Layers Of Colliculus Research Articles

Sensory tuning in neuronal movement commands

Movement control is critical for successful interaction with our environment. However, movement does not occur in complete isolation of sensation, and this is particularly true of eye movements. Here, we show that the neuronal eye movement commands emitted by the superior colliculus (SC), a structure classically associated with oculomotor control, encompass a robust visual sensory representation of eye movement targets. Thus, similar saccades toward different images are associated with different saccade-related "motor" bursts. Such sensory tuning in SC saccade motor commands appeared for all image manipulations that we tested, from simple visual features to real-life object images, and it was also strongest in the most motor neurons in the deeper collicular layers. Visual-feature discrimination performance in the motor commands was also stronger than in visual responses. Comparing SC motor command feature discrimination performance to that in the primary visual cortex during steady-state gaze fixation revealed that collicular motor bursts possess a reliable perisaccadic sensory representation of the peripheral saccade target's visual appearance, exactly when retinal input is expected to be most uncertain. Our results demonstrate that SC neuronal movement commands likely serve a fundamentally sensory function.

Somatosensory Crossmodal Plasticity in Superior Colliculus of Visually Deafferented Rats

Terminal fields of a certain pathway result denervated if the regeneration after the lesion of the pathway fails. If the lesion happened in a young animal, terminal fields of other nervous pathways that are spatially coincident or are close to the denervated field, growth of axon collaterals or reactive synaptogenesis could take place and reinervate deafferented neurons. In that way these denervated neurons can be recruited for functional compensatory responses and can convey information to areas that result enriched with additional inputs to be processed. The present paper reviews the plastic reactions that take place in the superior colliculus, a mesencephalic layered structure, after the neonatal suppression of its visual afferents that terminate in its superficial layers. The postlesional reactive ascending growth of somatosensory afferents that in control animals innervate intermediate and deep collicular layers invade the superficial layers and connect with visually deafferented cells that result recruited for descendent collicular responses and to send sensory information to the visual cortex via the colliculo-geniculate payhway. In that way in neonatally deafferented animals, somatosensory information gains additional territory to be processed. Two somatosensory connections to the superior collicuus will be discussed in this review. One ascending from the cuneitorm nucleus and the other descending that originates in the barrel cortex.

The sifting of visual information in the superior colliculus.

Much of the early visual system is devoted to sifting the visual scene for the few bits of behaviorally relevant information. In the visual cortex of mammals, a hierarchical system of brain areas leads eventually to the selective encoding of important features, like faces and objects. Here, we report that a similar process occurs in the other major visual pathway, the superior colliculus. We investigate the visual response properties of collicular neurons in the awake mouse with large-scale electrophysiology. Compared to the superficial collicular layers, neuronal responses in the deeper layers become more selective for behaviorally relevant stimuli; more invariant to location of stimuli in the visual field; and more suppressed by repeated occurrence of a stimulus in the same location. The memory of familiar stimuli persists in complete absence of the visual cortex. Models of these neural computations lead to specific predictions for neural circuitry in the superior colliculus.

Congruent representation of visual and acoustic space in the superior colliculus of the echolocating bat Phyllostomus discolor.

The midbrain superior colliculus (SC) commonly features a retinotopic representation of visual space in its superficial layers, which is congruent with maps formed by multisensory neurons and motor neurons in its deep layers. Information flow between layers is suggested to enable the SC to mediate goal-directed orienting movements. While most mammals strongly rely on vision for orienting, some species such as echolocating bats have developed alternative strategies, which raises the question how sensory maps are organized in these animals. We probed the visual system of the echolocating bat Phyllostomus discolor and found that binocular high acuity vision is frontally oriented and thus aligned with the biosonar system, whereas monocular visual fields cover a large area of peripheral space. For the first time in echolocating bats, we could show that in contrast with other mammals, visual processing is restricted to the superficial layers of the SC. The topographic representation of visual space, however, followed the general mammalian pattern. In addition, we found a clear topographic representation of sound azimuth in the deeper collicular layers, which was congruent with the superficial visual space map and with a previously documented map of orienting movements. Especially for bats navigating at high speed in densely structured environments, it is vitally important to transfer and coordinate spatial information between sensors and motor systems. Here, we demonstrate first evidence for the existence of congruent maps of sensory space in the bat SC that might serve to generate a unified representation of the environment to guide motor actions.

