Competition Between Saccade Goals in the Superior Colliculus Produces Saccade Curvature

2003 ◽  
Vol 89 (5) ◽  
pp. 2577-2590 ◽  
Author(s):  
Robert M. McPeek ◽  
Jae H. Han ◽  
Edward L. Keller
Keyword(s):  
Superior Colliculus ◽  
Search Task ◽  
Visual Target ◽  
Temporal Structure ◽  
Saccade Target ◽  
Stimulation Site ◽  
Electrical Microstimulation ◽  
Saccade Onset ◽  
Significant Difference ◽  
Increased Activity

When saccadic eye movements are made in a search task that requires selecting a target from distractors, the movements show greater curvature in their trajectories than similar saccades made to single stimuli. To test the hypothesis that this increase in curvature arises from competitive interactions between saccade goals occurring near the time of movement onset, we performed single-unit recording and microstimulation experiments in the superior colliculus (SC). We found that saccades that ended near the target but curved toward a distractor were accompanied by increased presaccadic activity of SC neurons coding the distractor site. This increased activity occurred ∼30 ms before saccade onset and was abruptly quenched on saccade initiation. The magnitude of increased activity at the distractor site was correlated with the amount of curvature toward the distractor. In contrast, neurons coding the target location did not show any significant difference in discharge for curved versus straight saccades. To determine whether this pattern of SC discharge is causally related to saccade curvature, we performed a second series of experiments using electrical microstimulation. Monkeys made saccades to single visual stimuli presented without distractors, and we stimulated sites in the SC that would have corresponded to distractor sites in the search task. The stimulation was subthreshold for evoking saccades, but when its temporal structure mimicked the activity recorded for curved saccades in search, the subsequent saccades to the visual target showed curvature toward the location coded by the stimulation site. The effect was larger for higher stimulation frequencies and when the stimulation site was in the same colliculus as the representation of the visual target. These results support the hypothesis that the increased saccade curvature observed in search arises from rivalry between target and distractor goals and are consistent with the idea that the SC is involved in the competitive neural interactions underlying saccade target selection.

Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells

1995 ◽  
Vol 73 (6) ◽  
pp. 2313-2333 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz
Keyword(s):  
Superior Colliculus ◽  
High Frequency ◽  
Low Frequency ◽  
Striking Difference ◽  
Related Activity ◽  
Slow Increase ◽  
High Frequency Discharge ◽  
Optimal Direction ◽  
Saccade Onset ◽  
Increased Activity

1. In the monkey superior colliculus (SC), the activity of most saccade-related neurons studied so far consists of a burst of activity in a population of cells at one place on the SC movement map. In contrast, recent experiments in the cat have described saccade-related activity as a slow increase in discharge before saccades followed by a hill of activity moving across the SC map. In order to explore this striking difference in the distribution of activity across the SC, we recorded from all saccade-related neurons that we encountered in microelectrode penetrations through the monkey SC and placed them in categories according to their activity during the generation of saccades. 2. When we considered the activity preceding the onset of the saccade, we could divide the cells into two categories. Cells with burst activity had a high-frequency discharge just before saccade onset but little activity between the signal to make a saccade and saccade onset. About two thirds of the saccade-related cells had only a burst of activity. Cells with a buildup of activity began to discharge at a low frequency after the signal to make a saccade and the discharge continued until generation of the saccade. About one third of the saccade-related cells studied had a buildup of activity, and about three fourths of these cells also gave a burst of activity with the saccade in addition to the slow buildup of activity. 3. The buildup of activity seemed to be more closely related to preparation to make a saccade than to the generation of the saccade. The buildup developed even in cases when no saccade occurred. 4. The falling phase of the discharge of these saccade-related cells stopped with the end of the saccade (a clipped discharge), shortly after the end of the saccade (partially clipped), or long after the end of the saccade (unclipped). 5. Some cells had closed movement fields in which saccades that were substantially smaller or larger than the optimal amplitude were not associated with increased activity. Other cells tended to have open-ended movement fields without any peripheral border; they were active for all saccades of optimal direction whose amplitudes were equal to or greater than a given amplitude.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Reversal of a Distractor Effect on Saccade Target Selection After Superior Colliculus Inactivation

2008 ◽  
Vol 99 (5) ◽  
pp. 2694-2702 ◽  
Author(s):  
Robert M. McPeek
Keyword(s):  
Superior Colliculus ◽  
Search Task ◽  
Target Location ◽  
Target Selection ◽  
Saccade Target ◽  
Search Array ◽  
Distractor Effect ◽  
Normal Trend ◽  
Winner Take All ◽  
Take All

