Superficial Collicular Layers Research Articles

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.

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.

Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: Possible substrates of a subcortical visual pathway to the amygdala

The aim of the present study was to identify synaptic contacts from axons originating in the superior colliculus with thalamic neurons projecting to the lateral nucleus of the amygdala. Axons from the superior colliculus were traced with the anterograde tracers Phaseolus vulgaris leucoagglutinin or the biotinylated and fluorescent dextran amine "Miniruby." Thalamo-amygdaloid projection neurons were identified with the retrograde tracer Fluoro-Gold. Injections of Fluoro-Gold into the lateral nucleus of the amygdala labeled neurons in nuclei of the posterior thalamus which surround the medial geniculate body, viz. the suprageniculate nucleus, the medial division of the medial geniculate body, the posterior intralaminar nucleus, and the peripeduncular nucleus. Anterogradely labeled axons from the superior colliculus terminated in the same regions of the thalamus. Tecto-thalamic axons originating from superficial collicular layers were found predominantly in the suprageniculate nucleus, whereas axons from deep collicular layers were detected in equal density in all thalamic nuclei surrounding the medial geniculate body. Double-labeling experiments revealed an overlap of projection areas in the above-mentioned thalamic nuclei. Electron microscopy of areas of overlap confirmed synaptic contacts of anterogradely labeled presynaptic profiles originating in the superficial layers of the superior colliculus with retrogradely labeled postsynaptic profiles of thalamo-amygdaloid projection neurons. These connections may represent a subcortical pathway for visual information transfer to the amygdala.

Temporal Correlations between Functional and Molecular Changes in NMDA Receptors and GABA Neurotransmission in the Superior Colliculus

Activation of the NMDA subtype of glutamate receptor is required for activity-dependent structural plasticity in many areas of the young brain. Previous work has shown that NMDA receptor currents decline approximately at the time that developmental synaptic plasticity ends, and in situ hybridization studies have suggested that receptor subunit changes may be occurring during the same developmental interval. To establish a system in which the relationship between these properties of developing synapses can be explored, we have combined patch-clamp recordings with mRNA- and protein-level biochemical analyses to study the developmental regulation of NMDA receptors in the superficial layers of the rat superior colliculus. These experiments document an abrupt decrease in the NMDA receptor contribution to synaptic currents that occurs before eye opening and is closely associated with changes in NR1 protein, rapidly rising levels of the NMDA receptor subunit NR2A, and decreasing levels of NR2B. The functional and molecular changes also are correlated with the developmental decline in structural plasticity in these layers. In addition, both physiological and biochemical methods show evidence of GABA-mediated inhibition in the superficial collicular layers beginning after eye opening. This may provide an additional heterosynaptic mechanism for controlling excitation and plasticity in this neuropil by pattern vision. Thus our findings lend support to the idea that high levels of NMDA receptor function are associated with the potential for structural rearrangement in CNS neuropil and that the functional downregulation of this molecule results, at least partially, from changes in its subunit composition.

Reticular thalamic region in the rabbit: Organisation of efferents to the superior colliculus

Although it is well-established that the reticular thalamic nucleus provides a strong GABAergic input to the dorsal thalamus, the existence of reticular efferents to other subcortical centres is less certain. In this study, we investigate whether the reticular nucleus projects to a major brainstem centre, the superior colliculus. The neuronal tracer, biotinylated dextran, was injected into superficial and deep layers of the superior colliculus of rabbits and the resultant labelling in the reticular region was examined. After large injections, which encompassed both superficial and deep collicular layers, two discrete populations of retrogradely labelled cells are seen in the region of the reticular nucleus. One population of retrogradely labelled cells lies in the dorsocaudal regions of the reticular nucleus, the classically defined visual sector. This group of retrogradely labelled reticular cells is also seen after injections into the superficial layers of the superior colliculus, but not after injections limited to the deeper collicular layers. The other population lies close to the ventromedial edge of the main body of the reticular nucleus, within a region referred to as the inner small-celled region. This group of small cells has been commonly thought to be part of the reticular nucleus, but our immunohistochemical studies suggest that this is a clearly separate region, a region continuous ventrally with zona incerta. The retrogradely labelled cells in the inner small-celled region are seen also after injections limited to the deeper collicular layers, but not after injections limited to the superficial collicular layers. Our results suggest functional heterogeneity within the reticular nucleus: Specifically, it suggests that the nucleus is in a position to influence the processing of visual information at both the dorsal thalamic and midbrain levels.

