Distractor Evoked Deviations of Saccade Trajectory Are Modulated by Fixation Activity in the Superior Colliculus: Computational and Behavioral Evidence

Previous studies have shown that saccades may deviate towards or away from task irrelevant visual distractors. This observation has been attributed to active suppression (inhibition) of the distractor location unfolding over time: early in time inhibition at the distractor location is incomplete causing deviation towards the distractor, while later in time when inhibition is complete the eyes deviate away from the distractor. In a recent computational study, Wang, Kruijne and Theeuwes proposed an alternative theory that the lateral interactions in the superior colliculus (SC), which are characterized by short-distance excitation and long-distance inhibition, are sufficient for generating both deviations towards and away from distractors. In the present study, we performed a meta-analysis of the literature, ran model simulations and conducted two behavioral experiments to further explore this unconventional theory. Confirming predictions generated by the model simulations, the behavioral experiments show that a) saccades deviate towards close distractors and away from remote distractors, and b) the amount of deviation depends on the strength of fixation activity in the SC, which can be manipulated by turning off the fixation stimulus before or after target onset (Experiment 1), or by varying the eccentricity of the target and distractor (Experiment 2).     

A Role for the Superior Colliculus in Decision Criteria

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Three-Dimensional Representation of Motor Space in the Mouse Superior Colliculus

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Retrograde Labeling of Retinal Ganglion Cells by Application of Fluoro-Gold on the Surface of Superior Colliculus

Retinal ganglion cell (RGC) counting is essential to evaluate retinal degeneration especially in glaucoma. Reliable RGC labeling is fundamental for evaluating the effects of any treatment. In rat, about 98% of RGCs is known to project to the contralateral superior colliculus (SC) (Forrester and Peters, 1967). Applying fluoro-gold (FG) on the surface of SC can label almost all the RGCs, so that we can focus on this most vulnerable retinal neuron in glaucoma. FG is taken up by the axon terminals of retinal ganglion cells and bilaterally transported retrogradely to its somas in the retina. Compare with retrograde labeling of RGC by putting FG at stump of transected optic nerve for 2 days, the interference of RGC survival is minimized. Compare with cresyl violet staining that stains RGCs, amacrine cells and endothelium of the blood vessel in the retinal ganglion cell layer, this labeling method is more specific to the RGC. This video describes the method of retrograde labeling of RGC by applying FG on the surface of SC. The surgical procedures include drilling the skull; aspirating the cortex to expose the SC and applying gelatin sponge over entire dorsal surface of SC are shown. Useful tips for avoiding massive intracranial bleeding and aspiration of the SC have been given.Download video file.^{(140M, mpg)}     

A Retinal Ganglion Cell Neurotrophic Factor Purified from the Superior Colliculus

Dissociated neonatal rat retinal ganglion cells can be maintained by the addition of an extract from the neonatal superior colliculus. This extract can support 95% of ganglion cells over 24 h in culture; in addition it promotes the expression of neurites from these cells. This report describes the purification of a neurotrophic factor from the superior colliculus which supports the survival of 80% of retinal ganglion cells over 24 h in vitro. The purification procedure involves a combination of dye-ligand, anion-exchange, and molecular sieve chromatography. The purified neurotrophic factor has a Stokes radius of approximately 200 A using molecular sieve chromatography in the presence of a chaotropic agent. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis of the purified factor indicates that it is a glycoprotein that migrates with a molecular mass greater than 400 kDa. Further characterization of this high-molecular-mass glycoprotein by enzymatic digestion demonstrated that it is a chondroitin sulfate proteoglycan. This factor is clearly distinguishable from other neurotrophic factors that have an effect on retinal ganglion cells such as brain-derived neurotrophic factor and fibroblast growth factor. The chondroitin sulfate proteoglycan from the neonatal superior colliculus is the first proteoglycan to be identified as a neurotrophic factor.     