Recent evidence indicates that inactivation of the primate superior colliculus (SC) results in an increase in saccade target-selection errors. The pattern of errors suggests that a winner-take-all competition selects the saccade goal and that SC inactivation perturbs this process by biasing the competition against stimuli in the inactivated field. To investigate this idea, the difficulty of target selection was manipulated in a color-oddity search task by varying the number of homogeneous distractors in the search array. Previous studies have shown that target selection is easier when a greater number of homogeneous distractors is present, due to perceptual grouping of the distractors. These results were replicated when testing with the SC intact. Surprisingly, during SC inactivation, this normal trend was reversed: target-selection performance declined significantly with more distractors, resulting in a greater proportion of errant saccades to distractors. Examination of the saccade endpoints indicates that after SC inactivation, many errant saccades were directed to distractors adjacent to the target. This pattern of results suggests that the salience signal used by the SC for target selection is relatively broad in spatial scope. As a result, when the area of the SC representing the target location is inactivated, distractors near the target are at a competitive advantage relative to more distant distractors and, consequently, are selected more often as the saccade goal. This contributes to the trend of worse performance with more distractors due to the greater proximity of distractors to the target.

scholarly journals Incomplete Suppression of Distractor-Related Activity in the Frontal Eye Field Results in Curved Saccades

2006 ◽  
Vol 96 (5) ◽  
pp. 2699-2711 ◽  
Author(s):  
Robert M. McPeek
Keyword(s):  
Target Location ◽  
Temporal Structure ◽  
Target Selection ◽  
Neural Correlates ◽  
Frontal Eye Field ◽  
Stimulation Site ◽  
Related Activity ◽  
Distractor Location ◽  
Significant Difference ◽  
Eye Field

Saccades in the presence of distractors show significant trajectory curvature. Based on previous work in the superior colliculus (SC), we speculated that curvature arises when a movement is initiated before competition between the target and distractor goals has been fully resolved. To test this hypothesis, we recorded frontal eye field (FEF) activity for curved and straight saccades in search. In contrast to the SC, activity in FEF is normally poorly correlated with saccade dynamics. However, the FEF, like the SC, is involved in target selection. Thus if curvature is caused by incomplete target selection, we expect to see its neural correlates in the FEF. We found that saccades that curve toward a distractor are accompanied by an increase in perisaccadic activity of FEF neurons coding the distractor location, and saccades that curve away are accompanied by a decrease in activity. In contrast, for FEF neurons coding the target location, there is no significant difference in activity between curved and straight saccades. To establish that the distractor-related activity is causally related to saccade curvature, we applied microstimulation to sites in the FEF before saccades to targets presented without distractors. The stimulation was subthreshold for evoking saccades and the temporal structure of the stimulation train resembled the activity recorded for curved saccades. The resulting movements curved toward the location coded by the stimulation site. These results support the idea that saccade curvature results from incomplete suppression of distractor-related activity during target selection.

Activity of the Brain Stem Omnipause Neurons During Saccades Perturbed by Stimulation of the Primate Superior Colliculus

1999 ◽  
Vol 82 (6) ◽  
pp. 3254-3267 ◽  
Author(s):  
Neeraj J. Gandhi ◽  
Edward L. Keller
Keyword(s):  
Superior Colliculus ◽  
Lead Time ◽  
Excitatory Input ◽  
Initial Component ◽  
Stimulation Site ◽  
Sequence Of Events ◽  
Saccade Onset ◽  
The Mean ◽  
And Control ◽  
Stimulation Of

Stimulation of the rostral ∼2 mm of the superior colliculus (SC) during a large, visual target-initiated saccade produces a spatial deviation of the ongoing saccade and then stops it in midflight. After the termination of the stimulation, the saccade resumes and ends near the location of the flashed target. The density of collicular projections to the omnipause neuron (OPN) region is greatest from the rostral SC and decreases gradually for the more caudal regions. It has been hypothesized that the microstimulation excites the OPNs through these direct connections, and the reactivation of OPNs, which are normally silent during saccades, stops the initial component in midflight by gating off the saccadic burst generator. Two predictions emerge from this hypothesis: 1) for microstimulation triggered on the onset of large saccades, the time from stimulation onset to resumption of OPN discharge should decrease as the stimulation site is moved rostral and 2) the lead time from reactivation of OPNs to the end of the initial saccade on stimulation trials should be equal to the lead time of pause end with respect to the end of control saccades. We tested this hypothesis by recording OPN activity during saccades perturbed by stimulation of the rostral ∼2 mm of the SC. The distance of the stimulation site from the most rostral extent of the SC and the time of reactivation with respect to stimulation onset were not significantly correlated. The mean lead of reactivation of OPNs relative to the end of the initial component of perturbed saccades (6.5 ms) was significantly less than the mean lead with respect to the end of control (9.6 ms) and resumed saccades (10.4 ms). These results do not support the notion that the excitatory input from SC neurons—in particular, the fixation neurons in the rostral SC—provide the major signal to reactivate OPNs and end saccades. An alternative, conceptual model to explain the temporal sequence of events induced by stimulation of the SC during large saccades is presented. Other OPN activity parameters also were measured and compared for control and stimulation conditions. The onset of pause with respect to resumed saccade onset was larger and more variable than the onset of pause with respect to control saccades, whereas pause end with respect to the end of resumed and control saccades was similar. The reactivated discharge of OPNs during the period between the end of the initial and the onset of the resumed saccades was at least as strong as that following control movements. This latter observation is interpreted in terms of the resettable neural integrator hypothesis.

scholarly journals Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

2012 ◽  
Vol 108 (5) ◽  
pp. 1392-1402 ◽  
Author(s):  
Elsie Premereur ◽  
Wim Vanduffel ◽  
Pieter R. Roelfsema ◽  
Peter Janssen
Keyword(s):  
Spatial Attention ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Oculomotor Control ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Alpha Power ◽  
Lateral Intraparietal Area ◽  
Electrical Microstimulation ◽  
Gamma Power

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.

