Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation

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.

1992 ◽  
Vol 67 (4) ◽  
pp. 1000-1002 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz

1. In the rostral pole of the monkey superior colliculus (SC) a subset of neurons (fixation cells) discharge tonically when a monkey actively fixates a target spot and pause during the execution of saccadic eye movements. 2. To test whether these fixation cells are necessary for the control of visual fixation and saccade suppression, we artificially inhibited them with a local injection of muscimol, an agonist of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). After injection of muscimol into the rostral pole of one SC, the monkey was less able to suppress the initiation of saccades. Many unwanted visually guided saccades were initiated less than 100 ms after onset of a peripheral visual stimulus and therefore fell into the range of express saccades. 3. We propose that fixation cells in the rostral SC form part of a fixation system that facilitates active visual fixation and suppresses the initiation of unwanted saccadic eye movements. Express saccades can only occur when activity in this fixation system is reduced.


1998 ◽  
Vol 79 (3) ◽  
pp. 1193-1209 ◽  
Author(s):  
Douglas P. Munoz ◽  
Peter J. Istvan

Munoz, Douglas P. and Peter J. Istvan. Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J. Neurophysiol. 79: 1193–1209, 1998. The intermediate layers of the monkey superior colliculus (SC) contain neurons the discharges of which are modulated by visual fixation and saccadic eye movements. Fixation neurons, located in the rostral pole of the SC, discharge action potentials tonically during visual fixation and pause for most saccades. Saccade neurons, located throughout the remainder of the intermediate layers of the SC, discharge action potentials for saccades to a restricted region of the visual field. We defined the fixation zone as that region of the rostral SC containing fixation neurons and the saccade zone as the remainder of the SC. It recently has been hypothesized that a network of local inhibitory interneurons may help shape the reciprocal discharge pattern of fixation and saccade neurons. To test this hypothesis, we combined extracellular recording and microstimulation techniques in awake monkeys trained to perform oculomotor paradigms that enabled us to classify collicular fixation and saccade neurons. Microstimulation was used to electrically activate the fixation and saccade zones of the ipsilateral and contralateral SC to test for inhibitory and excitatory inputs onto fixation and saccade neurons. Saccade neurons were inhibited at short latencies following electrical stimulation of either the ipsilateral (1–5 ms) or contralateral (2–7 ms) fixation or saccade zones. Fixation neurons were inhibited 1–4 ms after electrical stimulation of the ipsilateral saccade zone. Stimulation of the contralateral saccade zone led to much weaker inhibition of fixation neurons. Stimulation of the contralateral fixation zone led to short-latency (1–2 ms) excitation of fixation neurons. Only a small percentage of saccade and fixation neurons were activated by the electrical stimulation (latency: 0.5–2.0 ms). These responses were confirmed as either orthodromic or antidromic responses using collision testing. The results suggest that a local network of inhibitory interneurons may help shape not only the reciprocal discharge pattern of fixation and saccade neurons but also permit lateral interactions between all regions of the ipsilateral and contralateral SC. These interactions therefore may be critical for maintaining stable visual fixation, suppressing unwanted saccades, and initiating saccadic eye movements to targets of interest.


2016 ◽  
Vol 116 (6) ◽  
pp. 2541-2549 ◽  
Author(s):  
John R. Economides ◽  
Daniel L. Adams ◽  
Jonathan C. Horton

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.


1994 ◽  
Vol 11 (2) ◽  
pp. 229-241 ◽  
Author(s):  
Peter H. Schiller ◽  
Kyoungmin Lee

AbstractVisually guided saccadic eye movements to singly presented stationary targets form a bimodal distribution. After superior colliculus lesions, the so called “express saccades” that form the first mode of the distribution are no longer obtained. The aim of this study was to determine what role several other neural systems play in the generation of express and regular saccades, with the latter being those that form the second mode in the bimodal distribution. Lesions were made in the parvocellular and magnocellular portions of the lateral geniculate nucleus to disrupt either the midget system or the parasol system that originates in the retina and areas V4 and MT. The effects of the lesions were examined on the accuracy and latency of saccadic eye movements made to stationary and to moving visual targets. Following magnocellular and MT lesions deficits were observed in smooth pursuit and in the amplitude of saccades made to moving targets. However, none of the lesions produced significant changes in the bimodal distribution of saccadic latencies to stationary targets. The results suggest that express saccades and regular saccades are not selectively mediated by either the midget or the parasol systems or by areas V4 and MT. Neither are the frontal eye fields involved as had previously been shown. We suggest that the superior colliculus plays a central role in producing both express and regular saccades by virtue of highly convergent input from numerous cortical structures.


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.


