053.2009 ◽

2009 ◽

Vol 101 (6) ◽

pp. 2934-2942 ◽

Cited By ~ 13

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.

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

Journal of Neurophysiology ◽

10.1152/jn.1995.73.5.1988 ◽

1995 ◽

Vol 73 (5) ◽

pp. 1988-2003 ◽

Cited By ~ 221

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)

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Dependence on Target Configuration of Express Saccade-Related Activity in the Primate Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.1998.80.3.1407 ◽

1998 ◽

Vol 80 (3) ◽

pp. 1407-1426 ◽

Cited By ~ 65

Author(s):

Jay A. Edelman ◽

Edward L. Keller

Keyword(s):

Superior Colliculus ◽

Target Selection ◽

Visual Response ◽

Express Saccades ◽

Related Activity ◽

Express Saccade ◽

Spatial Properties ◽

Target Configuration ◽

Single Target ◽

Single Burst

Edelman, Jay A. and Edward L. Keller. Dependence on target configuration of express saccade-related activity in the primate superior colliculus. J. Neurophysiol. 80: 1407–1426, 1998. To help understand how complex visual stimuli are processed into short-latency saccade motor programs, the activity of visuomotor neurons in the deeper layers of the superior colliculus was recorded while two monkeys made express saccades to one target and to two targets. It has been shown previously that the visual response and perimotor discharge characteristic of visuomotor neurons temporally coalesce into a single burst of discharge for express saccades. Here we seek to determine whether the distributed visual response to two targets spatially coalesces into a command appropriate for the resulting saccade. Two targets were presented at identical radial eccentricities separated in direction by 45°. A gap paradigm was used to elicit express saccades. Express saccades were more likely to land in between the two targets than were saccades of longer latency. The speeds of express saccades to two targets were similar to those of one target of similar vector, as were the trajectories of saccades to one and two targets. The movement fields for express saccades to two targets were more broad than those for saccades to one target for all neurons studied. For most neurons, the spatial pattern of discharge for saccades to two targets was better explained as a scaled version of the visual response to two spatially separate targets than as a scaled version of the perimotor response accompanying a saccade to a single target. Only the discharge of neurons with large movement fields could be equally well explained as a visual response to two targets or as a perimotor response for a one-target saccade. For most neurons, the spatial properties of discharge depended on the number of targets throughout the entire saccade-related burst. These results suggest that for express saccades to two targets the computation of saccade vector is not complete at the level of the superior colliculus for most neurons and an explicit process of target selection is not necessary at this level for the programming of an express saccade.

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Extraretinal Inputs to Neurons in the Rostral Superior Colliculus of the Monkey During Smooth-Pursuit Eye Movements

Journal of Neurophysiology ◽

10.1152/jn.2001.86.5.2629 ◽

2001 ◽

Vol 86 (5) ◽

pp. 2629-2633 ◽

Cited By ~ 21

Author(s):

Richard J. Krauzlis

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Smooth Pursuit ◽

Saccadic Eye Movements ◽

Visual Response ◽

Smooth Pursuit Eye Movements ◽

Related Activity ◽

Pursuit Eye Movements ◽

Deep Layers ◽

Almost All

The intermediate and deep layers of the monkey superior colliculus (SC) are known to be important for the generation of saccadic eye movements. Recent studies have also provided evidence that the rostral SC might be involved in the control of pursuit eye movements. However, because rostral SC neurons respond to visual stimuli used to guide pursuit, it is also possible that the pursuit-related activity is simply a visual response. To test this possibility, we recorded the activity of neurons in the rostral SC as monkeys smoothly pursued a target that was briefly extinguished. We found that almost all rostral SC neurons in our sample maintained their pursuit-related activity during a brief visual blink, which was similar to the maintained activity they also exhibited during blinks imposed during fixation. These results indicate that discharge of rostral SC neurons during pursuit is not simply a visual response, but includes extraretinal signals.

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Saccades to somatosensory targets. II. motor convergence in primate superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.1996.75.1.428 ◽

1996 ◽

Vol 75 (1) ◽

pp. 428-438 ◽

Cited By ~ 43

Author(s):

J. M. Groh ◽

D. L. Sparks

Keyword(s):

Motor Activity ◽

Superior Colliculus ◽

Large Population ◽

Reaction Times ◽

The Body ◽

Behavioral Characteristics ◽

Related Activity ◽

Motor Pathway ◽

Visual Targets ◽

Motor Cells

1. We examined cells with saccade-related activity in the superior colliculus (SC) of monkeys performing saccades to both somatosensory and visual targets. Our goals were 1) to determine whether signals from these separate sensory systems have converged onto a common motor pathway by the level of the SC; 2) to determine the frame of reference of somatosensory saccade signals in the SC; and 3) to relate collicular motor activity to the behavioral characteristics of somatosensory saccades. 2. Somatosensory targets consisted of vibrotactile stimuli delivered to the hands, which were held in fixed spatial positions. Saccades of different directions and amplitudes were elicited from different initial eye positions. Of 86 cells with motor-related activity, 85 (99%) discharged for saccades to both visual and somatosensory targets. The remaining cell was active only for visual saccades. 3. Cells with saccade-related activity had movement fields representing the direction and amplitude of saccades to both visual and somatosensory targets. We found no cells that discharged for saccades to a particular somatosensory target regardless of the vector of the saccade. 4. Small modality-dependent differences in the spatial tuning of the movement fields were observed, but these variations formed no clear pattern. Given the large population of cells active in conjunction with each saccade, these small tuning differences may have no net effect. Because the visual and somatosensory movement fields of individual cells were similar to each other, the inaccuracy of somatosensory saccades is likely to be the result of inaccurate signals reaching the SC, rather than an error signal added downstream. 5. The peak discharge frequency of collicular motor cells was lower for somatosensory saccades than for visual saccades, although the number of spikes in the discharge was about the same. 6. The latency of the onset of the prelude of motor activity following the cue to initiate a saccade was about the same for somatosensory and visual trials, even though somatosensory saccades have longer reaction times than visual saccades. However, the peak of the motor activity was delayed on somatosensory trials such that the timing of the peak was the same with respect to the movement on somatosensory and visual trials. 7. We conclude that the same population of saccade-related neurons in the SC that represents saccades to visual targets also represents saccades to somatosensory targets. Somatosensory saccades are encoded by these cells as the change in eye position necessary to bring the target onto the fovea, rather than the location of the stimulus on the body surface. Modality-dependent differences in the frequency and timing of collicular motor activity may contribute to velocity and reaction time differences.

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