Optogenetic investigation of behavioral responses mediated by the mouse superior colliculus

Event Abstract Back to Event Optogenetic investigation of behavioral responses mediated by the mouse superior colliculus Emiel Geeraerts1*, Eline Dekeyster1, Chris Van Den Haute1, Claudia Mebis1, Lies De Groef1, Veerle Baekelandt1 and Lieve Moons1 1 KU Leuven, Belgium The superior colliculus (SC) is a midbrain structure involved in behavioral responses to external stimuli, such as escaping predators and pursuing objects of interest. Unilateral electrical stimulation of the SC has been shown to elicit contralateral (pursuing) and ipsilateral (escaping) movements. To further investigate the response properties of these circuits, we revisited these experiments using an optogenetic approach. We used the SSFO (ChR2 C128S/D156A), so a short light pulse results in prolonged (30 minutes) depolarization of opsin-expressing cells. After injecting AAV2/1-CMV-SSFOmCherry in the right SC of C57Bl6J mice, SSFO was efficiently incorporated in neurons of all collicular layers. In response to a 2-second blue light stimulus, mice showed a repeatable and strong behavioral change. At first, they ran around in their cage for 20 seconds as if escaping from a non-existing threat. After quieting down, mice displayed characteristic movements consisting of large counterclockwise body turns over 180-360 degrees. As time progressed, turning movements became shorter and less frequent, but preference for counterclockwise motion lasted up to 30 minutes after blue light stimulation. In summary, we described that prolonged SSFO-mediated activation of the SC elicits escape- and pursuit-like movements for the duration of the SSFO ‘open state’ conformation. Thus we demonstrated the potential of optogenetics to activate the natural functions of the SC neuronal circuits for a period of time corresponding to the opsin channel kinetics. Future experiments will investigate the effect of SC layer- and cell type-specific stimulation to further elucidate the way orienting behavior is governed. Keywords: Mouse, superior colliculus, optogenetics, visually guided navigation, Behavior, Animal, Optogenetic stimulation Conference: 11th National Congress of the Belgian Society for Neuroscience, Mons, Belgium, 22 May - 22 May, 2015. Presentation Type: Poster presentation Topic: Neuroscience Citation: Geeraerts E, Dekeyster E, Van Den Haute C, Mebis C, De Groef L, Baekelandt V and Moons L (2015). Optogenetic investigation of behavioral responses mediated by the mouse superior colliculus. Front. Neurosci. Conference Abstract: 11th National Congress of the Belgian Society for Neuroscience. doi: 10.3389/conf.fnins.2015.89.00057 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 29 Apr 2015; Published Online: 05 May 2015. * Correspondence: Mr. Emiel Geeraerts, KU Leuven, Leuven, Belgium, Emiel.Geeraerts@bio.kuleuven.be Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Emiel Geeraerts Eline Dekeyster Chris Van Den Haute Claudia Mebis Lies De Groef Veerle Baekelandt Lieve Moons Google Emiel Geeraerts Eline Dekeyster Chris Van Den Haute Claudia Mebis Lies De Groef Veerle Baekelandt Lieve Moons Google Scholar Emiel Geeraerts Eline Dekeyster Chris Van Den Haute Claudia Mebis Lies De Groef Veerle Baekelandt Lieve Moons PubMed Emiel Geeraerts Eline Dekeyster Chris Van Den Haute Claudia Mebis Lies De Groef Veerle Baekelandt Lieve Moons Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

