The role of the superior colliculus in saccade initiation: a study of express saccades and the gap effect

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.

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Injection of Nicotine Into the Superior Colliculus Facilitates Occurrence of Express Saccades in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.1999.82.3.1642 ◽

1999 ◽

Vol 82 (3) ◽

pp. 1642-1646 ◽

Cited By ~ 47

Author(s):

Hiroshi Aizawa ◽

Yasushi Kobayashi ◽

Masaru Yamamoto ◽

Tadashi Isa

Keyword(s):

Superior Colliculus ◽

Nicotinic Acetylcholine Receptors ◽

Acetylcholine Receptors ◽

Marked Change ◽

Major Change ◽

Visually Guided ◽

Express Saccades ◽

Macaque Monkeys ◽

The Relationship

To clarify the role of cholinergic inputs to the intermediate layer of the superior colliculus (SC), we examined the effect of microinjection of nicotine into the SC on visually guided saccades in macaque monkeys. After injection of 0.4–2 μl of 1–100 mM nicotine into the SC, frequency of extremely short latency saccades (express saccades; reaction time = 70–120 ms) dramatically increased, for the saccades the direction and amplitude of which were represented at the location of the injection site on the collicular map. However, no marked change was observed for the relationship between the peak velocities and the amplitudes of saccades. These results suggested that activation of nicotinic acetylcholine receptors in the SC can facilitate initiation but causes no major change in dynamics of visually guided saccades.

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Saccadic Performance as a Function of the Presence and Disappearance of Auditory and Visual Fixation Stimuli

Journal of Cognitive Neuroscience ◽

10.1162/089892999563337 ◽

1999 ◽

Vol 11 (2) ◽

pp. 206-213 ◽

Cited By ~ 16

Author(s):

Tracy L. Taylor ◽

Raymond M. Klein ◽

Douglas P. Munoz

Keyword(s):

Superior Colliculus ◽

Human Subjects ◽

Visual Stimuli ◽

Visual Fixation ◽

Gap Effect ◽

Auditory Target ◽

Auditory Stimuli ◽

Noise Stimulus ◽

Auditory Noise

Relative to when a fixated stimulus remains visible, saccadic latencies are facilitated when a fixated stimulus is extinguished simultaneously with or prior to the appearance of an eccentric auditory, visual, or combined visual-auditory target. In a study of nine human subjects, we determined whether such facilitation (the “gap effect”) occurs equivalently for the disappearance of fixated auditory stimuli and fixated visual stimuli. In the present study, a fixated auditory (noise) stimulus remained present (overlap) or else was extinguished simultaneously with (step) or 200 msec prior to (gap) the appearance of a visual, auditory (tone), or combined visual-auditory target 10° to the left or right of fixation. The results demonstrated equivalent facilitatory effects due to the disappearance of fixated auditory and visual stimuli and are consistent with the presumed role of the superior colliculus in the gap effect.

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Control of Reflexive Saccades following Hemispherectomy

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2010.21537 ◽

2011 ◽

Vol 23 (6) ◽

pp. 1368-1378 ◽

Cited By ~ 7

Author(s):

Patricia A. Reuter-Lorenz ◽

Troy M. Herter ◽

Daniel Guitton

Keyword(s):

Superior Colliculus ◽

Inhibitory Control ◽

Intractable Epilepsy ◽

Short Latency ◽

Gap Effect ◽

Express Saccades ◽

Antisaccade Task ◽

Intact Side ◽

Reflexive Saccades ◽

Saccade Generation

Individuals who have undergone hemispherectomy for treatment of intractable epilepsy offer a rare and valuable opportunity to examine the ability of a single cortical hemisphere to control oculomotor performance. We used peripheral auditory events to trigger saccades, thereby circumventing dense postsurgical hemianopia. In an antisaccade task, patients generated numerous unintended short-latency saccades toward contralesional auditory events, indicating pronounced limitations in the ability of a single hemicortex to exert normal inhibitory control over ipsilateral (i.e., contralesional) reflexive saccade generation. Despite reflexive errors, patients retained an ability to generate correct antisaccades in both directions. The prosaccade task revealed numerous contralesional express saccades, a robust contralesional gap effect, but the absence of both effects for ipsilesional saccades. These results indicate limits to the saccadic control capabilities following hemispherectomy: A single hemicortex can mediate antisaccades in both directions, but plasticity does not extend fully to the bilateral inhibition of reflexive saccades. We posit that these effects are due to altered control dynamics that reduce the responsivity of the superior colliculus on the intact side and facilitate the release of an auditory-evoked ocular grasp reflex into the blind hemifield that the intact hemicortex has difficulty suppressing.

