Ascending and descending projections to the inferior colliculus in the rat

The ascending and descending projections to the central nucleus of the inferior colliculus (IC) were studied with the aid of retrograde transport of horseradish peroxidase (HRP). HRP-labelled cells were found in contralateral cochlear nuclei, where the majority of different cell types was stained. Few labelled cells were observed in the ipsilateral cochlear nuclei. HRP-positive neurones were found in all nuclei of the superior olivary complex on the ipsilateral side with the exception of the medial nucleus of the trapezoid body, which was never labelled either ipsilaterally or contralaterally. The largest concentration of HRP-labelled cells was usually observed in the ipsilateral superior olivary nucleus. Smaller numbers of labelled cells were present in contralateral nuclei of the superior olivary complex. Massive projections to the inferior colliculus were found from the contralateral and ipsilateral dorsal nucleus of the lateral lemniscus and ipsilateral ventral nucleus of the lateral lemniscus. Many neurones of the central and external nuclei of the contralateral inferior colliculus were labelled with HRP. Topographic organisation of the pathways ascending to the colliculus was expressed in the cochlear nuclei, lateral superior olivary nucleus and in the dorsal nucleus of the lateral lemniscus. HRP--positive cells were found in layer V of the ipsilateral auditory cortex, however, the evidence for topographic organisation was lacking.     

Tectal and Related Target Areas of Spinal and Dorsal Column Nuclear Projections in Hedgehog Tenrecs

The terminal distributions of spinal and dorsal column nuclear projections to tectum, pretectum, and central gray of hedgehog tenrecs (Echinops telfairi and Setifer setosus) were investigated using anterograde axonal flow and various tracer substances. In the inferior colliculus, the densest and most extensive mesencephalic projections were found within the pericentral regions. One target area, referred to as the external portion of the inferior colliculus, was represented as a semicircle of grain patches lateral and caudal to the central nucleus. This region received somesthetic afferents from the dorsal column nuclei and from spinal segments at various levels. In contrast, after high cervical injections, the pericentral portion dorsomedial to the rostral half of the central nucleus was labeled almost exclusively. This area of labeling was distinct from the labeling in the central gray and might be best compared with the intercollicular zone in other species. The superior colliculus received projections predominantly from the high cervical cord; minor projections also arose from lumbar spinal segments and the dorsal column nuclei. The terminal field covered roughly the caudal half of the colliculus and involved the stratum griseum intermediale in a patch-like fashion. Some labeling was also found in the stratum griseum profundum and in the stratum griseum superficiale. Other than in the colliculi, weak pretectal projections were observed following dorsal column nuclear injections, while the nucleus of Darkschewitsch was labeled best following lumbosacral injections. All mesencephalic target areas were labeled consistently on the contralateral side, while their ipsilateral side was involved to a varying degree: The relatively most prominent ipsilateral labeling was seen in the central gray, being roughly similar on both sides; scarcely any labeling was noted in the ipsilateral superior colliculus. Tectal injections of retrograde tracer, in addition, revealed a considerable number of labeled neurons in a relatively cell-poor region immediately ventral to the high cervial dorsal horn. This region might correspond to the lateral cervical nucleus, an aggregation of neurons that so far has only been demonstrated in higher mammals.     

Somatosensory areas S2 and PV project to the superior colliculus of a prosimian primate, Galago garnetti

As part of an effort to describe the connections of the somatosensory system in Galago garnetti, a small prosimian primate, injections of tracers into cortex revealed that two somatosensory areas, the second somatosensory area (S2) and the parietal ventral somatosensory area (PV), project densely to the ipsilateral superior colliculus, while the primary somatosensory area (S1 or area 3b) does not. The three cortical areas were defined in microelectrode mapping experiments and recordings were used to identify appropriate injection sites in the same cases. Injections of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) were placed in S1 in different mediolateral locations representing body regions from toes to face in five galagos, and none of these injections labeled projections to the superior colliculus. In contrast, each of the two injections in the face representation of S2 in two galagos and three injections in face and forelimb representations of PV in three galagos produced dense patches of labeled terminations and axons in the intermediate gray (layer IV) over the full extent of the superior colliculus. The results suggest that the higher-order somatosensory areas, PV and S2, are directly involved in the visuomotor functions of the superior colliculus in prosimian primates, while S1 is not. The somatosensory inputs appear to be too widespread to contribute to a detailed somatotopic representation in the superior colliculus, but they may be a source of somatosensory modulation of retinotopically guided oculomotor instructions.     

