Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey

In retrograde studies of corticotectal projections in the monkey using horseradish peroxidase (HRP), projections of the frontal lobes were found to originate not only from the frontal eye fields and prefrontal association cortex but also from both motor and premotor cortex. Even small HRP injections into the superficial layers of the superior colliculus yielded labelled cells in the agranular cortex (area 6) of the anterior bank of the arcuate sulcus. After large collicular injections affecting all layers, labelled cells were found in both motor and premotor cortex. This projection appeared to be topographically organized. Injections into the anterolateral parts of the superior colliculus labelled cells that were distributed within the presumed finger-hand--arm-shoulder representation, whereas after more caudal injections labelled cells occurred more in the presumed arm-trunk representation. The supplementary motor cortex was not found to contain labelled cells. The corticotectal cells in the motor cortex differed from those in the premotor cortex in their size distribution; the former being small, the latter both small and large. The functional significance of the motor and premotor input into the superior colliculus for sensory, and particularly visual, guidance of movements is discussed in view of a collicular role in the extrapersonal space representation and of its possible participation in steering arm and hand movements.     

Global visual processing in the monkey superior colliculus

Neurons were recorded in the superficial layers of the superior colliculus in anesthetized monkeys. As classically described, cells were non-selective for target direction and speed when the target moved through an empty visual field. However, these same cells were sensitive to target direction and speed relative to a textured moving background. The target's response was suppressed when its direction and speed were similar to that of the background, irrespective of the absolute direction of background movement.     

Postnatal development of corticotectal neurons in the kitten striate cortex: a quantitative study with the horseradish peroxidase technique

Postnatal development of striate cortical neurons projecting to the superior colliculus (SC) was studied in cats, ranging in age from newborn to adult, by injection of horseradish peroxidase (HRP) into the SC. At birth HRP-labelled cells were widely distributed throughout the cortex between the splenial and suprasylvian sulci, although a very rough topographic correspondence seemed to exist between the striate cortex and SC. The labelled cells were confined to layer V of the cortex, as in the adult. They were very densely packed and their somas were already pyramidal in shape although very slender. During the third to eighth days, apical dendrites of a substantial number of cells, mostly located in the upper bank of the splenial sulcus, were filled with HRP up to layer I and their somas were larger than those of cells located near the crown of the lateral and postlateral gyri. At the eighth day and thereafter, the distribution of the labelled cells across the visual cortex was not so widespread as that seen in the newborn kittens. The dendritic arborization pattern of labelled cells became nearly adultlike at the four week, and its full maturation was seen at the eighth week. A quantitative analysis of the cross-sectional areas of the cells and their packing density in layer V of the cortex revealed that (1) the size of cells increased very rapidly during the second week and became almost adultlike at the fifth week; (2) the density of cells reduced dramatically during the second week and thereafter at a low rate until the eighth week; and (3) the ratio of the labelled to unlabelled cells in layer V decreased remarkably also during the second week. These results suggest that an elimination of axon collaterals of corticotectal cells or their death may take place mostly during the second week of age, when eye-opening occurs in kittens. By comparison with previous data on functional development of the SC, it is also suggested that the maturation of visual response properties of SC neurons may depend on postnatal development of corticotectal cells.     

Projections from the functional subdivisions of the frontal eye field to the superior colliculus in the monkey

The frontal eye field (FEF) can be divided into the lateral subdivision representing the central visual field (VF), and the medial subdivision representing the peripheral VF. In this report, we examined neurally projected parts within the superior colliculus (SC) from those electrophysiologically identified subdivisions in the FEF using the horseradish peroxidase anterograde transport method. We found that the lateral subdivision projected into the anterolateral portion of the SC, whereas the medial one into the posteromedial portion, indicating that there is a correlation in the VF representation between the source and the target of this corticotectal system.     