A spiking model of superior colliculus for bottom-up saliency

Active exploration of visual space is controlled by a saccadic system using a combination of bottom-up and top-down signals. Rate based models [1] and simple V1 models (e.g. [2]), have been proposed to explain bottom-up or attentional mechanisms. We present a biologically detailed spiking model of superior colliculus to generate saccadic eye movements using a competitive mechanism based on spike arrival times. Various pop-out tasks based on color, orientation features and motion is used to analyze the reaction time of the model. The superior colliculus is modeled as a two layer network with feature-specific superficial layers driving a common deep layer. The superficial layers of the superior colliculus are topologically organized and is driven by retinal parasols cells, V1 layer 2/3 orientation-selective cells, V1 layer 2/3 color-selective cells, and MT cells. These enable luminance, orientation, color and motion based popout respectively. In this model, the earliest spikes are considered the most salient. A saccade is triggered when there is a consistent winner in the superficial layers at the same spatial region over an extended period of time, 40 ms to 100 ms. The superficial layers implement a temporal winner-take-all mechanism; specifically, there exists a separate inhibitory subnetwork that allows each superficial layer to choose a winner. The deep layer integrates these winners over time and selects a single spatial region. It implements a bump attractor network mediated by short-range excitation (AMPA and NMDA) and long range inhibition, which generates a bump of activity before and during a saccade. An interesting property of bump attractor network based circuit is that a single cell response is independent of size of the stimulus. Similar spiking response was also observed in most of the visually selective superior colliculus cells in monkeys [3]. Additionally, this model captures known behavioral and neurophysiological properties of the superior colliculus such as saccadic suppression, activity buildup before saccade generation, and GABAb mediated inhibition from the deep layer to superficial layers resulting in selective inhibition in recently attended region. All the connections in the SC model are pre-wired to satisfy the response characteristics of superficial and deep layers. The reaction time of the model was tested on simple and conjunctive pop-out tasks. We observe only a mild shift in reaction time based on the number of distractors. Higher reaction time was observed as the complexity of the search task was increased. Also, reaction time increases based on the level of visual hierarchy that is connected to the superior colliculus layers.

Model approach to neurological variants of visuo-spatial neglect

Neglect is a neurological disorder of spatial attention with reduced awareness of visual stimuli in the hemifield contralateral to an acute temporo-parietal lesion mainly of the right hemisphere. There is a close association of multisensory orientation centers (MSO) and vestibular tonus imbalance. A lesion of the dominant right MSO causes a left-sided neglect due to a lack of ipsilateral activation of the visual cortex, which is further enhanced by increasing inhibition from the contralateral visual cortex. The nondominant MSO in the left hemisphere might be involved in the manifestation of the less frequent and more transient right-sided neglect and in the plastic mechanisms of gradual recovery from left-sided neglect or extinction. There is evidence that a vestibular tonus inbalance due to peripheral or central vestibular pathway lesions may also induce a neglect. In a first model approach using an attractor network and assuming that there is only one MSO in the right hemisphere, it is possible to simulate attentional shifts into a visual hemifield and to induce a neglect. The neural network model consists of four layers of neurons: retina, MSO, visual cortex V1, and superior colliculus. The superior colliculus layer is modeled as a recurrent attractor network with one inhibitory interneuron and synaptic weights chosen to implement a winner-take-all network that centers the hill of activity on the strongest input. We are well aware of the simplifications used in the conceptual drawings and the computational model, but nevertheless hope that they will serve as an inspiration for further modeling and clinical studies.