Somatosensory areas S2 and PV project to the superior colliculus of a prosimian primate,Galago garnetti

As part of an effort to describe the connections of the somatosensory system in Galago garnetti, a small prosimian primate, injections of tracers into cortex revealed that two somatosensory areas, the second somatosensory area (S2) and the parietal ventral somatosensory area (PV), project densely to the ipsilateral superior colliculus, while the primary somatosensory area (S1 or area 3b) does not. The three cortical areas were defined in microelectrode mapping experiments and recordings were used to identify appropriate injection sites in the same cases. Injections of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) were placed in S1 in different mediolateral locations representing body regions from toes to face in five galagos, and none of these injections labeled projections to the superior colliculus. In contrast, each of the two injections in the face representation of S2 in two galagos and three injections in face and forelimb representations of PV in three galagos produced dense patches of labeled terminations and axons in the intermediate gray (layer IV) over the full extent of the superior colliculus. The results suggest that the higher-order somatosensory areas, PV and S2, are directly involved in the visuomotor functions of the superior colliculus in prosimian primates, while S1 is not. The somatosensory inputs appear to be too widespread to contribute to a detailed somatotopic representation in the superior colliculus, but they may be a source of somatosensory modulation of retinotopically guided oculomotor instructions.     

Pulvina-lateralis posterior nucleus complex of mammals and the visual function

It is now well established that the lateral posterior-pulvinar (LP-P) complex of mammals is involved in visual processing. However, the actual function of these large nuclei of the thalamus remains unknown. In contrast to the nearby lateral geniculate nucleus, the LP-P complex does not receive any substantial direct projections from the retina. Its main visual inputs come from the mesencephalon and the neocortex. Most cells in the LP-P complex behave like cortical units. They are tuned to the orientation, direction, spatial and temporal frequencies of the visual stimulus. In addition, most units are binocular and sensitive to relative retinal disparity. Despite their multiple inputs, the LP-P complex cells form an homogeneous population and their overall properties do not reflect those of a given cortical or subcortical area. On the basis of its afferent and efferent connectivity, it has been proposed that the LP-P complex may serve as a relay of an extrageniculate ascendant pathway which originates from the superior colliculus, and/or provide another route for the geniculo-striate input to reach the extrastriate areas. Despite the fact that there is some electro-physiological evidence of such functions, it is now often suggested that the LP-P complex may integrate its multiple inputs and be involved in functions which go beyond those of a simple thalamic relay. Recent findings suggest that the LP-P complex might play a role in visual spatial attention.     

Independent parcellation of the embryonic visual cortex and thalamus revealed by combinatorial Eph/ephrin gene expression

The visual cortex in primates is parcellated into cytoarchitectonically, physiologically, and connectionally distinct areas: the striate cortex (V1) and the extrastriate cortex, consisting of V2 and numerous higher association areas [1]. The innervation of distinct visual cortical areas by the thalamus is especially segregated in primates, such that the lateral geniculate (LG) nucleus specifically innervates striate cortex, whereas pulvinar projections are confined to extrastriate cortex [2--8]. The molecular bases for the parcellation of the visual cortex and thalamus, as well as the establishment of reciprocal connections between distinct compartments within these two structures, are largely unknown. Here, we show that prospective visual cortical areas and corresponding thalamic nuclei in the embryonic rhesus monkey (Macaca mulatta) can be defined by combinatorial expression of genes encoding Eph receptor tyrosine kinases and their ligands, the ephrins, prior to obvious cytoarchitectonic differentiation within the cortical plate and before the establishment of reciprocal connections between the cortical plate and thalamus. These results indicate that molecular patterns of presumptive visual compartments in both the cortex and thalamus can form independently of one another and suggest a role for EphA family members in both compartment formation and axon guidance within the visual thalamocortical system.     

The neurons of origin of non-cortical afferent connections to the oculomotor nucleus. A retrograde labeling study in the rabbit.

