Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades

1996 ◽  
Vol 76 (2) ◽  
pp. 908-926 ◽  
Author(s):  
J. A. Edelman ◽  
E. L. Keller

1. We recorded visuomotor burst neurons in the deeper layers of the superior colliculus while two monkeys (Macaca fascicularis) made short-latency saccades known as express saccades to visual targets in order to determine whether the visual discharge normally seen for these cells served as the premotor burst during express saccades. We then compared saccade-related activity during express saccades with that recorded during regular latency saccades and delayed saccades. 2. Saccade latency histograms for two monkeys during trials with a temporal gap between fixation-point offset and target onset showed a distinct peak of saccades around 70-80 ms. One monkey also showed an additional peak around 125 ms. 3. Express saccades were found on the average to have the same relationship of saccade peak velocity to saccade amplitude as regular latency saccades and delayed saccades. Express saccades tended to be somewhat more hypometric than the other classes of saccades. However, express saccades were clearly visually guided and not anticipatory responses. 4. For most cells studied (33/40), express saccades were accompanied by a single, uninterrupted burst of activity beginning 40-50 ms after target onset and continuing until sometime around the end of the saccade. For a smaller group of cells (7/40), two peaks of burst activity were seen, although the second peak was smaller and tended to occur late, after saccade onset. Across all cells, the peak of visuomotor cell activity during express saccades correlated just as well with target onset as it did with saccade onset. 5. When considered as discharge temporally aligned to the onset of the saccade, bursts accompanying express saccades tended to begin at approximately the same time as that for regular and delayed saccades. However, this discharge generally peaked earlier for express than for regular and delayed saccades. Also, the magnitude of discharge for express saccades was higher than that for delayed saccades throughout the burst. 6. When considered as discharge temporally aligned to the appearance of the target, bursts began earlier for express and regular saccade trials than for delayed saccade trials. Peak discharge tended to be greater for express saccades than for the other classes of saccades. 7. The results of this investigation are consistent with the suggestion that the visual burst of visuomotor neurons in the deeper layers of the superior colliculus plays a role in the initiation of express saccades similar to that played by the premotor burst for saccades of longer latency. The elevated discharge for express saccades supports the idea that the superior colliculus plays a more critical role in express saccade generation than in the generation of longer-latency saccades. The elevated discharge also suggests that visuomotor bursters do not code one-to-one for saccade velocity nor for saccade dynamic motor error.

2020 ◽  
Vol 123 (5) ◽  
pp. 1907-1919 ◽  
Author(s):  
Suryadeep Dash ◽  
Tyler R. Peel ◽  
Stephen G. Lomber ◽  
Brian D. Corneil

Express saccades are the shortest-latency saccade. The frontal eye fields (FEF) are thought to promote express saccades by presetting the superior colliculus. Here, by reversibly inactivating the FEF either unilaterally or bilaterally via cortical cooling, we support this by showing that the FEF plays a facilitative but not critical role in express saccade generation. We also found that FEF inactivation lowered express saccade peak velocity, emphasizing a contribution of the FEF to express saccade kinematics.


2004 ◽  
Vol 21 (2) ◽  
pp. 119-127 ◽  
Author(s):  
PETER H. SCHILLER ◽  
JOHANNES HAUSHOFER ◽  
GEOFFERY KENDALL

The frequency with which express saccades are generated under a variety of conditions in rhesus monkeys was examined. Increasing the gap time between fixation spot termination and target onset increased express saccade frequency but was progressively less effective in doing so as the number of target positions in the sample was increased. Express saccades were rarely produced when two targets were presented simultaneously and the choice of either of which was rewarded; a temporal asynchrony of only 17 ms between the targets reinstated express saccade generation. Express saccades continued to be generated when the vergence or pursuit systems was coactivated with the saccadic system.


1987 ◽  
Vol 57 (4) ◽  
pp. 1033-1049 ◽  
Author(s):  
P. H. Schiller ◽  
J. H. Sandell ◽  
J. H. Maunsell

Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 81 (5) ◽  
pp. 2279-2296 ◽  
Author(s):  
Vivek Chaturvedi ◽  
Jan A. M. van Gisbergen

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.