Bilateral and ipsilateral ascending tectopulvinar pathways in mammals: A study in the squirrel (spermophilus beecheyi)

The mammalian pulvinar complex is a collection of dorsal thalamic nuclei related to several visual and integrative processes. Previous studies have shown that the superficial layers of the superior colliculus project to multiple divisions of the pulvinar complex. Although most of these works agree about the existence of an ipsilateral tectopulvinar projection arising from the stratum griseum superficialis, some others report a bilateral projection originating from this same tectal layer. We investigated the organization of the tectopulvinar projections in the Californian ground squirrel using cholera toxin B (CTb). We confirmed previous studies showing that the caudal pulvinar of the squirrel receives a massive bilateral projection originating from a specific cell population located in the superficial collicular layers (SGS3, also called the "lower SGS" or "SGSL"). We found that this projection shares striking structural similarities with the tectorotundal pathway of birds and reptiles. Morphology of the collicular cells originating this projection closely corresponds to that of the bottlebrush tectal cells described previously for chickens and squirrels. In addition, we found that the rostral pulvinar receives an exclusively ipsilateral projection from a spatially separate population of collicular cells located at the base of the stratum opticum, deeper than the cells projecting to the caudal pulvinar. These results strongly support, at a structural level, the homology of the pathway originating in the SGS3 collicular cells upon the caudal pulvinar with the tectorotundal pathway of nonmammalian amniotes and contribute to clarifying the general organization of the tectopulvinar pathways in mammals.

Saccade, search and orient – the neural control of saccadic eye movements

One of the most important functions of the brain is to guide our behavior through an ever-changing environment as our goals and desires fluctuate. One simple, yet elegant system for investigating how sensory information and goal-related information combine to control and coordinate efficient behavior is the guidance of saccadic eye movements. The brain relies heavily on visual input to guide and coordinate our complex actions, but it is impossible for our brain to simultaneously process every aspect of visual information present in real world scenes at any given moment. Instead, the retina has evolved a highly specialized fovea in the center where we have the highest visual acuity. Therefore, to analyze a visual scene optimally, the eyes reorient in complex sequences so that the high acuity fovea of the retina can be directed to specific objects of interest. These saccadic eye movements are interspersed with periods of active fixation during which the visual system performs a detailed analysis of an object that may pertain to our current goals. Alternating between the serial process of making saccades and the analytical process of active fixation is repeated several hundred thousand times per day and is critical for numerous behaviors like reading this issue of EJN, driving an automobile or negotiating a busy sidewalk. In the laboratory, saccadic behavior can be measured easily and accurately. Quantitative analysis of saccade behavior can also serve as an important tool to investigate brain disorders in a host of neurological and psychiatric disorders (Leigh & Zee, 2006). Over the past few decades, there has been a tremendous increase in our knowledge of the systems that contribute to the control of saccadic eye movements. There have been many recent and exciting advances. Anatomical, physiological, clinical and imaging studies have contributed to our extensive knowledge of the saccade control circuit (Fig. 1), which includes regions of the occipital, parietal and frontal cortex, basal ganglia, thalamus, superior colliculus, cerebellum, and brainstem reticular formation. Within each of these brain regions are multiple populations of neurons and subnuclei that perform critical operations to coordinate behavior. In addition to overt eye movements that explicitly orient the visual system, visual selection may also be directed covertly to different locations or objects without any movement of the eyes. For example, we have the ability to shift attention away from where we look without initiating a saccade. Both overt (move the eyes) and covert (only shift attention) orienting can be directed voluntarily to a specific location or object, or involuntarily ‘captured’ by an abrupt change in the visual environment (Posner, 1980; Theeuwes, 1991; Fecteau & Munoz, 2006). There is significant overlap in the brain areas that participate in overt and covert orienting, which include several components of the frontoparietal network and the superior colliculus. This special issue of EJN contains reviews and original articles by some of the leading experts in the fields of saccades and visual search. There have been many recent exciting advances in these fields that are captured in the contributions in this issue. The contributions focus on different brain areas but the content ranges from the sensory input to the motor output and everything in between (Fig. 1). There are several different state-of-the-art technologies employed including quantitative behavioral analysis, neurophysiology, neuroimaging, clinical investigation, transcranial magnetic stimulation and modeling.