Cortical projections to the superior colliculus in tree shrews (Tupaia belangeri)

The visuomotor functions of the superior colliculus depend not only on direct inputs from the retina, but also on inputs from neocortex. As mammals vary in the areal organization of neocortex, and in the organization of the number of visual and visuomotor areas, patterns of corticotectal projections vary. Primates in particular have a large number of visual areas projecting to the superior colliculus. As tree shrews are close relatives of primates, and they are also highly visual, we studied the distribution of cortical neurons projecting to the superior colliculus by injecting anatomical tracers into the colliculus. Since projections from visuotopically organized visual areas are expected to match the visuotopy of the superior colliculus, injections at different retinotopic locations in the superior colliculus provide information about the locations and organization of topographic areas in extrastriate cortex. Small injections in the superior colliculus labeled neurons in locations within areas 17 (V1) and 18 (V2) that are consistent with the known topography of these areas and the superior colliculus. In addition, the separate locations of clusters of labeled cells in temporal visual cortex provide evidence for five or more topographically organized areas. Injections that included deeper layers of the superior colliculus also labeled neurons in medial frontal cortex, likely in premotor cortex. Only occasional labeled neurons were observed in somatosensory or auditory cortex. Regardless of tracer injection location, we found that, unlike primates, a substantial projection to the superior colliculus from posterior parietal cortex is not a characteristic of tree shrews. J. Comp. Neurol. 521:1614–1632, 2013. © 2012 Wiley Periodicals, Inc.     

Cholinergic projections from the parabigeminal nucleus (Ch8) to the superior colliculus in the mouse: a combined analysis of horseradish peroxidase transport and choline acetyltransferase immunohistochemistry

Choline acetyltransferase (ChAT) immunocytochemistry, acetylcholinesterase histochemistry and muscarinic receptor autoradiography demonstrated a cholinergic innervation within the superior colliculus. A method for the concurrent visualization of ChAT and transported horseradish peroxidase showed that a major extrinsic source for this cholinergic input is in the parabigeminal nucleus. We have designated these cholinergic neurons as the Ch8 cell group.     

Cortical somatosensory and trigeminal inputs to the cat superior colliculus: Light and electron microscopic analyses

Two different axonal transport tracers were used in single animals to test the hypothesis that the expansive intermediate gray layer of the cat superior colliculus (stratum griseum intermediale, SGI) is composed of sensorimotor domains. The results show that two sensory pathways, the trigeminotectal and the corticotectal arising from the fourth somatosensory area, commingle in patches across the middle tier of the SGI. Furthermore, the data reveal that tectospinal cells are distributed within these patches. Taken together, these results show a commingling of functionally related afferents and a consistent spatial relationship between these afferents and tectospinal neurons. These relationships indicate that the SGI consists of domains that can be distinguished by their unique combinations of afferent and efferent connections. The ultrastructural characteristics and synaptic relationships of these somatosensory afferent pathways suggest that they have distinct roles within the sensorimotor domain of the SGI. The trigeminotectal terminals are relatively small, contain round vesicles and make asymmetrical synapses on small, presumably distal, dendrites. We submit that these trigeminal terminals bestow the basic receptive field properties upon SGI neurons. In contrast, the somatosensory corticotectal terminals are relatively large, contain round vesicles, make asymmetrical synapses, participate in triads, and are presynaptic to proximal dendrites. We suggest that these cortical terminals bestow integrative abilities on SGI neurons. J. Comp. Neurol. 388:313–326, 1997. © 1997 Wiley-Liss, Inc.     

Sublamination within the superficial gray layer of the squirrel monkey: an analysis of the tectopulvinar projection using anterograde and retrograde transport methods

Anterograde and retrograde tracing methods have been used to analyze the cells of origin and the axonal distribution of the tectopulvinar projection in the squirrel monkey. Our most interesting finding is that tectopulvinar neurons occupy a cytoarchitecturally distinct sublamina of the stratum griseum superficiale (SGS) called the lower SGS (SGSL). The distinction between the SGSL and the upper SGS (SGSU) is further indicated by the findings of others that the SGSL receives different amounts of retinal and cortical input compared to the SGSU. Previous physiological studies have also shown that cells in the SGSL possess different response characteristics than those in the SGSU. Differences in cytoarchitecture, afferent and efferent connections, and physiological properties of the SGSL versus the SGSU indicate that sublaminae are the anatomical mechanism which enables different information channels to maintain some degree of autonomy within the SGS, and at the same time use the same topographic map within this layer.     