Genetically Defined Functional Modules for Spatial Orienting in the Mouse Superior Colliculus

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Audiogenic Epilepsy and Structural Features of Superior Colliculus in KM Rats

Using immunoblotting, we showed that in rats of audiogenic epilepsy (AE) prone strain (Krushinsky- Molodkina, KM) the superior colliculus tissue (SC) contains significantly less quantity of glial neurotrophic factor (GDNF), beta-tubulin and actin in comparison to the same brain region in “0” rats, nonprone to AE. This fact led to the suggestion that the histological structure of the SC in KM rats could differ significantly from that of the “0” strain. Using neuromorphologу technique, we demonstrated that the total number of SC cells, as well as the number of neurons were significantly less in KM rats than in the “0” strain rats. Particularly strong differences were found in the deep layers of SC, the area of terminals from IC. Further studies of the midbrain structures, will help to identify the novel aspects of neural networks, involved in the genesis of AE in rats of KM strain.     

Perisaccadic Remapping and Rescaling of Visual Responses in Macaque Superior Colliculus

Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.     

The Mechanism of Saccade Motor Pattern Generation Investigated by a Large-Scale Spiking Neuron Model of the Superior Colliculus

The subcortical saccade-generating system consists of the retina, superior colliculus, cerebellum and brainstem motoneuron areas. The superior colliculus is the site of sensory-motor convergence within this basic visuomotor loop preserved throughout the vertebrates. While the system has been extensively studied, there are still several outstanding questions regarding how and where the saccade eye movement profile is generated and the contribution of respective parts within this system. Here we construct a spiking neuron model of the whole intermediate layer of the superior colliculus based on the latest anatomy and physiology data. The model consists of conductance-based spiking neurons with quasi-visual, burst, buildup, local inhibitory, and deep layer inhibitory neurons. The visual input is given from the superficial superior colliculus and the burst neurons send the output to the brainstem oculomotor nuclei. Gating input from the basal ganglia and an integral feedback from the reticular formation are also included.We implement the model in the NEST simulator and show that the activity profile of bursting neurons can be reproduced by a combination of NMDA-type and cholinergic excitatory synaptic inputs and integrative inhibitory feedback. The model shows that the spreading neural activity observed in vivo can keep track of the collicular output over time and reset the system at the end of a saccade through activation of deep layer inhibitory neurons. We identify the model parameters according to neural recording data and show that the resulting model recreates the saccade size-velocity curves known as the saccadic main sequence in behavioral studies. The present model is consistent with theories that the superior colliculus takes a principal role in generating the temporal profiles of saccadic eye movements, rather than just specifying the end points of eye movements.     

High-Field fMRI Reveals Brain Activation Patterns Underlying Saccade Execution in the Human Superior Colliculus

Background

The superior colliculus (SC) has been shown to play a crucial role in the initiation and coordination of eye- and head-movements. The knowledge about the function of this structure is mainly based on single-unit recordings in animals with relatively few neuroimaging studies investigating eye-movement related brain activity in humans.

Methodology/Principal Findings

The present study employed high-field (7 Tesla) functional magnetic resonance imaging (fMRI) to investigate SC responses during endogenously cued saccades in humans. In response to centrally presented instructional cues, subjects either performed saccades away from (centrifugal) or towards (centripetal) the center of straight gaze or maintained fixation at the center position. Compared to central fixation, the execution of saccades elicited hemodynamic activity within a network of cortical and subcortical areas that included the SC, lateral geniculate nucleus (LGN), occipital cortex, striatum, and the pulvinar.

Conclusions/Significance

Activity in the SC was enhanced contralateral to the direction of the saccade (i.e., greater activity in the right as compared to left SC during leftward saccades and vice versa) during both centrifugal and centripetal saccades, thereby demonstrating that the contralateral predominance for saccade execution that has been shown to exist in animals is also present in the human SC. In addition, centrifugal saccades elicited greater activity in the SC than did centripetal saccades, while also being accompanied by an enhanced deactivation within the prefrontal default-mode network. This pattern of brain activity might reflect the reduced processing effort required to move the eyes toward as compared to away from the center of straight gaze, a position that might serve as a spatial baseline in which the retinotopic and craniotopic reference frames are aligned.     