Somatosensory cross-modal plasticity in the superior colliculus of visually deafferented rats

The effects of neonatal visual deafferentation on the final adult pattern of cortico-collicular connections from the rat primary somatosensory cortex barrel field were studied by injecting an anterograde tracer (BDA) into different locations of the barrel cortex. Collicular afferents originating in the barrel cortex normally end in the intermediate collicular strata (SGI and SAI). However, neonatal visual deafferentation caused an invasion of abundant somatosensory cortical afferents into the lateral portions of the superficial collicular strata (SGS and SO). Moreover, anterograde-labelled fibers in the intermediate strata were more densely packed in visually deafferented animals. In order to study the activity of the altered somatosensory cortico-collicular connection, the effects of two different types of whisker stimuli on c-fos expression in the SC were analyzed (apomorphine treatment and enriched environment exploration). In stimulated control animals, c-fos expression was clearly evident in neurons of the intermediate layers 2 h after whisker stimulation. Similar stimulation in adult animals that underwent neonatal visual deafferentation triggered higher levels of c-fos expression in the superficial collicular layers that were invaded by cortico-collicular axonal branches. In exploration experiments, increased levels of c-fos expression were also detected in lateral parts of the intermediate layers of visually deafferented animals. These results suggest that the ascending fibers of somatosensory cortical origin can recruit deafferented superficial collicular neurons that enabling them to participate in extravisual behavioural responses mediated by collicular circuits.

Injury to retinal ganglion cell axons increases polysialylated neural cell adhesion molecule (PSA-NCAM) in the adult rodent superior colliculus

The adult mammalian central nervous system (CNS) exhibits a limited regenerative response to injury. It is well established that polysialylated neural cell adhesion molecule (PSA-NCAM) contributes to nervous system plasticity. In the visual system, PSA-NCAM participates in retinal ganglion cell (RGC) axon growth during development and specifically influences RGC innervation of its principle target tissue, the superior colliculus (SC). The goals of this study were to determine whether PSA-NCAM is expressed in the normal adult mouse SC and to evaluate PSA-NCAM expression following RGC injury. In the normal rostral, but not caudal, SC we find that PSA-NCAM is present in the retinorecipient layers; however, PSA-NCAM and RGC axons do not co-localize. In the deeper collicular layers, PSA-NCAM is observed as several distinct patches that occur at the same depth along the medial–lateral axis throughout the colliculus. RGC axotomy denervates predominantly the contralateral colliculus, where increased PSA-NCAM levels are seen at 7 and 10 days after the injury. Further evaluation of the retinorecipient layers of the partially denervated SC reveals that some intact CTB-traced RGC axons (less than 5%) labeled from the ipsilateral eye do co-localize with PSA-NCAM. This study is the first characterization of PSA-NCAM expression in the normal and partially denervated adult SC and may indicate that PSA-NCAM is involved in attempted visual system remodeling after injury.

Aberrant retinal projections in congenitally deaf mice: How are phenotypic characteristics specified in development and evolution?

The contribution of sensory input to the formation of sensory system-specific (sensoritopic) connections of the thalamus and midbrain was investigated using mice lacking the Na+-K+-2Cl- cotransporter (NKCC1) or the plasma membrane Ca2+-ATPase isoform2 (PMCA2). Because these mice are congenitally deaf, the developing nervous system has no exposure to sensory-driven neural activity from the auditory system. Here we compared the retinofugal pathway in normal and congenitally deaf mice using intraocular injections of neuroanatomical tracers into each eye, and relating tracer patterns to identified thalamic nuclei and superior colliculus layers. We demonstrate that loss of such activity results in aberrant projections of the retina into nonvisual auditory structures such as the medial geniculate nucleus and the intermediate layers of the superior colliculus. These findings indicate that activity from peripheral sensory receptor arrays is necessary not only for the refinement of developing connections within a unimodal structure, but for the establishment of sensoritopic or sensory-specific connections of unimodal and multimodal structures. We hypothesize that specification of such connections may occur through the modulation of spatial expression patterns of molecules known to be involved in the development of topography of connections between brain structures, such as the ephrins, via activity-dependent, CRE-mediated gene expression.

