Evidence That the Superior Colliculus Participates in the Feedback Control of Saccadic Eye Movements

2002 ◽  
Vol 87 (2) ◽  
pp. 679-695 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs
Keyword(s):  
Superior Colliculus ◽  
Firing Rate ◽  
Saccadic Eye Movements ◽  
Burst Duration ◽  
Saccadic Amplitude ◽  
Optimal Vector ◽  
Deceleration Phase ◽  
Acceleration And Deceleration ◽  
Motor Error ◽  
Saccade Duration

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.

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)

Evidence Against a Moving Hill in the Superior Colliculus During Saccadic Eye Movements in the Monkey

2002 ◽  
Vol 87 (6) ◽  
pp. 2778-2789 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Saccadic Eye Movements ◽  
Conclusive Evidence ◽  
Topographic Map ◽  
Hill Model ◽  
Saccade Onset ◽  
Motor Error ◽  
Deep Layers ◽  
The Hill

Saccadic eye movements of different sizes and directions are represented in an orderly topographic map across the intermediate and deep layers of the superior colliculus (SC), where large saccades are encoded caudally and small saccades rostrally. Based on experiments in the cat, it has been suggested that saccades are initiated by a hill of activity at the caudal site appropriate for a particular saccade. As the saccade evolves and the remaining distance to the target, the motor error, decreases, the hill moves rostrally across successive SC sites responsible for saccades of increasingly smaller amplitudes. When the hill reaches the “fixation zone” in the rostral SC, the saccade is terminated. A moving hill of activity has also been posited for the monkey, in which it is supposed to be transported via so-called build-up neurons (BUNs), which have a prelude of activity that culminates in a burst for saccades. However, several studies using a variety of approaches have yet to provide conclusive evidence for or against a moving hill. The moving hill scenario predicts that during a large saccade the burst of a BUN in the rostral SC will be delayed until the motor error remaining in the evolving saccade is equal to the saccadic amplitude for which that BUN discharges best, i.e., its optimal amplitude. Therefore a plot of the burst lead preceding the “optimal” motor error against the time of occurrence of the optimal motor error should have a slope of zero. A slope of −1 indicates no moving hill. For our 20 BUNs, we used three measures of burst timing: the leads to the onset, peak, and center of the burst. The average slopes of these relations were −1.09, −0.79, and −0.58, respectively. For individual BUNs, the slopes of all three relations always differed significantly from zero. Although the peak and center leads fall between −1 and 0, a hill of activity moving rostrally at a rate indicated by either of these slopes would arrive at the fixation zone much too late to terminate the saccade at the appropriate time. Calculating our same three timing measures from averaged data leads us to the same conclusion. Thus our data do not support the moving hill model. However, we argue in the discussion that the constant lead of the burst onset relative to saccade onset (∼27 ms) suggests that the BUNs may help to trigger the saccade.

scholarly journals TEMPORAL ANALYSIS OF THE ACCELERATION AND DECELERATION PHASES FOR VISUAL SACCADES

2004 ◽  
Vol 16 (06) ◽  
pp. 355-362 ◽  
Author(s):  
HSUAN-HUNG LIN ◽  
YUNG-FU CHEN ◽  
TAINSONG CHEN ◽  
TZU-TUNG TSAI ◽  
KUO-HSIEN HUANG
Keyword(s):  
Peak Velocity ◽  
Temporal Analysis ◽  
Shape Parameters ◽  
Saccadic Amplitude ◽  
Acceleration Time ◽  
Deceleration Phase ◽  
Acceleration Amplitude ◽  
Acceleration And Deceleration ◽  
Triangular Profile ◽  
Deceleration Time

Previous studies showed that the relation for product of peak velocity and duration against saccadic amplitude was highly linear correlated. The velocity profile was related as a triangular profile and referred to the saccadic amplitude as an integration of the profile, so that the amplitude is proportional to the product of peak velocity and duration. The saccadic amplitude can be described as a function of peak velocity and duration. In this study, in addition to the triangular profile, the rational power function was applied to explain the above linear relation. The acceleration and deceleration phases can be described, respectively, with the different shape parameters (n1 and n2). Finally, we described the product of peak velocity and acceleration time relating to the acceleration amplitude, and the product of peak velocity and deceleration time relating to the deceleration amplitude. The results show that the acceleration and deceleration phase parameters could be used to accurately delineate the saccadic characteristics.