Direction selectivity and physiological compensation in the superior colliculus following removal of areas 17 and 18.

Previous studies indicate that cortical areas 17 and 18 play a prominent role in generating the direction selectivities of neurons in the superior colliculus of the cat. This hypothesis was tested by quantifying the activities of neurons in the superficial collicular layers in intact cats and cats which incurred ablation of areas 17 and 18 and part of area 19. In addition, since behavioral and anatomical studies suggest a functional adjustment in the superior colliculus following removal of inputs from areas 17, 18, and 19 in the neonatal cat, we included a group of neonatally lesioned cats. Computation of an index of directionality indicated that the majority of neurons in intact cats preferred movement in one direction, thus confirming reports of others. Following ablation of areas 17 and 18 and part of area 19 in both groups of lesioned cats, only modest changes in the population indices were detected when poorly responsive neurons were eliminated from the analyses. Based upon levels of visually evoked neuronal activity, our data suggest a physiological compensation by neurons in stratum griseum superficiale following removal of areas 17, 18, and 19 inputs. In the intact and neonatally operated groups, activity in stratum griseum superficiale is high, whereas in the adult lesioned group activity is low. In stratum opticum, neuronal activity was similar in all three groups of cats. These results show that neurons in stratum griseum superficiale undergo a physiological compensation following removal of immature areas 17 and 18.

Evidence for intrinsic expression of enkephalin-like immunoreactivity and opioid binding sites in cat superior colliculus

We have investigated the cellular localization of opioid peptides and binding sites in the cat's superior colliculus by testing the effects of retinal deafferentation and intracollicular excitotoxin lesions on patterns of enkephalin-like immunostaining and opiate receptor ligand binding. In normal cats, enkephalin-like immunoreactivity marks a thin tier in the most dorsal stratum griseum superficiale, small neurons of the stratum griseum superficiale, and patches of fibers in the intermediate and deeper gray layers. Eliminating crossed retinotectal afferents by contralateral eye enucleation had little immediate effect on this pattern, although chronic eye enucleation from birth did reduce immunoreactivity in the superficial layers. By contrast, fiber-sparing destruction of collicular neurons by the excitotoxins N-methyl- d-aspartate and ibotenic acid virtually eliminated enkephalin-like immunoreactivity in the neuropil of the upper stratum griseum superficiale, presumably by killing enkephalinergic cells of the superficial layers. Such lesions did not eliminate the patches of enkephalin-like immunoreactivity in the deeper layers. In normal cats, opiate receptor ligand binding is dense in the stratum griseum superficiale, particularly in its upper tier, and moderately dense in the intermediate gray layer. Contralateral eye removal had no detectable effect on the binding pattern, but excitotoxin lesions of the colliculus dramatically reduced binding in both superficial and deep layers. Some ligand binding, including part of that in the upper stratum griseum superficiale, apparently survived such lesions. Similar effects were observed in the lateral geniculate nucleus: enucleation produced no change in binding, whereas excitotoxin lesions greatly reduced specific opiate binding. We conclude that in the superficial collicular layers, both enkephalin-like opioid peptides and their membrane receptors are largely expressed by neurons of intrinsic collicular origin. The close correspondence between the location of these intrinsic opioid elements and the tier of retinal afferents terminating in the upper stratum griseum superficiale further suggests that opiatergic interneurons may modulate retinotectal transmission postsynaptically.