Maturation of cortical control over superior colliculus cells in cat

The specialized receptive field properties of superior colliculus cells are believed to be dependent upon cortical influences. Yet despite a corticotectal projection near the time of birth and adult-like cortical cells at the beginning of the second week of life, specialized properties do not appear in many superior colliculus cells until quite late in postnatal development. We now report that this apparent conflict is due to the protracted functional maturation of the corticotectal system.     

Intercollicular fibers terminating in the superficial layers of the superior colliculus: a WGA-HRP study in the rat

The intercollicular pathway in the albino rat was studied using a lectin, wheat germ agglutinin, conjugated to horseradish peroxidase (WGA-HRP) as a pathway tracer and a modified HRP histochemistry method. The results showed that a small number of intercollicular fibers were observed in the rostral half of the superficial layers and the caudal half of the intermediate layers of the superior coliculus, while the majority of the intercollicular fibers were distributed in the intermediate and deep layers in the rostral half of the colliculus. The fibers which terminated in the superficial layers of the colliculus were studied in some detail and were subdivided into 4 different morphological types. These results suggest that the intercollicular projection is more broadly distributed in the superior colliculus than has been reported previously in most of the mammalian species studied, and the optic portion of the colliculus receives direct input from different morphological types of intercollicular neurons located on the opposite side of the midbrain.     

Hypothalamic and ventral thalamic projections to the superior colliculus in the cat

The present report describes the organization of collicular afferents that arise within either the hypothalamus or the ventral thalamus. Following the placement of large injections of WGA-HRP into the superior colliculus of the cat, retrogradely labeled neurons are located within the reticular nucleus of the thalamus, the zona incerta, the fields of Forel, and throughout the hypothalamus. Although the dorsal hypothalamic area contains the largest number of labeled hypothalamic neurons, labeled cells are also found within the periventricular, paraventricular, dorsomedial, ventromedial, posterior, lateral, and anterior hypothalamic nuclei. A strikingly similar pattern of distribution of labeled neurons is also observed following placement of small injections of WGA-HRP that are restricted within the stratum griseum intermedium (SGI). In contrast, hypothalamic and ventral thalamic labeling is not seen after placement of injections within the stratum griseum superficiale. Following the placement of injections of tritiated anterograde tracers within the dorsal hypothalamic area, transported label is organized in two bands of clusters over the SGI. When injections of tritiated tracers are placed within the zona incerta, terminal label is also located over the SGI; however, the distribution of silver grains does not appear as clusters or distinct puffs. On the basis of the comparison of the cellular types that give rise to these projections and the differences in terminal distribution, we suggest that the hypothalamic and ventral thalamic projections to the superior colliculus are totally separate and unrelated pathways. The functional implications of the hypothalamotectal pathway are also discussed.     

Auditory brainstem projections to the ferret superior colliculus: Anatomical contribution to the neural coding of sound azimuth

The mammalian superior colliculus (SC) contains a neural map of auditory space. It is not known whether this topographic representation emerges at the level of the SC or is relayed there from other auditory areas. We have used retrograde labelling techniques in ferrets to examine the sources and pattern of innervation from auditory brainstem nuclei. After multiple injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the SC, the heaviest concentrations of labelled cells were found in the nucleus of the brachium (BIN) and external nucleus of the inferior colliculus, with much weaker labelling in the nucleus sagulum, dorsal, intermediate and ventral nuclei of the lateral lemniscus, paralemniscal regions, and periolivary nuclei. The projections were predominantly ipsilateral, although labelled cells were found on both sides of the brainstem. Single injections of WGA-HRP or discrete injections of red and green latex microspheres revealed that the caudal and lateral regions of the SC receive the heaviest projections, although the majority of the retrogradely labelled neurons in the contralateral BIN project to rostral SC. On the ipsilateral side, neurons in rostral and caudal regions of the BIN were labelled primarily by the tracer injected into rostral and caudal regions of the SC, respectively. However, no clear segregation was apparent in the BIN after injections into the medial and lateral regions or in any of the other nuclei after either injection paradigm. These data suggest that converging inputs from several auditory brainstem nuclei contribute to the construction of the auditory space map in the SC, although information about sound azimuth may be conveyed to this nucleus via a spatially ordered projection from the ipsilateral BIN. J. Comp. Neurol. 390:342–365, 1998. © 1998 Wiley-Liss, Inc.     