1999 ◽  
Vol 22 (4) ◽  
pp. 681-682 ◽  
Author(s):  
Michael C. Dorris ◽  
Douglas P. Munoz

The Findlay & Walker target article emphasizes the role of the target-nonspecific “fixate” system while downplaying the role of the target-specific “move” system in determining saccade latency. We agree that disengagement of the fixate system is responsible for the target-nonspecific latency reduction associated with the gap effect. However, high target predictability and extensive training at a target location can also result in latency reductions, the culmination of this being express saccades. The target-specificity associated with the latter forms of latency reduction implicate a mechanism involving the move system. Recently discovered neurophysiological correlates underlying these behavioural phenomena reside in the superior colliculus.


2016 ◽  
Vol 113 (24) ◽  
pp. 6743-6748 ◽  
Author(s):  
Nathan J. Hall ◽  
Carol L. Colby

A key structure for directing saccadic eye movements is the superior colliculus (SC). The visual pathways that project to the SC have been reported to carry only luminance information and not color information. Short-wavelength–sensitive cones (S-cones) in the retina make little or no contribution to luminance signals, leading to the conclusion that S-cone stimuli should be invisible to SC neurons. The premise that S-cone stimuli are invisible to the SC has been used in numerous clinical and human psychophysical studies. The assumption that the SC cannot use S-cone stimuli to guide behavior has never been tested. We show here that express saccades, which depend on the SC, can be driven by S-cone input. Further, express saccade reaction times and changes in SC activity depend on the amount of S-cone contrast. These results demonstrate that the SC can use S-cone stimuli to guide behavior. We conclude that the use of S-cone stimuli is insufficient to isolate SC function in psychophysical and clinical studies of human subjects.


1998 ◽  
Vol 80 (3) ◽  
pp. 1407-1426 ◽  
Author(s):  
Jay A. Edelman ◽  
Edward L. Keller

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.


2019 ◽  
Author(s):  
Suryadeep Dash ◽  
Tyler R. Peel ◽  
Stephen G. Lomber ◽  
Brian D. Corneil

AbstractExpress saccades (ESs) are a manifestation of a visual grasp reflex triggered when visual information arrives in the intermediate layers of the superior colliculus (SCi), which in turn orchestrates the lower level brainstem saccade generator to evoke a saccade with a very short latency (∼100ms). A prominent theory regarding express saccades generation is that they are facilitated by preparatory signals, presumably from cortical areas, which prime the SCi prior to the arrival of visual information. Here, we test this theory by reversibly inactivating a key cortical input to the SCi, the frontal eye fields (FEF), while monkeys perform an oculomotor task that promotes ES generation. Across three tasks with a different combination of potential target locations and uni- or bilateral FEF inactivation, we found a spared ability for monkeys to generate ESs, despite decreases in ES frequency during FEF inactivation. This result is consistent with the FEF having a facilitatory but not critical role in ES generation, likely because other cortical areas compensate for the loss of preparatory input to the SCi. However, we did find decreases in the accuracy and peak velocity of ESs generated during FEF inactivation, which argues for an influence of the FEF on the saccadic burst generator even during ESs. Overall, our results shed further light on the role of the FEF in the shortest-latency visually-guided eye movements.New & NoteworthyExpress saccades (ESs) are the shortest-latency visually-guided saccade. The frontal eye fields (FEF) is thought to promote ES by establishing the necessary preconditions in the superior colliculus. Here, by reversibly inactivate the FEF either unilaterally or bilaterally, we support this view by showing that the FEF plays an assistive but not critical role in ES generation. We also found that FEF inactivation lowered ES peak velocity, emphasizing a contribution of the FEF to ES kinematics.