Developmental changes in the pattern of retinal projections in pigmented and albino rabbits

The distribution of retinal axons and/or terminals in the retino-recipient nuclei of pigmented and albino rabbits varying in age from the 24th postconceptional day (24PCD) to adulthood was examined following unilateral intraocular injections of the enzyme horseradish peroxidase. Both in pigmented and albino rabbits contralateral retinal axons and/or terminals in the dorsal and ventral lateral geniculate nuclei (DLG and VLG), superior colliculi (SC), pretecta (PT) and accessory optic tract nuclei (AON) were already present on 24PCD. In the period 26–30PCD the contralateral projection occupied the entire volume of the DLG, VLG and SC. Although 32PCD (the day of birth) the proportions of the volumes of DLG and VLG occupied by the contralateral projections were slightly reduced, their volume continued to increase in absolute terms up to adulthood. In pigmented rabbits the ipsilateral projections to all retino-recipient nuclei were most dense and extensive on 26PCD. From 26PCD, the relative extent of the ipsilateral projections was gradually reduced, but a reduction in their absolute extent did not become evident until 32PCD. By 32PCD the ipsilateral projection to the AON had disappeared completely. The distribution of ipsilateral axons and/or terminals and the relative proportion of the nuclei occupied by the ipsilateral projection in all other retino-recipient nuclei had become adult-like by 34PCD. In albino rabbits only a sparse ipsilateral projection to the presumptive superficial collicular layers was present on 24PCD. In the remaining retino-recipient nuclei an ipsilateral projection was present on 26PCD. From 26PCD the relative extent and from 30PCD the absolute extent of ipsilateral retinal axons and/or terminals was gradually reduced. The relative extent of the ipsilateral projection had become almost adult-like by 34PCD. Throughout development ipsilateral projections in albinos were consistently less dense and less extensive than those in pigmented rabbits, and unlike in pigmented rabbits, the ipsilateral projections to the VLG and PT were only transient. The differences betweent the two strains in the pattern of retinofugal projections were further enhanced during the period of segregation of the ipsilateral and contralateral projections. Considering the fact that in both strains there is a partial correspondence between the period in which the spatial extent of the ipsilateral projections is reduced and the period of retinal ganglion cell (RGC) death 79,80, it is likely that RGC death plays a role in the process of segregation of the retinal afferents into ocular domains. However, our data suggest that other mechanism(s) also play an important role in the process.

The mosaic of the uncrossed retinal projection in the superior colliculus of the cat.

The uncrossed retinocollicular projection in the cat was labeled by axonal transport of horseradish peroxidase from the eye and visualized in tangential sections through the superior colliculus. The terminals of this pathway are distributed in clusters and form a mosaic pattern rather than stripes in the superficial collicular layers. It is suggested that the periodicity of this pattern relates to the smallest receptive field diameters across the visual field.

Convergence of retinal W-cell and corticotectal input to cells of the cat superior colliculus.

1. Conduction velocities of retinotectal W-cell afferents were estimated from differences among latencies of collicular unit responses to supramaximal stimulation of the contralateral optic disk (OD), optic chiasm (OX), and ipsilateral optic tract (OT). W-cell afferents driving collicular neurons had very slowly conducting axons, nearly all below 8 m/s (mean = 5.3 m/s). These match the conduction velocities of W-cell axons terminating in the uppermost superficial gray layer and triggering juxtazonal potentials (JZPs). Such slow conduction velocities are typical of W-cells belonging to the W2 subclass ("phasic W-cells"), but are slower than nearly all W1 cells ("tonic W-cells"). 2. Most W-driven cells were activated at latencies longer than expected for monosynaptic input from these W-cell afferents. However, comparable delays were observed among JZPs, which signal monosynaptic excitation of collicular neurons by W-cell terminals. This suggests that the delayed activation of W-driven cells reflects slowed conduction in the preterminal segments of W-cell afferents rather than polysynaptic transmission of W-cell signals through intermediary neurons in the brain stem or cortex. Thus monosynaptic inputs from retinal W2 cells appear to drive most neurons of the superficial collicular layers. 3. Convergence of retinotectal W-cell and corticotectal pathways was assessed by recording responses of W-driven collicular cells to intracortical stimulation of area 17. The great majority of W-driven collicular cells were activated by cortical stimulation (41/52; 79%), indicating that such convergence is widespread. 4. The population of corticotectal cells influencing W-driven collicular cells may differ from that mediating Hoffmann's Y-indirect pathway. W-driven collicular cells were activated from the striate cortex at longer latencies (mean = 6.3 ms) than cells driven by the Y-indirect pathway (mean = 2.5 ms). In addition, cortically activated W-driven cells were common throughout the superficial gray layer, whereas cells driven by the Y-indirect input were encountered only in the deepest part of the superficial gray and below. 5. W2 cells, apparently the dominant retinotectal cell type, nearly all project contralaterally and are tuned for slow stimulus velocities. Thus the binocularity of W-driven collicular cells and their sensitivity to moderately fast stimulus motion probably reflect the convergent cortical input described here.