scholarly journals A test of spatial temporal decoding mechanisms in the superior colliculus

2012 ◽  
Vol 107 (9) ◽  
pp. 2442-2452 ◽  
Author(s):  
Husam A. Katnani ◽  
A. J. Van Opstal ◽  
Neeraj J. Gandhi
Keyword(s):  
Nervous System ◽  
Motor Control ◽  
Eye Movements ◽  
Superior Colliculus ◽  
Motor Behavior ◽  
Saccadic Eye Movements ◽  
Population Coding ◽  
Population Activity ◽  
Low Levels

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.

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.

scholarly journals Neuronal modulation in the mouse superior colliculus during covert visual selective attention

2021 ◽  
Author(s):  
Lupeng Wang ◽  
James P. Herman ◽  
Richard J. Krauzlis
Keyword(s):  
Visual Attention ◽  
Selective Attention ◽  
Superior Colliculus ◽  
Firing Rate ◽  
Spatial Location ◽  
Relevant Information ◽  
Brain Regions ◽  
Uncued Location ◽  
Visual Selective Attention ◽  
Covert Visual Attention

AbstractCovert visual attention is accomplished by a cascade of mechanisms distributed across multiple brain regions. Recent studies in primates suggest a parcellation in which visual cortex is associated with enhanced representations of relevant stimuli, whereas subcortical circuits are associated with selection of visual targets and suppression of distractors. Here we identified how neuronal activity in the superior colliculus (SC) of head-fixed mice is modulated during covert visual attention. We found that spatial cues modulated both firing rate and spike-count correlations, and that the cue-related modulation in firing rate was due to enhancement of activity at the cued spatial location rather than suppression at the uncued location. This modulation improved the neuronal discriminability of visual-change-evoked activity between contralateral and ipsilateral SC neurons. Together, our findings indicate that neurons in the mouse SC contribute to covert visual selective attention by biasing processing in favor of locations expected to contain relevant information.

scholarly journals Normal correspondence of tectal maps for saccadic eye movements in strabismus

2016 ◽  
Vol 116 (6) ◽  
pp. 2541-2549 ◽  
Author(s):  
John R. Economides ◽  
Daniel L. Adams ◽  
Jonathan C. Horton
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Superior Colliculus ◽  
Saccadic Eye Movements ◽  
Systematic Change ◽  
Free Viewing ◽  
Pattern Deviation ◽  
Ocular Deviation ◽  
The Right ◽  
Stem Structure

The superior colliculus is a major brain stem structure for the production of saccadic eye movements. Electrical stimulation at any given point in the motor map generates saccades of defined amplitude and direction. It is unknown how this saccade map is affected by strabismus. Three macaques were raised with exotropia, an outwards ocular deviation, by detaching the medial rectus tendon in each eye at age 1 mo. The animals were able to make saccades to targets with either eye and appeared to alternate fixation freely. To probe the organization of the superior colliculus, microstimulation was applied at multiple sites, with the animals either free-viewing or fixating a target. On average, microstimulation drove nearly conjugate saccades, similar in both amplitude and direction but separated by the ocular deviation. Two monkeys showed a pattern deviation, characterized by a systematic change in the relative position of the two eyes with certain changes in gaze angle. These animals' saccades were slightly different for the right eye and left eye in their amplitude or direction. The differences were consistent with the animals' underlying pattern deviation, measured during static fixation and smooth pursuit. The tectal map for saccade generation appears to be normal in strabismus, but saccades may be affected by changes in the strabismic deviation that occur with different gaze angles.

scholarly journals Blink-Perturbed Saccades in Monkey. II. Superior Colliculus Activity