Superior Colliculus GABAergic Neurons Are Essential for Acute Dark Induction of Wakefulness in Mice

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Defined Cell Types in Superior Colliculus Make Distinct Contributions to Prey Capture Behavior in the Mouse

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Element Distribution in Visual System,the Optic Chiasma,Lateral Geniculate Body,and Superior Colliculus

To elucidate compositional changes of the visual system with aging, the authors investigated age-related changes of elements in the optic chiasma, lateral geniculate body, and superior colliculus, relationships among their elements, relationships among their brain regions from a viewpoint of elements, and gender differences in their elements by direct chemical analysis. After ordinary dissection at Nara Medical University was finished, the optic chiasmas, lateral geniculate bodies, and superior colliculi were resected from identical cerebra of the subjects. The subjects consisted of 14 men and 10 women, ranging in age from 75 to 96 years (average age = 85.6 ± 5.9 years). After ashing with nitric acid and perchloric acid, element contents were determined by inductively coupled plasma-atomic emission spectrometry. As the result, the average content of P was significantly higher in the optic chiasma and superior colliculus compared with the lateral geniculate body. Regarding age-related changes of elements, no significant changes with aging were found in seven elements of the optic chiasma, lateral geniculate body, and superior colliculus in the subjects more than 75 years of age. The findings that with regard to the relationships among elements, there were extremely significant direct correlations between Ca and Zn contents and significant inverse correlations between Mg and Na contents were obtained in common in all of the optic chiasma, lateral geniculate body, and superior colliculus. It was examined whether there were significant correlations among the optic chiasma, lateral geniculate body, and superior colliculus in the seven elements and the following results were obtained: There were significant direct correlations between the optic chiasma and lateral geniculate body in both the P and Mg contents; there was a significant direct correlation between the optic chiasma and superior colliculus in the Fe content; and a significant direct correlation was found between the lateral geniculate body and superior colliculus in the Mg content. Regarding the gender differences in elements, it was found that both the Ca and Zn contents of the lateral geniculate body were significantly higher in women than in men.     

Contribution of GABAA receptor-mediated inhibition to the determination of the velocity tuning of low pass-tuned neurons of the Superior Colliculus

The participation of intrinsic inhibitory networks in providing the velocity selectivity of neurons of the superior colliculus (SC) of the Syrian hamster was tested using iontophoretic application of bicuculline methiodide, a GABA_A receptor competitive antagonist. The impulse activity of 22 low pass-tuned (LP) cells was recorded extracellularly. Following application of bicuculline, 10 cells exhibited an increase in the velocity selectivity, while the other 12 units showed decreases in their tuning. We assume that SC intrinsic inhibitory networks contributing to the velocity tuning of neurons of this structure are driven in a dissimilar way by afferent volleys arriving from the retina through “fast” Y and “slow” W channels. Neirofiziologiya/Neurophysiology, Vol. 39, Nos. 4/5, pp. 385–387, July–October, 2007.     

The Distinct Role of the Amygdala,Superior Colliculus and Pulvinar in Processing of Central and Peripheral Snakes

Introduction

Visual processing of ecologically relevant stimuli involves a central bias for stimuli demanding detailed processing (e.g., faces), whereas peripheral object processing is based on coarse identification. Fast detection of animal shapes holding a significant phylogenetic value, such as snakes, may benefit from peripheral vision. The amygdala together with the pulvinar and the superior colliculus are implicated in an ongoing debate regarding their role in automatic and deliberate spatial processing of threat signals.

Methods

Here we tested twenty healthy participants in an fMRI task, and investigated the role of spatial demands (the main effect of central vs. peripheral vision) in the processing of fear-relevant ecological features. We controlled for stimulus dependence using true or false snakes; snake shapes or snake faces and for task constraints (implicit or explicit). The main idea justifying this double task is that amygdala and superior colliculus are involved in both automatic and controlled processes. Moreover the explicit/implicit instruction in the task with respect to emotion is not necessarily equivalent to explicit vs. implicit in the sense of endogenous vs. exogenous attention, or controlled vs. automatic processes.

Results

We found that stimulus-driven processing led to increased amygdala responses specifically to true snake shapes presented in the centre or in the peripheral left hemifield (right hemisphere). Importantly, the superior colliculus showed significantly biased and explicit central responses to snake-related stimuli. Moreover, the pulvinar, which also contains foveal representations, also showed strong central responses, extending the results of a recent single cell pulvinar study in monkeys. Similar hemispheric specialization was found across structures: increased amygdala responses occurred to true snake shapes presented to the right hemisphere, with this pattern being closely followed by the superior colliculus and the pulvinar.

Conclusion

These results show that subcortical structures containing foveal representations such as the amygdala, pulvinar and superior colliculus play distinct roles in the central and peripheral processing of snake shapes. Our findings suggest multiple phylogenetic fingerprints in the responses of subcortical structures to fear-relevant stimuli.