3H]nicotine binding sites are associated with mammalian optic nerve terminals.

The autoradiographic distribution of [3H]nicotine binding sites was examined in the superior colliculus in normal rats and cats, and in animals in which one or both eyes were removed. [3H]Nicotine binding sites in normal animals were densely concentrated in the superficial layers of the colliculus corresponding to the zone of termination of optic nerve fibers. Following bilateral enucleation, [3H]nicotine binding in the superficial collicular layers was drastically reduced. Unilateral enucleation markedly reduced [3H]nicotine binding sites in the colliculus contralateral to the removed eye, with little effect on the ipsilateral colliculus. These results provide further evidence that nicotinic acetylcholine receptors have a presynaptic location on optic tract terminals and may therefore modulate retinotectal transmission in both the rat and cat visual system.

The morphology of neurons in rat tectal transplants as revealed by Golgi-Cox impregnation.

The Golgi technique has been used to examine the morphology of neurons within tectal transplants. Embryonic tectal tissue was transplanted to the midbrain of newborn rats. Four to eight months later, host animals were decapitated under anaesthesia, the unfixed brains removed and processed by Golgi-Cox impregnation. In tectal grafts, different types of neuron were recognized on the basis of the size and shape of their somata and the morphology of their dendritic trees. Neuronal types found in transplants resembled cell classes found in normal rat superior colliculus (SC). Neurons characteristic of the superficial collicular layers such as marginal, ganglion type I, stellate and horizontal cells and multipolar cells typical of the deeper collicular layers were identified in the transplants. Compared with normal cells, grafted neurons often had smaller dendritic fields and fewer dendritic spines. No laminar organization was discernable in the grafts and there was commonly no preferential orientation of perikarya or dendrites. Small cells with similar dendritic morphology were sometimes found grouped together in patches within the graft neuropil. These patches resembled cytologically and histochemically distinct areas described in previous studies and may represent areas homologous to the superficial layers of normal SC.

Quantitative morphological changes in the superior colliculus and the parabigeminal nucleus in the bilaterally microphthalmic rat.

Quantitative morphological changes in the superior colliculus (SC) and the parabigeminal nucleus (PB) were studied in hereditary bilaterally microphthalmic rat, which lacks the optic nerve completely. Volumes of the retinorecipient superficial collicular layers of SC (SCS) to the central gray matter were decreased by 35% with respect to the normal. However, the cell density in SCS was increased as much as 150% of the normal. The stratum griseum superficiale was packed densely and irregularly with small-sized round nerve cells. The stratum opticum of the mutant rat appeared as a narrow band with few fiber components, but it contained some medium-sized polygonal neurons. No significant changes were found in the deeper layers of the microphthalmic SC. Bilaterally microphthalmic PB reduced both its volume and cellular density per unit area (about 30 and 75% of the normal, respectively). Furthermore, in contrast to the normal rat, the mutant PB could not be subdivided into the dorsal, middle and ventral subgroups.