The cellular origin of the brainstem projections to the oculomotor nucleus in the rabbit has been investigated by using free (HRP) and lectin-conjugated horseradish peroxidase (WGA-HRP). Following injections of these tracers into the somatic oculomotor nucleus (OMC), retrogradely labeled cells have been observed in numerous brainstem structures. In particular, bilateral labeling has been found in the four main subdivisions of the vestibular complex, predominantly in the superior and medial vestibular nuclei and the interstitial nucleus of Cajal, while ipsilateral labeling was found in the rostral interstitial nucleus of the medial longitudinal fascicle (Ri-MLF), the Darkschewitsch and the praepositus nuclei. Neurons labeled only contralaterally have been identified in the following structures: mesencephalic reticular formation dorsolateral to the red nucleus, abducens internuclear neurons, group Y, several areas of the lateral and medial regions of the pontine and medullary reticular formation, ventral region of the lateral cerebellar nucleus and caudal anterior interpositus nucleus. This study provides also information regarding differential projections of some centers to rostral and caudal portions of the OMC. Thus, the rostral one-third appears to receive predominant afferents from the superior and medial vestibular nuclei, while the caudal two-thirds receive afferents from all the four vestibular nuclei. Finally, the group Y sends afferents to the middle and caudal, but not to the rostral OMC.     

The corticofugal pathways of the visual system

Cortical neurons belonging to the same topological ensemble send axons to thalamic and mesencephalic structures and also to contra and ipsilateral cortical areas. The projections are called the corticofugal system. This review addresses the organization and the functions of the efferent cortical fibers within the visual network. For example, the cortico-geniculate fibers participate in shaping the structure of the concentric receptive fields of geniculate cells. Namely, the size of the surround area depends on descending impulses from the cortex. By contrast, cortico-mesencephalic fibers have a more global influence on visual responses. Following the interruption of cortical activity all responses to visual stimuli decline; although in rodents and lagomorphs cortical inactivation does not eliminate those visual responses that are sent to the superior colliculus or pretectum directly from the retina. In each hemisphere it has been demonstrated that contra-lateral cortico-cortical fibers participate in the continuity of the two visual hemi-fields, as the interruption of the callosal impulses results in a truncated field in which the contralateral part of the receptive field is missing., overlaps the vertical meridian is missing. Finally, ipsilateral cortico-cortical fibers allow a consolidation of visual properties of cortical cells. It must be added that there are considerable differences among species in the organization of cortico-cortical relationships. However, this survey seems to indicate that all corticofugal axons are excitatory.     

An autoradiographic study of the retinal projections in the Formosan monkey

This study investigated the retinal projections of the adult Formosan rock monkey by monocular injection of radioactive proline and fucose. We found that the retinofugal fibers terminated bilaterally in the suprachiasmatic, pregeniculate, lateral geniculate, pretectal complex, pulvinar nucleus, superior colliculus, dorsal and lateral terminal nuclei of the accessory optic system. More crossed retinal terminations were observed, with the exception that the suprachiasmatic nucleus received almost equally of both retinal projections. The existence of the retinal projection to the medial terminal nucleus of the accessory nucleus was in doubt. In the geniculate nucleus, the retinal fibers terminated contralaterally in layers 1, 4 and 6; and ipsilaterally in 2, 3 and 5. In the superior colliculus, most retinal fibers were aggregated superficially in a band located in the contralateral striatum griseum superficialis of the superior colliculus, and had few gaps on the ipsilateral one. The present investigation shows that the Formosan rock monkey has a similar pattern of optic fiber distribution to that of other macaques.     

Tectospinal and tectoreticular cells: their distribution and afferent connections

Experiments on chloralose-anaesthetized cats have shown that cells in the superior colliculus may be antidromically activated either from the pontomedullary reticular formation or the ventral cervical spinal cord, or from both sites. In tests on 111 units this has provided a basis for differentiating between cells of origin of the tectospinal tract and the tectoreticular system within the superior colliculus. Tectospinal cells may be activated both by spinal and pontine stimulation; tectoreticular cells cannot be activated by spinal stimulation. Both tectoreticular and tectospinal cells respond to visual and muscle afferent stimulation. The afferent connections may be strongly inhibitory as afferent input to the superior colliculus ofter prevented subsequent antidromic invasion. This was more commonly seen in tectospinal cells than tectoreticular cells. The distribution of the two cell populations within the superior colliculus was also found to be dissimilar. Evidence has also been obtained to suggest that the tectoreticular system, in part, consists of collaterals of the tectospinal tract.     

