scholarly journals Activity in the human superior colliculus relating to endogenous saccade preparation and execution

2015 ◽  
Vol 114 (2) ◽  
pp. 1048-1058 ◽  
Author(s):  
Michele Furlan ◽  
Andrew T. Smith ◽  
Robin Walker

In recent years a small number of studies have applied functional imaging techniques to investigate visual responses in the human superior colliculus (SC), but few have investigated its oculomotor functions. Here, in two experiments, we examined activity associated with endogenous saccade preparation. We used 3-T fMRI to record the hemodynamic activity in the SC while participants were either preparing or executing saccadic eye movements. Our results showed that not only executing a saccade (as previously shown) but also preparing a saccade produced an increase in the SC hemodynamic activity. The saccade-related activity was observed in the contralateral and to a lesser extent the ipsilateral SC. A second experiment further examined the contralateral mapping of saccade-related activity with a larger range of saccade amplitudes. Increased activity was again observed in both the contralateral and ipsilateral SC that was evident for large as well as small saccades. This suggests that the ipsilateral component of the increase in BOLD is not due simply to small-amplitude saccades producing bilateral activity in the foveal fixation zone. These studies provide the first evidence of presaccadic preparatory activity in the human SC and reveal that fMRI can detect activity consistent with that of buildup neurons found in the deeper layers of the SC in studies of nonhuman primates.

1995 ◽  
Vol 73 (6) ◽  
pp. 2313-2333 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz

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)


2001 ◽  
Vol 86 (5) ◽  
pp. 2543-2558 ◽  
Author(s):  
Gregory D. Horwitz ◽  
William T. Newsome

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.


2001 ◽  
Vol 86 (5) ◽  
pp. 2629-2633 ◽  
Author(s):  
Richard J. Krauzlis

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.


2005 ◽  
Vol 93 (6) ◽  
pp. 3659-3673 ◽  
Author(s):  
Andrew H. Bell ◽  
M. Alex Meredith ◽  
A. John Van Opstal ◽  
Douglas P. Munoz

Saccades to combined audiovisual stimuli often have reduced saccadic reaction times (SRTs) compared with those to unimodal stimuli. Neurons in the intermediate/deep layers of the superior colliculus (dSC) are capable of integrating converging sensory inputs to influence the time to saccade initiation. To identify how neural processing in the dSC contributes to reducing SRTs to audiovisual stimuli, we recorded activity from dSC neurons while monkeys generated saccades to visual or audiovisual stimuli. To evoke crossmodal interactions of varying strength, we used auditory and visual stimuli of different intensities, presented either in spatial alignment or to opposite hemifields. Spatially aligned audiovisual stimuli evoked the shortest SRTs. In the case of low-intensity stimuli, the response to the auditory component of the aligned audiovisual target increased the activity preceding the response to the visual component, accelerating the onset of the visual response and facilitating the generation of shorter-latency saccades. In the case of high-intensity stimuli, the auditory and visual responses occurred much closer together in time and so there was little opportunity for the auditory stimulus to influence previsual activity. Instead, the reduction in SRT for high-intensity, aligned audiovisual stimuli was correlated with increased premotor activity (activity after visual burst but preceding saccade-aligned burst). These data provide a link between changes in neural activity related to stimulus modality with changes in behavior. They further demonstrate how crossmodal interactions are not limited to the initial sensory activity but can also influence premotor activity in the SC.


2017 ◽  
Author(s):  
Suryadeep Dash ◽  
Tyler R. Peel ◽  
Stephen G. Lomber ◽  
Brian D. Corneil

AbstractA neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of preparatory activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of iSC preparatory activity precede shorter SRTs. The frontal eye fields (FEF) are one likely source of such iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF’s role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys we examined iSC preparatory activity during unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced fixation-related activity in the rostral iSC. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. These analyses revealed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades, suggesting that the integration of preparatory and visual signals in the SC just before saccade initiation is largely independent of the FEF for saccades generated in this task.Significance statementHow does the brain decide when to move? Here, we investigate the role of two oculomotor structures, the superior colliculus (SC) and frontal eye fields (FEF), in dictating visually-guided saccadic reaction times (SRTs). In both structures, higher levels of preparatory activity precede shorter SRTs. Here, we show that FEF inactivation increases SRTs and decreases SC preparatory activity. Surprisingly, a population-level analysis of SC preparatory activity showed a negligible impact of FEF inactivation, providing one examines SRT-matched saccades. Thus, while the FEF is one source of preparatory input to the SC, it is not a critical source, and it is not involved in the integration of preparatory activity and visual signals that precedes saccade initiation in simple visually-guided saccade tasks.


2012 ◽  
Vol 107 (9) ◽  
pp. 2442-2452 ◽  
Author(s):  
Husam A. Katnani ◽  
A. J. Van Opstal ◽  
Neeraj J. Gandhi

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


2002 ◽  
Vol 87 (2) ◽  
pp. 679-695 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs

There is general agreement that saccades are guided to their targets by means of a motor error signal, which is produced by a local feedback circuit that calculates the difference between desired saccadic amplitude and an internal copy of actual saccadic amplitude. Although the superior colliculus (SC) is thought to provide the desired saccadic amplitude signal, it is unclear whether the SC resides in the feedback loop. To test this possibility, we injected muscimol into the brain stem region containing omnipause neurons (OPNs) to slow saccades and then determined whether the firing of neurons at different sites in the SC was altered. In 14 experiments, we produced saccadic slowing while simultaneously recording the activity of a single SC neuron. Eleven of the 14 neurons were saccade-related burst neurons (SRBNs), which discharged their most vigorous burst for saccades with an optimal amplitude and direction (optimal vector). The optimal directions for the 11 SRBNs ranged from nearly horizontal to nearly vertical, with optimal amplitudes between 4 and 17°. Although muscimol injections into the OPN region produced little change in the optimal vector, they did increase mean saccade duration by 25 to 192.8% and decrease mean saccade peak velocity by 20.5 to 69.8%. For optimal vector saccades, both the acceleration and deceleration phases increased in duration. However, during 10 of 14 experiments, the duration of deceleration increased as fast as or faster than that of acceleration as saccade duration increased, indicating that most of the increase in duration occurred during the deceleration phase. SRBNs in the SC changed their burst duration and firing rate concomitantly with changes in saccadic duration and velocity, respectively. All SRBNs showed a robust increase in burst duration as saccadic duration increased. Five of 11 SRBNs also exhibited a decrease in burst peak firing rate as saccadic velocity decreased. On average across the neurons, the number of spikes in the burst was constant. There was no consistent change in the discharge of the three SC neurons that did not exhibit bursts with saccades. Our data show that the SC receives feedback from downstream saccade-related neurons about the ongoing saccades. However, the changes in SC firing produced in our study do not suggest that the feedback is involved with producing motor error. Instead, the feedback seems to be involved with regulating the duration of the discharge of SRBNs so that the desired saccadic amplitude signal remains present throughout the saccade.


1991 ◽  
Vol 6 (1) ◽  
pp. 3-13 ◽  
Author(s):  
James T. McIlwain

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.


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