Connectional organization of the superior colliculus

The mammalian superior colliculus is a prominent subcortical sensorimotor integrator that plays an important and specific role in allowing the animal to orient to visual, auditory and somatosensory stimuli 1–8. Over the past decade, anatomical and physiological studies have revealed some important organizational correlates of this functional specificity. In the early 1970s, combined anatomical and behavioral studies in the laboratory of I.T. Diamond 1,5, as well as electrophysiological analyses by B. Gordon 9 and B. Stein 7 and colleagues, demonstrated fundamental differences between the superficial collicular layers (I–III) and the deep layers (IV–VII). This ‘superficial-deep’ distinction was in turn refined as a result of studies that revealed connectional and functional differences between individual layers comprised in these two major regions. Recent data indicate that the layers are themselves divisible according to criteria based on anatomical connections and physiology. In light of these recent findings we suggest that the connectional subdivisions of individual superficial layers differ in type from those of individual deep layers. We further suggest that the different types of subdivision reflect the different quantities and qualities of connections of the superficial versus the deep layers.

An EM-autoradiographic analysis of the projection from cortical areas 17, 18, and 19 to the superior colliculus in the cat.

The electron microscopic autoradiographic method was used to identify terminals of axons from cortical areas 17, 18, and 19 in the superficial layers of the superior colliculus. The results show that terminals of area 17 neurons contain round vesicles and made asymmetrical synaptic contacts predominantly onto one or more dendrites or dendritic appendages. Some profiles postsynaptic to labeled terminals contain vesicles and presumably are involved in serial synaptic arrangements. Terminals of area 18 and 19 neurons in the superficial collicular layers appear to comprise two populations, one similar in most respects to area 17 terminals, containing round vesicles and making asymmetrical contacts. The other contains pleomorphic vesicles and makes symmetrical contacts upon dendrites and dendritic appendages. These terminals rarely contact more than one postsynaptic profile, and rarely do the postsynaptic profiles contain vesicles. The two populations of area 18 and 19 terminals containing round and pleomorphic vesicles, respectively, are present in the ratio of approximately 3:1, although this ratio varies throughout the sublaminae of the superficial collicular layers. The presence of two distinct types of cortical terminals in the colliculus suggests that cortical modulation of collicular processing is more complex than was previously conceived.

Histochemical identification and afferent connections of subdivisions in the lateralis posterior-pulvinar complex and related thalamic nuclei in the cat

Fiber pathways of the extrageniculate visual system have been shown in the cat to define an orderly sequence of adjoining, roughly parallel zones within the posterolateral thalamus. The present study provides evidence that these and related thalamic subdivisions can be identified histochemically by their differing contents of acetylthiocholinesterase. The brains of fifty cats were prepared for acetylthiocholinesterase histochemistry by the methods of Geneser-Jensen & Blackstad and Karnovsky & Roots. Serial sections were cut in each of the three Horsley-Clarke planes and a standard transverse cholinesterase series, containing occasional reference sections stained for myelin or Nissl substance, was used to assemble graphic reconstructions of the main cholinesterase subdivisions. Patterns of afferent connections were visualized by anterograde axon transport or fiber-degeneration techniques and recorded in thirteen sets of detailed chartings. In nine sets, serially adjoining sections processed by the cholinesterase and anterograde methods were directly compared and plotted together. The caudal part of the lateral thalamic region was divided into two main subdivisions: the lateralis posterior-pulvinar complex, which receives extrageniculate visual input, and the complex comprising the nuclei lateralis medialis and suprageniculatus (LM-Sg), which receives fiber projections from auditory association cortex and the deep layers of the superior colliculus. The latter complex occupies a ventromedial zone alongside the lateralis posterior-pulvinar complex. It is distinguished in the cholinesterase stain by prominent 0.5–1.5 mm wide patches of high enzyme activity that appear against a pale background. Within the lateralis posterior-pulvinar complex, three zones could be distinguished: (1) the medial part of the nucleus lateralis posterior (LPm) is rich in cholinesterase activity and receives input from the superficial collicular layers; (2) the lateral part of the nucleus lateralis posterior and the nucleus posterior of Rioch (LP1-NP) have much weaker cholinesterase activity and receive input from the striate cortex and other areas of visual cortex; (3) the pulvinar, the most lateral of the subdivisions, is a zone of high cholinesterase activity in which some pale patches appear. It receives input from the pretectum and is associated with a differentiated lateral marginal zone receiving direct projections from the retina and area 17. The intermediate nucleus of the lateral group was divided into two parts. The pars caudalis (LIc) has a mottled appearance in the cholinesterase stain; it receives an ascending input from the pretectotectal border zone and a descending projection from parietal cortex including area 7. The pars oralis of the intermediate nucleus (LIo) is rich in cholinesterase activity; it receives a descending projection from the anterior parietal cortex comprising in part area 5. These two intermediate subdivisions were flanked dorsally and rostrally by the nucleus lateralis dorsalis. The cholinesterase material suggested a division of the lateralis dorsalis into at least medial and lateral parts, but the connections of these regions were not analyzed in detail. The finding of clear chemoarchitectural subdivisions in the lateralis posterior-pulvinar complex and adjoining regions has practical significance as a guide to thalamic organization and raises the possibility that some extrageniculate and related transthalamic pathways may be differentiated from one another by the neurotransmitters they employ in the thalamus.