Development of the human superior colliculus and the retinocollicular projection

We have used carbocyanine dye tracing from the brachium of the superior colliculus in conjunction with Nissl staining and immunohistochemistry to GAP-43 and calretinin to study the development of retinal projections to the superior colliculus in 17 human embryos and fetuses aged from 8 to 28 weeks. Lamination of the superior colliculus begins to emerge by 11 weeks, and by 16 weeks all seven layers of the mature superior colliculus are visible. Fibres immunoreactive to GAP-43 were seen at 13 weeks in the most superficial layers. By 19 weeks, GAP-43 immunoreactivity was present in the stratum opticum as well as the deeper fibres layers, indicating the development of fibre pathways following those laminae. Carbocyanine dye tracing of retinocollicular projections showed extensive rostrocaudally running unbranched fibres in the superficial superior colliculus at 12 weeks. Shortly after this (13 weeks), retinocollicular fibres penetrate the deeper collicular layers and branching becomes apparent. We also saw occasional retrogradely labelled somata following DiI insertion into the superior brachium. Our findings indicate that development of the human superior colliculus and its connections is largely complete by 20 weeks. This would suggest that functional capacity of the human superior colliculus should also be mature by the middle of gestation.

Organization of electrically and chemically evoked defensive behaviors within the deeper collicular layers as compared to the periaqueductal gray matter of the rat

Stimulation of the periaqueductal gray matter (PAG) and the deeper layers of superior colliculus (SC) produces both freezing (tense immobility) and flight (trotting, galloping and jumping) behaviors along with exophthalmus (fully opened bulging eyes) and, less often, micturition and defecation. The topography of these behaviors within the distinct layers of SC remains unclear. Therefore, this study compared the defensive repertoire of intermediate (ILSC) and deep (DLSC) layers of SC to those of dorsolateral periaqueductal gray matter (DLPAG) and lateral periaqueductal gray matter (LPAG) [Neuroscience 125 (2004) 71]. Electrical stimulation was carried out through intensity- (0–70μA) and frequency-varying (0–130Hz) pulses. Chemical stimulation employed a slow microinfusion of N-methyl- d-aspartic acid (NMDA, 0–2.3nmol, 0.5nmol/min). Probability curves of intensity-, frequency- and NMDA-evoked behaviors, as well as the unbiased estimates of median stimuli, were obtained by threshold logistic analysis. Compared with the PAG, the most important differences were the lack of frequency-evoked jumping in both layers of SC and the lack of NMDA-evoked galloping in the ILSC. Moreover, although galloping and jumping were also elicited by NMDA stimulation of DLSC, effective doses were about three times higher than those of DLPAG, suggesting the spreading of the injectate to the latter structure. In contrast, exophthalmus, immobility and trotting were evoked throughout the tectum structures. However, whatever the response and kind of stimulus, the lowest thresholds were always found in the DLPAG and the highest ones in the ILSC. Besides, neither the appetitive, nor the offensive, muricide or male reproductive behaviors were produced by any kind of stimulus in the presence of appropriate targets. Accordingly, the present data suggest that the deeper layers of SC are most likely involved in the increased attentiveness (exophthalmus, immobility) or restlessness (trotting) behaviors that herald a full-blown flight reaction (galloping, jumping) mediated in the PAG.

Removal of the cortical projections alters expression of NOS in the different cell types of the superficial layers of the superior colliculus in rats

Nitric oxide has several biological roles and nitric oxide synthase (NOS) is expressed in the nervous system, and co-localizes with NADPH-diaphorase. The superficial layers of the superior colliculus (SC), which receive retinal and cortical inputs, present NADPH-d staining in a sub-population of neurons that include all cell types. We have previously shown, by NADPH-diaphorase, that eye enucleation alters the intracellular distribution of NOS. Here, we studied the effect of cortical ablation on NOS expression by neurons in collicular superficial layers. Our results show that cortical ablation alters the proportion of different NOS-positive cell types, but not the intracellular distribution of the enzyme.