Circadian Modulation of c-Fos Expression Occurs only in the SCN and not in Other Visual Projection Areas in the Rat

Brief photic stimuli at different circadian times induce differential expression of c-Fos in the suprachiasmatic nuclei (SCN). Whether circadian modulation of light-induced c-Fos expression occurs in other visual projection areas is not known. We addressed this question by estimating the immunohistochemical expression of c-Fos induced by 60 min light pulses at three different circadian times. The areas studied were the SCN, the ventral lateral geniculate nucleus, the intergeniculate leaflet, the ventral tegmental area, the superior colliculus and a non-visual control, the paraventricular thalamic nucleus (PVT). Light pulses induced an increase in the number of c-Fos immunoreactive cells in the SCN as a function of the circadian time. Remaining visual structures showed a light-induced increase in c-Fos expression but this was not dependent on the circadian time. The non-visual control area (PVT) did not respond to light pulses. Since no circadian modulation was found in the intergeniculate leaflet, which rec eives collateral projections from the same retinal ganglion cells that project to the SCN, nor in other primary visual projection areas, the present findings suggest that the circadian modulation of light-induced c-Fos expression in the SCN depends mainly on the functional properties of its intrinsic neurons.     

Circadian Modulation of c-Fos Expression Occurs only in the SCN and not in Other Visual Projection Areas in the Rat

Brief photic stimuli at different circadian times induce differential expression of c-Fos in the suprachiasmatic nuclei (SCN). Whether circadian modulation of light-induced c-Fos expression occurs in other visual projection areas is not known. We addressed this question by estimating the immunohistochemical expression of c-Fos induced by 60 min light pulses at three different circadian times. The areas studied were the SCN, the ventral lateral geniculate nucleus, the intergeniculate leaflet, the ventral tegmental area, the superior colliculus and a non-visual control, the paraventricular thalamic nucleus (PVT). Light pulses induced an increase in the number of c-Fos immunoreactive cells in the SCN as a function of the circadian time. Remaining visual structures showed a light-induced increase in c-Fos expression but this was not dependent on the circadian time. The non-visual control area (PVT) did not respond to light pulses. Since no circadian modulation was found in the intergeniculate leaflet, which rec eives collateral projections from the same retinal ganglion cells that project to the SCN, nor in other primary visual projection areas, the present findings suggest that the circadian modulation of light-induced c-Fos expression in the SCN depends mainly on the functional properties of its intrinsic neurons.     

Primary optic projections in the rabbit. Study using the horseradish peroxidase anterograde labeling technic

The primary visual pathways, in particular those to the lateral geniculate body, of 11 albino and 7 pigmented rabbits, were studied using the method of anterograde labelling with horseradish peroxidase following injection of the tracer into the vitreous body of one eye. A heavy projection to the contralateral dorsal lateral geniculate nucleus was seen in all animals. In both albino and pigmented animals a region devoid of label was present in the medial part of the alpha sector of the nucleus. This region corresponded to a compact, oval or wedge-shaped field of terminal label in the ipsilateral nucleus, which was much heavier in pigmented than in albino rabbits. In the ventral lateral geniculate nucleus, contralateral retinal input was almost entirely confined to the caudal half of the lateral sector of the nucleus, where two laminae of dense terminal label, separated by a less densely labelled area, were oriented parallel to one another and to the optic tract. This bilaminar distribution of retinal afferents to the ventral lateral geniculate nucleus has not been described in previous studies. The ipsilateral projection was to the dorsal part of the lateral sector and was most prominent in pigmented animals. The "intergeniculate leaflet" received a prominent contralateral input in all animals, and a clear ipsilateral input in pigmented animals, which overlapped with the contralateral input. Projections to other primary visual centres (pretectal nuclei, superior colliculus, nuclei of the accessory optic tract) are also described.     