1994 ◽  
Vol 72 (6) ◽  
pp. 2648-2664 ◽  
Author(s):  
R. J. Cowie ◽  
D. L. Robinson

1. These studies were initiated to understand the neural sites and mechanisms controlling head movements during gaze shifts. Gaze shifts are made by saccadic eye movements with and without head movements. Sites were stimulated electrically within the brain stem of awake, trained monkeys relatively free to make head movements to study the head-movement components of gaze shifts. 2. Electrical stimulation in and around the gigantocellular reticular nucleus evoked head movements in the ipsilateral direction. Gaze shifts were never evoked from these sites, presumably because the vestibulo-ocular reflex compensated. The rough topography of this region included large head movements laterally, small movements medially, downward movements from dorsal sites, and upward movements more ventrally. 3. The initial position of the head influenced the magnitude of the elicited movement with larger movements produced when the head was directed to the contralateral side. Attentive fixation was associated with larger and faster head movements when compared with those evoked during spontaneous behavior. 4. The superior colliculus makes a significant contribution to gaze shifts and has been shown to contribute to head movements. Because the colliculus is a major source of afferents to the gigantocellular reticular nucleus, comparable stimulation studies of the superior colliculus were conducted. When the colliculus was excited, shifts of gaze in the contralateral direction were predominant. These were most often accomplished by saccadic eye movements, however, we frequently elicited head movements that had an average latency 10 ms longer than those elicited from the reticular head movement region. Sites evoking head movements tended to be deeper and more caudal than loci eliciting eye movements. Neither the onset latencies, amplitudes, nor peak velocities of head movements and eye movements were correlated. Gaze shifts evoked from the caudal colliculus with the head free were larger than those elicited from the same site with the head fixed. 5. These studies demonstrate that both the superior colliculus and gigantocellular reticular nucleus mediate head movements. The colliculus plays a role in orienting to external events, and so collicular head movements predominantly were associated with gaze shifts, with the eye and head movements uncoupled. The medullary reticular system may play a role in the integration of a wider range of movements. Head movements from the medullary reticular sites probably participate in several forms of head movements, such as those that are related to postural reflexes, started volitionally, and/or oriented to external events.


2017 ◽  
Vol 117 (3) ◽  
pp. 1281-1292 ◽  
Author(s):  
Suraj Upadhyaya ◽  
Hui Meng ◽  
Vallabh E. Das

Disruption of binocular vision during the critical period for development leads to eye misalignment in humans and in monkey models. We have previously suggested that disruption within a vergence circuit could be the neural basis for strabismus. Electrical stimulation in the rostral superior colliculus (rSC) leads to vergence eye movements in normal monkeys. Therefore, the purpose of this study was to investigate the effect of SC stimulation on eye misalignment in strabismic monkeys. Electrical stimulation was delivered to 51 sites in the intermediate and deep layers of the SC (400 Hz, 0.5-s duration, 10–40 μA) in 3 adult optical prism-reared strabismic monkeys. Scleral search coils were used to measure movements of both eyes during a fixation task. Staircase saccades with horizontal and vertical components were elicited by stimulation as predicted from the SC topographic map. Electrical stimulation also resulted in significant changes in horizontal strabismus angle, i.e., a shift toward exotropia/esotropia depending on stimulation site. Electrically evoked saccade vector amplitude in the two eyes was not significantly different ( P > 0.05; paired t-test) but saccade direction differed. However, saccade disconjugacy accounted for only ~50% of the change in horizontal misalignment while disconjugate postsaccadic movements accounted for the other ~50% of the change in misalignment due to electrical stimulation. In summary, our data suggest that electrical stimulation of the SC of strabismic monkeys produces a change in horizontal eye alignment that is due to a combination of disconjugate saccadic eye movements and disconjugate postsaccadic movements. NEW & NOTEWORTHY Electrical stimulation of the superior colliculus in strabismic monkeys results in a change in eye misalignment. These data support the notion of developmental disruption of vergence circuits leading to maintenance of eye misalignment in strabismus.


1985 ◽  
Vol 53 (1) ◽  
pp. 266-291 ◽  
Author(s):  
O. Hikosaka ◽  
R. H. Wurtz

Our previous observations led to the hypothesis that cells in the substantia nigra pars reticulata (SNr) tonically inhibit saccade-related cells in the intermediate layers of the superior colliculus (SC). Before saccades to visual or remembered targets, cells in SNr briefly reduce that inhibition, allowing a burst of spikes of SC cells that, in turn, leads to the initiation of a saccadic eye movement. Since this inhibition is likely to be mediated by gamma-aminobutyric acid (GABA), we tested this hypothesis by injecting a GABA agonist (muscimol) or a GABA antagonist (bicuculline) into the superior colliculus and measured the effects on saccadic eye movements made to visual or remembered targets. An injection of muscimol selectively suppressed saccades to the movement field of the cells near the injection site. The affected area expanded over time, thus suggesting the diffusion of muscimol in the SC; the area never included the other hemifield, suggesting that the diffusion was limited to one SC. One of the monkeys became unable to make any saccades to the affected area. Saccades to visual targets following injection of muscimol had longer latency and slightly shorter amplitudes that were corrected by subsequent saccades. The most striking change was a decrease in the peak velocity of the saccade, frequently to less than half the preinjection value. Saccades to remembered targets following injection of muscimol also showed an increase in latency and decrease in velocity, but in addition, showed a striking decrease in the accuracy of the saccades. The trajectories of saccades became distorted as if they were deflected away from the affected area. After muscimol injection, the area over which spontaneous eye movements were made shifted toward the side ipsilateral to the injection. Saccades toward the contralateral side were less frequent and slower. In nystagmus, which developed later, the slow phase was toward the contralateral side. In contrast to muscimol, injection of bicuculline facilitated the initiation of saccades. Injection was followed almost immediately by stereotyped and apparently irrepressible saccades made toward the center of the movement field of the SC cells at the injection site. The monkeys became unable to fixate during the tasks; the fixation was interrupted by saccadic jerks made to the affected area of the visual field and then back to the fixation point.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


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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