Quantifying presynaptic terminals at the light microscope level in intact and deafferented central nervous structures

Quantification of presynaptic terminals often requires laborious techniques that involve tissue preparation for ultrastructural analysis [Science 171 (1971) 804; Vision Res. Suppl. 3 (1971) 281]. Modern preembedding immunohistochemical techniques provide a high morphological resolution at the light microscope level, thus allowing us to identify immunostained presynaptic boutons using specific antibodies. When absolute density of boutons ( D a) is analysed for comparison between control and deafferented nervous tissue, quantification may be distorted due to tissue shrinkage that follows deafferentiation. The magnitude of this effect must be, therefore, estimated to correct quantitative data. Using the superior colliculus (SC) as a model, an easily applicable protocol to quantify the density of small size labelled particles in control and deafferented nervous tissue is described. This protocol was used to analyse the effect of neonatal and adult enucleation on the adult pattern of cholinergic input to the rat SC. Statistical treatment of data demonstrated that neonatal enucleation caused a drastic increase in bouton density in the visual collicular layers, stratum zonale (SZ) and stratum griseum superficiale (SGS). The same lesion carried out in adult animals caused an increase in the bouton density exclusively in the SZ.

Commissural connections of human superior colliculus

The superior colliculus of higher mammals is a laminated structure of the midbrain that receives visual input in superficial layers, and visual, auditory and somatosensory input in deep layers. The superior colliculi on either side are interconnected via the intercollicular commissure, which has been proposed to play a role in visual transfer and gaze orienting. Intercollicular connections have been anatomically demonstrated in various species including macaque monkeys but not in man. Here we describe the organization of commissural connections of the superior colliculus in man. A single injection of the carbocyanine tracer 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate was made into the superior colliculus in five post-mortem brains. Contralateral to the injection, labelled axons formed a dense bundle in the deep collicular layers and isolated axons were present in the superficial layers. Synaptic-like boutons were found in all collicular layers. Injections placed at different rostro-caudal levels revealed a roughly topographical organization; the bulk of the labelled axons were found opposite to the injection, with a progressive decrease in labelling at more rostral and caudal levels. Our results demonstrate that superficial and, to a larger extent, deep layers participate in intercollicular connections, and suggest that visual information crosses at the collicular level.

The fine organization of nigro-collicular channels with additional observations of their relationships with acetylcholinesterase in the rat

The nigro-collicular pathway that links the basal ganglia to the sensorimotor layers of superior colliculus plays a crucial role in promoting orienting behaviors. This connection originating in the pars reticulata and lateralis of the substantia nigra has been shown in rat and cat to be topographically organized. In rat, a functional compartmentalization of the substantia nigra has also been shown reflecting that of the striatum. In light of this, we reinvestigated the topographical arrangement of the nigro-collicular pathway by examining the innervation of each nigral functional zone. We performed small injections of either biocytin or wheatgerm agglutinin conjugated with horseradish peroxidase restricted to identified somatic, visual and auditory nigral zones. Frontally cut sections showed that innervations provided by the three main nigral zones form a mosaic of complementary domains stratified from the stratum opticum to the ventral part of the intermediate collicular layers, with the somatic afferents sandwiched between the visual and the auditory ones. When reconstructed from semi-horizontal sections, nigral innervations organized in the form of a honeycomb-like array composed of 100 cylindrical modules covering three-quarters of the collicular surface. Such a modular architecture is reminiscent of the acetylcholinesterase lattice we previously described in rat intermediate collicular layers. In the enzyme lattice, the surroundings of the cylindrical modules are composed of a mosaic of dense and diffuse enzyme subdomains. Thus, we compared the distribution of the overall nigral projection and of its constituent channels with the acetylcholinesterase lattice. The procedure combined axonal labelling with histochemistry on single sections for acetylcholinesterase activity. The results demonstrate that the overall nigral projection overlaps the acetylcholinesterase lattice and its constituent channels converge with either the dense or the diffuse enzyme subdomains. The stereometric arrangement of the nigro-collicular pathway is suggestive of an architecture promoting the selection of collicular motor programs for different classes of orienting behavior.