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Effects of Local Nicotinic Activation of the Superior Colliculus on Saccades in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.00558.2004 ◽

2005 ◽

Vol 93 (1) ◽

pp. 519-534 ◽

Cited By ~ 21

Author(s):

Masayuki Watanabe ◽

Yasushi Kobayashi ◽

Yuka Inoue ◽

Tadashi Isa

Keyword(s):

Superior Colliculus ◽

Reaction Times ◽

Low Frequency ◽

Visually Guided ◽

Population Activity ◽

Affected Area ◽

Movement Field ◽

Neural Interactions ◽

Restricted Region

To examine the role of competitive and cooperative neural interactions within the intermediate layer of superior colliculus (SC), we elevated the basal SC neuronal activity by locally injecting a cholinergic agonist nicotine and analyzed its effects on saccade performance. After microinjection, spontaneous saccades were directed toward the movement field of neurons at the injection site (affected area). For visually guided saccades, reaction times were decreased when targets were presented close to the affected area. However, when visual targets were presented remote from the affected area, reaction times were not increased regardless of the rostrocaudal level of the injection sites. The endpoints of visually guided saccades were biased toward the affected area when targets were presented close to the affected area. After this endpoint effect diminished, the trajectories of visually guided saccades remained modestly curved toward the affected area. Compared with the effects on endpoints, the effects on reaction times were more localized to the targets close to the affected area. These results are consistent with a model that saccades are triggered by the activities of neurons within a restricted region, and the endpoints and trajectories of the saccades are determined by the widespread population activity in the SC. However, because increased reaction times were not observed for saccades toward targets remote from the affected area, inhibitory interactions in the SC may not be strong enough to shape the spatial distribution of the low-frequency preparatory activities in the SC.

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GABAA and GABAC Receptors Have Contrasting Effects on Excitability in Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.1999.82.4.2020 ◽

1999 ◽

Vol 82 (4) ◽

pp. 2020-2023 ◽

Cited By ~ 35

Author(s):

Michael Pasternack ◽

Mathias Boller ◽

Belinda Pau ◽

Matthias Schmidt

Keyword(s):

Superior Colliculus ◽

Receptor Agonist ◽

Brain Slices ◽

Superficial Layer ◽

Field Potentials ◽

Competitive Antagonist ◽

Postsynaptic Potential ◽

Late Potential ◽

Receptor Agonists And Antagonists

We have recently found that GABAC receptor subunit transcripts are expressed in the superficial layers of rat superior colliculus (SC). In the present study we used immunocytochemistry to demonstrate the presence of GABAC receptors in rat SC at protein level. We also investigated in acute rat brain slices the effect of GABAA and GABAC receptor agonists and antagonists on stimulus-evoked extracellular field potentials in SC. Electrical stimulation of the SC optic layer induced a biphasic, early and late, potential in the adjacent superficial layer. The late component was completely inhibited by 6-cyano-7-nitroquinoxaline-2,3-dione or CoCl2, indicating that it was generated by postsynaptic activation. Muscimol, a potent GABAA and GABAC receptor agonist, strongly attenuated this postsynaptic potential at concentrations >10 μM. In contrast, the GABAC receptor agonist cis-aminocrotonic acid, as well as muscimol at lower concentrations (0.1–1 μM) increased the postsynaptic potential. This increase was blocked by (1,2,5,6-tetrahydropyridine-4-yl)methylphosphinic acid, a novel competitive antagonist of GABAC receptors. Our findings demonstrate the presence of functional GABAC receptors in SC and suggest a disinhibitory role of these receptors in SC neuronal circuitry.