Parabigeminal projections to the superior colliculus in the cat

Small amounts of horseradish peroxidase were injected into the superior colliculus of the cat and the distribution of labeled neurons in the parabigeminal nuclei was mapped. After injections placed dorsal to the stratum opticum in the superior colliculus, the parabigeminal nucleus is the only mesencephalic and/or rhombencephalic structure in which labeled neurons are observed. The number of labeled neurons in the parabigeminal nucleus increases after injections that include both the superficial and the deep layers of the superior colliculus. Each part of the superior colliculus receives projections from wide areas of both parabigeminal nuclei, although it also receives more abundant projections from one or more restricted parts of these nuclei. The anterior third of the parabigeminal nuclei is the part which sends the fewest projections to the superior colliculus. These projections terminate principally in the central and intermediate part of the contralateral colliculus, while a smaller number of fibers terminate in the lateral and rostral part of the ipsilateral colliculus. The intermediate third of the parabigeminal nuclei sends projections to all parts of the ipsilateral colliculus, but the greatest number of these goes to the contralateral colliculus. These contralateral projections terminate principally in the lateral parts of the contralateral colliculus, and in lesser number in its central and rostral, and medial and rostral areas. The posterior third of the parabigeminal nucleus sends scant efferents to wide areas of the ipsilateral and contralateral colliculi, and a dense projection to the medial and intermediate, medial and caudal and central and intermediate parts of the ipsilateral colliculus. There are also consistent projections from the posterior third of the parabigeminal nucleus to the central and rostral and medial and rostral parts of this ipsilateral colliculus. These results demonstrate a topographical organization of the parabigemino-tectal projections in the cat, as a pathway that facilitates the integration in the colliculus of visual impulses of different origin in the retina. This organization permits the modulation of the superior colliculus in its participation in both the extrageniculate visual system and in the regulation of eye and head orientation movements through the parabigeminal projections to the superficial and deep layers of the colliculus, respectively.     

Quantitation of synaptic vesicle antigen in rabbit superior colliculus during normal development and after neonatal visual cortical lesion

Radioimmunoassay of a synaptic vesicle-associated antigen (SV Ag) using monoclonal antibodies was used to study synapse formation in the rabbit superior colliculus (SC). Normal postnatal development was compared with development following unilateral neonatal visual cortex lesion. Neonatal lesion of the visual cortex prevents the cortical innervation of the SC, which normally accounts for 35% of the total SV Ag levels in the rabbit SC. Following such lesions, a small but significant increase in SV Ag levels over that in normally innervated SC was observed. These observations suggest that competition between retinotectal and corticotectal inputs may be required for normal development of synaptic connections in the SC.     

The projection from striate and extrastriate cortical areas to the superior colliculus in the rat

Following single injections of horseradish peroxidase (HRP) in the superior colliculus (SC) and [3H]proline in the striate cortex of rats, a close correspondence was observed in the topographical arrangements of extrastriate cortical fields of HRP retrograde label and of isotope anterograde label. These results support the notion that extrastriate cortex is divided into multiple physiologically and anatomically defined areas, and they suggest that these areas project separately to SC.     

Efferent projections of the neonatal superior colliculus: Extraoculomotor-related brain stem structures

The development of eye movements is a prolonged process which presumably involves the efferents of the superior colliculus. In the present study we sought to determine which, if any, of the colliculus efferents that influence eye movements in adult cats were present in neonatal kittens. The autoradiographic and orthograde horseradish peroxidase tracing methods were employed in kittens ranging from 6 h to 5 weeks of age and in adult cats.Surprisingly, most of the known projections from the superior colliculus which are believed to be involved in eye movements were already present in the youngest animals studied. These included projections to (a) the ventral central gray matter overlying the oculomotor nucleus, and (b) those portions of the pontine and medullary reticular formation which provide excitatory and inhibitory inputs to abducens neurons. Apparently, the pathways over which the superior colliculus influences eye movements are elaborated quite early in life. However, in the predorsal bundle and pontomedullary reticular areas the density of transported label was less in 1-day-old kittens than in older animals. Thus, anatomical as well as functional development of portions of this circuitry appear to require a significant period of postnatal maturation.