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.

Differences in intersaccadic adaptation transfer between inward and outward adaptation

2011 ◽  
Vol 106 (3) ◽  
pp. 1399-1410 ◽  
Author(s):  
Fabian Schnier ◽  
Markus Lappe
Keyword(s):  
Peak Velocity ◽  
The Other ◽  
Saccade Target ◽  
Control Mechanisms ◽  
Saccadic Adaptation ◽  
Saccade Onset ◽  
Independent Parameters ◽  
Saccade Duration ◽  
Velocity Decrease

Saccadic adaptation is a mechanism to increase or decrease the amplitude gain of subsequent saccades, if a saccade is not on target. Recent research has shown that the mechanism of gain increasing, or outward adaptation, and the mechanism of gain decreasing, or inward adaptation, rely on partly different processes. We investigate how outward and inward adaptation of reactive saccades transfer to other types of saccades, namely scanning, overlap, memory-guided, and gap saccades. Previous research has shown that inward adaptation of reactive saccades transfers only partially to these other saccade types, suggesting differences in the control mechanisms between these saccade categories. We show that outward adaptation transfers stronger to scanning and overlap saccades than inward adaptation, and that the strength of transfer depends on the duration for which the saccade target is visible before saccade onset. Furthermore, we show that this transfer is mainly driven by an increase in saccade duration, which is apparent for all saccade categories. Inward adaptation, in contrast, is accompanied by a decrease in duration and in peak velocity, but only the peak velocity decrease transfers from reactive saccades to other saccade categories, i.e., saccadic duration remains constant or even increases for test saccades of the other categories. Our results, therefore, show that duration and peak velocity are independent parameters of saccadic adaptation and that they are differently involved in the transfer of adaptation between saccade categories. Furthermore, our results add evidence that inward and outward adaptation are different processes.

scholarly journals Perturbation of Combined Saccade-Vergence Movements by Microstimulation in Monkey Superior Colliculus

1999 ◽  
Vol 81 (5) ◽  
pp. 2279-2296 ◽  
Author(s):  
Vivek Chaturvedi ◽  
Jan A. M. van Gisbergen
Keyword(s):  
Superior Colliculus ◽  
Local Population ◽  
Three Dimensional ◽  
Weighted Averaging ◽  
Target Onset ◽  
Saccade Onset ◽  
Different Depths

Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus. This study investigated the role of the monkey superior colliculus (SC) in the control of visually (V)-guided combined saccade-vergence movements by assessing the perturbing effects of microstimulation. We elicited an electrical saccade (E) by stimulation (in 20% of trials) in the SC while the monkey was preparing a V-guided movement to a near target. The target was aligned such that E- and V-induced saccades had similar amplitudes but different directions and such that V-induced saccades had a significant vergence component (saccades to a near target). The onset of the E-stimulus was varied from immediately after V-target onset to after V-saccade onset. E-control trials, where stimulation was applied during fixation of a V-target, yielded the expected saccade but no vergence. By contrast, early perturbation trials, where the E-stimulus was applied soon after the onset of the V-target, caused an E-triggered response with a clear vergence component toward the V-target. Midflight perturbation, timed to occur just after the monkey initiated the movement toward the target, markedly curtailed the ongoing vergence component during the saccade. Examination of pooled responses from both types of perturbation trials showed weighted-averaging effects between E- and V-stimuli in both saccade and fast vergence components. Both components exhibited a progression from E- to V-dominance as the E-stimulus was delayed further. This study shows that artificial intervention in the SC, while a three-dimensional (3D) refixation is being prepared or is ongoing, can affect the timing (when) and the metric specification (where) of both saccades and vergence. To explain this we interpret the absence of overt vergence in the E-controls as being caused by a zero-vergence change command rather than reflecting the mere absence of a collicular vergence signal. In the perturbation trials, the E-evoked zero-vergence signal competes with the V-initiated saccade-vergence signal, thereby giving rise to a compromised 3D response. This effect would be expected if the population of movement cells at each SC site is tuned in 3D, combining the well-known topographical code for direction and amplitude with a nontopographical depth representation. On E-stimulation, the local population would yield a net saccade signal caused by the topography, but the cells coding for different depths would be excited equally, causing the vergence change to be zero.

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.

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