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Amygdala Underlies the Environment Dependency of Defense Responses Induced via Superior Colliculus

Frontiers in Neural Circuits ◽

10.3389/fncir.2021.768647 ◽

2022 ◽

Vol 15 ◽

Author(s):

Kaoru Isa ◽

Kota Tokuoka ◽

Sakura Ikeda ◽

Sara Karimi ◽

Kenta Kobayashi ◽

...

Keyword(s):

Superior Colliculus ◽

Natural Environment ◽

Ibotenic Acid ◽

Defense Responses ◽

Male Mice ◽

Contextual Modulation ◽

Innate Defense ◽

Open Platform ◽

Environmental Setting

In our previous study, we showed that the defense responses induced by the selective optogenetic activation of the uncrossed output pathway from the deeper layer of the superior colliculus were environment dependent in the mouse. In a small closed box, the stimulus frequently induced flight (fast forward run away) responses, while in a large open field, the stimulus tended to induce backward retreat responses. We tested a hypothesis that the amygdala is involved in such environment dependency of the innate defense responses. For this purpose, we made a bilateral lesion of the amygdala induced by the ibotenic acid injections in male mice. As a result, in the mice with lesions of substantial portions of the basolateral and basomedial complex, the flight responses in the closed box disappeared and retreat responses were mainly induced. The retreat responses on the open platform were unchanged. Classically, the amygdala has been considered to be involved in the memory-dependent contextual modulation of the fear responses. In contrast, the present results suggest a novel view on the role of the amygdala in which the amygdala plays a key role in sensing the current environmental setting for making a quick decision of action upon emergency, which is critical for survival in the natural environment.

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The role of fixation disengagement in the parallel programming of sequences of saccades

Experimental Brain Research ◽

10.1007/s00221-019-05641-9 ◽

2019 ◽

Vol 237 (11) ◽

pp. 3033-3045

Author(s):

Eugene McSorley ◽

Iain D. Gilchrist ◽

Rachel McCloy

Keyword(s):

Eye Movements ◽

Parallel Programming ◽

Response Times ◽

Saccadic Eye Movements ◽

Gap Effect ◽

Task Completion ◽

Published Data ◽

Trial Duration ◽

Visual Tasks

Abstract One of the core mechanisms involved in the control of saccade responses to selected target stimuli is the disengagement from the current fixation location, so that the next saccade can be executed. To carry out everyday visual tasks, we make multiple eye movements that can be programmed in parallel. However, the role of disengagement in the parallel programming of saccades has not been examined. It is well established that the need for disengagement slows down saccadic response time. This may be important in allowing the system to program accurate eye movements and have a role to play in the control of multiple eye movements but as yet this remains untested. Here, we report two experiments that seek to examine whether fixation disengagement reduces saccade latencies when the task completion demands multiple saccade responses. A saccade contingent paradigm was employed and participants were asked to execute saccadic eye movements to a series of seven targets while manipulating when these targets were shown. This both promotes fixation disengagement and controls the extent that parallel programming can occur. We found that trial duration decreased as more targets were made available prior to fixation: this was a result both of a reduction in the number of saccades being executed and in their saccade latencies. This supports the view that even when fixation disengagement is not required, parallel programming of multiple sequential saccadic eye movements is still present. By comparison with previous published data, we demonstrate a substantial speeded of response times in these condition (“a gap effect”) and that parallel programming is attenuated in these conditions.

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The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey

Journal of Neurophysiology ◽

10.1152/jn.1987.57.4.1033 ◽

1987 ◽

Vol 57 (4) ◽

pp. 1033-1049 ◽

Cited By ~ 318

Author(s):

P. H. Schiller ◽

J. H. Sandell ◽

J. H. Maunsell

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Short Latency ◽

The Other ◽

Frontal Eye Field ◽

Express Saccades ◽

Unimodal Distribution ◽

Other Hand ◽

Eye Field ◽

The Mean

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)

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