1993 ◽  
Vol 70 (2) ◽  
pp. 576-589 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz

1. We tested the hypothesis that a subset of neurons, which we have referred to as fixation cells, located within the rostral pole of the monkey superior colliculus (SC) controls the generation of saccadic eye movements. We altered the activity of these neurons with either electrical stimulation or GABAergic drugs. 2. An increase in the activity of fixation cells in the rostral SC, induced by a train of low-frequency electrical stimulation, delayed the initiation of saccades. With bilateral stimulation the monkey was able to make saccades only after stimulation ceased. 3. Pulses of stimulation delivered during the saccade produced an interruption of the saccade in midflight. The latency to the onset of this perturbation was as short as 12 ms. 4. Injection of the gamma-aminobutyric acid (GABA) antagonist bicuculline into the rostral pole of the SC, which decreases normal GABA inhibition and increases cell activity, increased the latency of saccades to both visual and remembered targets. 5. Injection of the GABA agonist muscimol into the rostral SC, which increases normal GABA inhibition and decreases activity, reduced the latency for saccades to visual targets. The monkey also had difficulty maintaining visual fixation and suppressing unwanted saccades. 6. After muscimol injections, monkeys frequently made very short-latency saccades forming a peak in the saccade latency histogram at < 100 ms. These saccades are similar to express saccades made by normal monkeys. This finding suggests that the fixation cells in the rostral SC are critical for controlling the frequency of express saccades. 7. These results support the hypothesis that fixation cells in the rostral SC inhibit the generation of saccadic eye movements and that they form part of a system of oculomotor control, that of visual fixation.


1996 ◽  
Vol 76 (6) ◽  
pp. 3666-3681 ◽  
Author(s):  
M. Pare ◽  
D. P. Munoz

1. The introduction of a period of darkness between the disappearance of an initial fixation target and the appearance of a peripheral saccade target produces a general reduction in saccadic reaction time (SRT)-known as the gap effect- and often very short latency express saccades. To account for these phenomena, premotor processes may be facilitated by release of visual fixation and advanced preparation of saccadic programs. The experiments described in this paper were designed to test the relevance of the ocular fixation disengagement and oculomotor preparation hypotheses by identifying the influence of different factors on SRTs and the occurrence of express saccades in the monkey. 2. The SRTs of two monkeys were measured in two behavioral paradigms. A peripheral saccade target appeared at the time of disappearance of a central fixation target in the no-gap task, whereas a 200-ms period of no stimuli was interposed between the fixation target disappearance and the saccade target appearance in the gap task. The distribution of SRTs in these tasks was generally bimodal; the first and second mode was composed of express and regular saccades, respectively. We measured the mean SRT, mean regular saccade latency, mean express saccade latency, and percentage of express saccades in both tasks. We also estimated the gap effect, i.e., the difference between the SRTs in no-gap trial and the SRTs in gap trials. 3. Once the animals were trained to make saccades to a single target location and produce express saccades, SRTs in both no-gap and gap trials displayed a broad tuning with respect to the spatial location of the trained target when the target location was varied randomly in a block of trials. Express saccades were made only to a restricted region of the visual field surrounding the trained target location. A gap effect was present for nearly all target locations tested, irrespective of express saccade occurrence. Finally, the probability of generating an express saccade at the trained target location decreased with the introduction of uncertainty about target location. 4. The occurrence of express saccades increased with the duration of the visual and nonvisual (gap) fixation that the animal was required to maintain before the onset of a saccade target. The gap duration was effective in reducing the mean SRT for gaps < or = 300 ms, and it was more influential than comparable variation in the visual fixation duration. 5. The occurrence of express saccades made to targets of identical eccentricity increased when the initial eye fixation position was shifted eccentric in a direction opposite to the saccade direction. Concomitantly, mean SRT decreased by approximately 2 ms for each 1-deg change in initial eye fixation position. 6. The occurrence of express saccades depended upon contextual factors, i.e., on both the behavioral task (no-gap or gap) and the latency of the saccade that the monkey executed to the same target in the preceding trial. The highest percentage of express saccades was observed after an express saccade in a no-gap trial, whereas the lowest percentage was obtained after a regular saccade in a gap trial. 7. These findings indicate that training-dependent express saccades are restricted to a specific spatial location dictated by the training target, and their incidence is facilitated by high predictability of target presentation, long-duration foreperiod, absence of visual fixation, eccentric initial eye position opposite to the saccade direction, and express saccade occurrence in the previous trial. The release of fixation afforded by the gap accounts for the general gap effect, but has only a modulatory influence on express saccade generation. We conclude that advanced motor preparation of saccadic programs generally reduces SRT and is primarily responsible for the occurrence of express saccades, which therefore may be caused mainly by neuronal changes restricted to a specific locus-coding for the trained movemen


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