Periodic-compartmental distribution of acetylcholinesterase in the superior colliculus of the human brain

The superior colliculus of the human brain was studied in autopsy material stained by the acetylthiocholinesterase methods of Geneser-Jensen & blackstad (1971) and Karnovsky & roots (1964) . The histochemical findings suggest that in the human, as in common laboratory mammals, the superior colliculus is characterized by a periodic vertical segmentation in addition to a horizontal stratification into layers. In frontal sections through the superior colliculus in each of three human brains, acetylthiocholinesterase staining in the middle gray layer was distributed in a series of 200–400 μm wide patches separated by less densely stained zones. The patches were irregular in shape and some were composed of a core of intense enzyme activity surrounded by a rim of weaker stain. Comparable concentrations of the enzyme were not apparent in the superficial collicular layers. Dorsalview reconstructions of the enzyme patches were prepared in two cases from drawings of serial sections. The resulting planar maps showed that the patches present in frontal sections form parts of narrow bands of varying length that run in a roughly longitudinal direction through the colliculus. This pattern of banding is remarkably similar to that observed with cholinesterase methods in the intermediate gray layer of the cat superior colliculus and recalls also the bands formed by nigrotectal terminals in this layer. It is not yet clear which tissue elements are being stained by the cholinesterase method. Nevertheless, the finding of histochemically distinct repeating units in the human superior colliculus demonstrates the existence, in the brain of man, of a periodic ordering with many of the characteristics of columnar organization.

Sources of subcortical projections to the superior colliculus in the cat.

A comprehensive search for subcortical projections to the cat superior colliculus was conducted using the retrograde horseradish peroxidase (HRP) method. Over 40 different subcortical structures project to the superior colliculus. The more notable among these are grouped under the following categories. Visual structures: ventral lateral geniculate nucleus, parabigeminal nucleus, pretectal area (nucleus of the optic tract, posterior pretectal nucleus, nuclei of the posterior commissure). Auditory structures: inferior colliculus (external and pericentral nuclei), dorsomedial periolivary nucleus, nuclei of the trapezoid body, ventral nucleus of the lateral lemniscus. Somatosensory structures: sensory trigeminal complex (all divisions, but mainly the gamma division of nucleus oralis), dorsal column nuclei (mostly cuneate nucleus), and the lateral cervical nucleus. Catecholamine nuclei: locus coeruleus, raphe dorsalis, and the parabrachial nuclei. Cerebellum: medial, interposed, and lateral nuclei, and the perihypoglossal nuclei. Reticular areas: zona incerta, substantia nigra, midbrain tegmentum, nucleus paragigantocellularis lateralis, and the hypothalamus. Evidence is presented that only the parabigeminal nucleus, the nucleus of the optic tract, and the posterior pretectal nucleus project to the superficial collicular layers (striatum griseum superficiale and stratum opticum), while all other afferents terminate in the deeper layers of the colliculus. Also presented is information concerning the rostrocaudal distribution of some of these afferent connections. These findings stress the multiplicity and diversity of inputs to the deeper collicular layers, and more specifically, identify multiple sources of the physiologically well-known representations of the somatic and auditory modalities in the colliculus.