2000 ◽  
Vol 83 (6) ◽  
pp. 3430-3452 ◽  
Author(s):  
H.H.L.M. Goossens ◽  
A. J. Van Opstal
Keyword(s):  
Superior Colliculus ◽  
Firing Rate ◽  
High Frequency ◽  
Displacement Vector ◽  
Neural Mechanism ◽  
Fixed Number ◽  
Deep Layers ◽  
The Mean ◽  
Reflex Blinks ◽  
Frequency Burst

Trigeminal reflex blinks evoked near the onset of a saccade cause profound spatial-temporal perturbations of the saccade that are typically compensated in mid-flight. This paper investigates the influence of reflex blinks on the discharge properties of saccade-related burst neurons (SRBNs) in intermediate and deep layers of the monkey superior colliculus (SC). Twenty-nine SRBNs, recorded in three monkeys, were tested in the blink-perturbation paradigm. We report that the air puff stimuli, used to elicit blinks, resulted in a short-latency (∼10 ms) transient suppression of saccade-related SRBN activity. Shortly after this suppression (within 10–30 ms), all neurons resumed their activity, and their burst discharge then continued until the perturbed saccade ended near the extinguished target. This was found regardless whether the compensatory movement was into the cell's movement field or not. In the limited number of trials where no compensation occurred, the neurons typically stopped firing well before the end of the eye movement. Several aspects of the saccade-related activity could be further quantified for 25 SRBNs. It appeared that 1) the increase in duration of the high-frequency burst was well correlated with the (two- to threefold) increase in duration of the perturbed movement. 2) The number of spikes in the burst for control and perturbed saccades was quite similar. On average, the number of spikes increased only 14%, whereas the mean firing rate in the burst decreased by 52%. 3) An identical number of spikes were obtained between control and perturbed responses when burst and postsaccadic activity were both included in the spike count. 4) The decrease of the mean firing rate in the burst was well correlated with the decrease in the velocity of perturbed saccades. 5) Monotonic relations between instantaneous firing rate and dynamic motor error were obtained for control responses but not for perturbed responses. And 6) the high-frequency burst of SRBNs with short-lead and long-lead presaccadic activity (also referred to as burst and buildup neurons, respectively) showed very similar features. Our findings show that blinking interacts with the saccade premotor system already at the level of the SC. The data also indicate that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensation for blink-related perturbations. We propose that these interactions occur downstream from the motor SC and that the latter may encode the desired displacement vector of the eyes by sending an approximately fixed number of spikes to the brainstem saccadic burst generator.

Modified saccades evoked by stimulation of the macaque superior colliculus account for properties of the resettable integrator

1995 ◽  
Vol 73 (4) ◽  
pp. 1724-1728 ◽  
Author(s):  
A. A. Kustov ◽  
D. L. Robinson
Keyword(s):  
Superior Colliculus ◽  
Pulse Signal ◽  
Good Evidence ◽  
Visually Guided ◽  
Saccadic System ◽  
Time Period ◽  
Motor Error ◽  
Stimulation Of

1. Models of the saccadic system propose that there is an integration of the pulse signal, and there is good evidence that the integrator is reset gradually (Nichols and Sparks 1994, 1995). Other studies of the superior collicular contribution to the saccadic system have proposed a sensory, not motor, nature for its signal. 2. To test experimentally the resetting of the integrator and the nature of the collicular signal, we electrically stimulated the superior colliculus during periods of fixation and during the course of visually guided saccades. Trains of stimuli which were presented during periods of fixation evoked saccades with fixed vectors. Identical stimulation at the beginning of a visually guided saccade evoked saccades whose direction was rotated and amplitude extended from the fixed vector. The direction of the rotation was opposite that of the visually guided saccade, and the magnitude of this rotation could be as large as 80 degrees. 3. Stimulation which was applied at progressively later times during the visually guided saccade, evoked saccades with progressively smaller rotations and progressively less elongations. The time period during which saccades were modified persisted beyond the end of the visually guided saccade, when the eyes were stationary. Thus, we confirm the previous findings (Nichols and Sparks 1994, 1995; Robinson, 1972), that the end of the saccade is not a period of quiescence within the oculomotor pathways. 4. Our results confirm that the resetting of the integration of the saccade signal is gradual rather than abrupt. Furthermore, these data suggest that the superior colliculus signals a motor error.

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