Developmental Depression of Glutamate Neurotransmission by Chronic Low-Level Activation of NMDA Receptors

Slabs of slow-release plastic (Elvax) containing NMDA or solvent were implanted over the rat colliculus beginning on postnatal day 8 (P8). Whole-cell patch clamping in the superficial superior collicular layers (sSCs) from P10 to P21 demonstrated a severe decrease in spontaneous EPSC frequency after chronic NMDA treatment. The decrease was not attributable to an increase in GABA(A) receptor-mediated inhibition and was present only when NMDA receptor (NMDAR) current was blocked by Mg(2+). Analysis of miniature EPSCs indicated that many active sites on NMDA-treated neurons lacked functional AMPA and kainate receptor (AMPA/KAR) currents, and AMPA/KAR:NMDAR current ratios of evoked EPSCs were also significantly reduced. In addition, the normal downregulation of NMDAR decay time in sSC neurons at P11 was absent after NMDA treatment. Nevertheless, neither AMPA nor NMDA receptor subunit expression was altered by NMDA treatment, and experiments with the NMDAR antagonist ifenprodil suggested that incorporation of NR2A-containing NMDARs at the sSC synapses was unperturbed. Thus, disrupting but not blocking NMDARs suppresses the development of AMPA/KAR currents. The absence of the P11 NMDAR current downregulation is likely a secondary effect resulting from the reduction of AMPA/KAR function. Chronic agonist application reduces but does not eliminate NMDAR conductances. Therefore these data support an active role for NMDAR currents in synaptic development. Prolonged NMDA treatment in vivo, which couples reduced postsynaptic Ca(2+) responses with normally developing afferent activity, produces a long-lasting synaptic depression and stalls glutamatergic synaptogenesis, suggesting that the correlation between robust NMDAR activation and afferent activity is an essential component during normal development.

Plastic response of the retrospleniocollicular connection after removal of retinal inputs in neonatal rats. An anterograde tracing study.

The effects of neonatal enucleation on the final adult pattern of retrospleniocollicular connection in the rat was studied using the anterograde tracer biotindextranamine 10,000 (BDA) iontophoretically injected in different anteroposterior locations of the retrosplenial cortex. Retrosplenial afferents are normally distributed in all collicular layers beneath the stratum griseum superficiale (SGS) throughout almost the entire rostrocaudal and lateromedial collicular axes. Neonatal enucleation caused an invasion of lower SGS by abundant retrosplenial afferents, whose distribution remained unaltered in intermediate and deep collicular layers. Axons entering the deafferented SGS showed variable morphologies and arborization patterns. Some of them ran lateromedially close to the SGS-stratum opticum (-SO) limit, giving rise to many collaterals which invaded the lower part of the SGS; whereas others formed narrow terminal arbors, mostly branching in the SO. In the intermediate layers, synaptic profiles were mainly found close to the borders of acetylcholinesterase (AChE) patches in both control and enucleated animals, indicating that neonatal enucleation does not alter the final pattern of retrospleniocollicular afferents to these collicular regions. The results presented here demonstrate that neonatal enucleation leads to the development of an aberrant projection from the retrosplenial cortex to the deafferented superficial layers of the superior colliculus. These results provide new information regarding the reorganization of connections subsequent to neonatal enucleation and suggest that, in enucleated animals, nonvisual multisensorial information could be relayed to central circuits which in intact animals belong to the visual system.