Directed early axonal outgrowth from retinal transplants into host rat brains

Axons from retinae transplanted to the brain stem of neonatal rats exhibit two patterns of outgrowth that can be experimentally uncoupled from each other depending upon the location of the graft. Retinae placed close to the surface of the rostral brain stem (as much as 5 mm from the tectum) emit axons that project toward the superior colliculus along the subpial margin of the rostral brain stem. In contrast, axons from grafts embedded deep within the midbrain parenchyma project through the neuropil directly to the overlying superior colliculus, as long as the retina is within about 1 mm of the tectal surface. The present study shows that, as long as the retina is located outside the superior colliculus, and regardless of whether the axons derive from grafts in subpial or intraparenchymal locations, the earliest projections are oriented towards the superior colliculus. We have also found, however, that axons from retinae transplanted directly onto the superior colliculus can form projections that extend along the subpial margin away from the tectum. There are several major conclusions that may be drawn from these observations. First, the final tectopetal, transplant-derived projection does not result from the reorganization of an initially random outgrowth but is directed from the start toward an appropriate region of termination. Second, it appears that the interaction of retinal axons with a primary target alters the ability of the growth cone to respond to directional cues along the optic tract. Thus, although adding support to the proposal that optic axons attain the superior colliculus through an interaction involving substrates distributed along the optic tract and diffusible factors originating in the target region, it is increasingly clear that such interactions are likely to be complex and hierarchical.     

Cross-species recognition of tectal cues by retinal fibers in vitro

The retinae of vertebrates project in a topographic manner to several visual centers of the brain. The formation of these projections could depend on the existence of position-specific properties of retinal and target cells. In this study, we have tested the in vitro growth of mouse retinal fibers on membranes derived from various regions of the embryonic superior colliculus, a main target of the retina in this species. Fibers had the choice of elongating on membranes taken from either the anterior or the posterior half of the superior colliculus. Fibers from temporal areas of the retina prefer to elongate on anterior collicular membranes, while fibers from nasal areas do not show a preference. These phenomena are observed with membranes from embryonic (E15-E18) or young postnatal mice. In interspecies cultures where mouse retinal fibers had to grow on chick tectal membranes, or vice versa, the same preference for anterior tectal or collicular membranes in growth of temporal retinal fibers is observed, suggesting some similarities in the cues used in both species.     

Electrophysiological properties of isthmic neurons in frogs revealed by in vitro and in vivo studies

The frog nucleus isthmi (parabigeminal nucleus in mammals) is a visually responsive, cholinergic and anatomically well-defined group of neurons in the midbrain. It shares reciprocal topographic projections with the ipsilateral optic tectum (superior colliculus in mammals) and strongly influences visual processing. Anatomical and biochemical information indicates the existence of distinct neural populations within the frog nucleus isthmi, which raises the question: are there electrophysiological distinctions between neurons that are putatively classified by their anatomical and biochemical properties? To address this question, we measured frog nucleus isthmi neuron cellular properties in vitro and visual response properties in vivo. No evidence for distinct electrophysiological classes of neurons was found. We thus conclude that, despite the anatomical and biochemical differences, the cells of the frog nucleus isthmi respond homogeneously to both current injections and simple visual stimuli.     

Remapping for visual stability

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.     

Oculomotor areas in the rabbits midbrain and pretectum.

The role of some meso- and diencephalic structures in eye movements was investigated by ablation and stimulation experiments. Optokinetic nystagmus was abolished by small lesions in the lateral pretectum, but not by complete removal of the superior colliculi. Stimulation of the superior colliculus and other visual centers was effective in eliciting nystagmus (slow phase ipsilateral), but the most efficient trigger zones are found in the lateral pretectum and the midbrain tegmentum. Only from these areas could nystagmus still be elicited after degeneration of the primary optic fibers. The lateral pretectal trigger zone is probably identical with the nucleus of the optic tract. It is postulated that this nucleus is an essential station for horizontal optokinetic reactions. Saccades were obtained by stimulation of the mesencephalic central grey, but not for any visual centers such as the superior colliculus.     

Oculomotor areas in the rabbit's midbrain and pretectum

The role of some meso- and diencephalic structures in eye movements was investigated by ablation and stimulation experiments. Optokinetic nystagmus was abolished by small lesions in the lateral pretectum, but not by complete removal of the superior colliculi. Stimulation of the superior colliculus and other visual centers was effective in eliciting nystagmus (slow phase ipsilateral), but the most efficient trigger zones are found in the lateral pretectum and the midbrain tegmentum. Only from these areas could nystagmus still be elicited after degeneration of the primary optic fibers. The lateral pretectal trigger zone is probably identical with the nucleus of the optic tract. It is postulated that this nucleus is an essential station for horizontal optokinetic reactions. Saccades were obtained by stimulation of the mesencephalic central grey, but not for any visual centers such as the superior colliculus.