Retinal ganglion cell size groups projecting to the superior colliculus and the dorsal lateral geniculate nucleus in the North American opossum

The retinal ganglion cells projecting to the superior colliculus (SC) and dorsal lateral geniculate nucleus (LGNd) of the North American opossum (Didelphis virginiana) were studied by using the retrograde transport of horseradish peroxidase (HRP). The four ganglion cell size groups recognized previously were found to project in systematically different ways. After injections of HRP into the superior colliculus, labeled cells were seen in nasal retina contralateral to the injection and in temporal retina both ipsilateral and contralateral to the injection. In contralateral nasal retina cells of all size classes were labeled, while in contralateral temporal retina small (8-14 micrometers diameter), small-medium (15-19 micrometers diameter), and large (greater than 24 micrometers diameter) cells were labeled but few, if any, large-medium (20-24 micrometers diameter) cells were labeled. In ipsilateral temporal retina, soma size groups labeled included small-medium, large-medium, and large cells, but very few small cells. A nasal-temporal difference in the soma size of ganglion cells projecting to the SC was found: Labeled cells in temporal retina were 1.7-4.2 micrometers larger than their counterparts in nasal retina. Following injection of HRP into the LGNd, label was seen in contralateral nasal and ipsilateral temporal retina with no label seen in contralateral temporal retina. The labeled cells were small-medium, large-medium, and large. No small ganglion cells were labeled from the LGNd. A small nasal-temporal soma size difference in retinal ganglion cells projecting to the LGNd was seen: labeled cells in temporal retina were 1.0-2.1 micrometers larger than in nasal. It is concluded that all four ganglion cell size groups in the opossum project to the SC, but that only the three largest project to the LGNd.     

Correlation between different types of retinal ganglion cells and their projection pattern in the albino rat

Injecting Fluoro-Gold (FG) and Evans-Blue (EB) into the right dLGN and SC in the adult albino rat, ipsilaterally projecting double-labeled retinal ganglion cells were mainly seen in the ventrotemporal crescent. They were mainly large sized cells. The ipsilaterally projecting double-labeled cells tended to have larger somata than the single- and double-labeled cells projecting to the contralateral superior colliculus and/or dorsal nucleus of the lateral geniculate body.     

Retinal ganglion cell projections to individual layers of the lateral geniculate body in Galago crassicaudatus

The genus Galago provides an unique opportunity to study the relation between layers of the lateral geniculate body and classes of retinal ganglion cells. In the present experiments HRP was restricted to individual layers of the lateral geniculate body with the following results: After injections of the magnocellular layers, layers 1 and 2, labeled retinal ganglion cells ranged in size from 8 to 20 μm. After injections of the parvocellular layers, layers 3 and 6, labeled retinal ganglion cells ranged in size from 6 to 12 μm. After injections involving layers 4 and 5, which layers contain only very small, pale cells, labeled retinal ganglion cells ranged in size from 5 to 14 μm. Thus, the very largest ganglion cells were labeled only after injections of magnocellular layers 1 and 2, while small and medium retinal ganglion cells were labeled after HRP injections in every layer of the lateral geniculate body. Because the magnocellular layers actually contain a mixture of large, medium, and small-sized cells, we suggest that retinal ganglion cells of different size-classes project to geniculate relay cells of the corresponding size-class.     

The morphology, number, distribution and central projections of Class I retinal ganglion cells in albino and hooded rats

Class I retinal ganglion cells have been identified in wholemounts of rat retinae following injections of horseradish peroxidase (HRP) into retino-recipient nuclei. Class I cells are characterized by relatively large somata, 3-7 fairly frequently branching large-gauge primary dendrites and relatively thick axons. Cells with a very similar morphology have been visualized in the ganglion cell layer of retinal wholemounts using a neurofibrillar stain. The size of the somata and dendritic trees of Class I cells is affected by the density of all classes of ganglion cells: both somata and dendritic trees of Class I cells located in the region of peak density are smaller than those located in medium- and low-density ganglion cell regions. The mean numbers of Class I ganglion cells labelled following massive injections of HRP into retino-recipient nuclei were 876 (in albino rats) and 944 (in hooded rats), while the mean number of cells stained with the neurofibrillar method in albino retinae was 791. Thus, with the total number of positively identified retinal ganglion cells being 110,000-115,000 [Potts et al., 1982; Perry et al., 1983], Class I cells in both strains of rat constitute less than 1% of all retinal ganglion cells. Nevertheless the dendritic fields of Class I cells cover the entire retina. Although Class I cells are distributed relatively evenly across the retina, the density is slightly greater in the lower temporal retina where the bulk of the ipsilaterally projecting fibres originates. While Class I cells represent up to 10% of ipsilaterally projecting retinal ganglion cells in both strains of rat, fewer Class I cells project ipsilaterally in albinos than in hooded rats. All contralaterally projecting Class I cells appear to send branching axons to the superior colliculus and dorsal lateral geniculate nucleus. Class I cells represent a larger proportion of the ganglion cells projecting to the dorsal lateral geniculate nucleus (4-5%) than that of ganglion cells projecting to the superior colliculus (about 1%). The morphology, numbers, distribution and the pattern of the central projections of Class I retinal ganglion cells in rats suggest that they are likely to be homologues of the alpha-type ganglion cells distinguished in carnivores.     

Organization of subcortical pathways for sensory projections to the limbic cortex. II. Afferent projections to the thalamic lateral dorsal nucleus in the rat

Afferent projections to the thalamic lateral dorsal nucleus were examined in the rat by the use of retrograde axonal transport techniques. Small iontophoretic injections of horseradish peroxidase were placed at various locations within the lateral dorsal nucleus, and the location and morphology of cells of origin of afferent projections were identified by retrograde labeling. For all cases examined, subcortical retrogradely labeled neurons were most prominent in the pretectal complex, the intermediate layers of the superior colliculus, and the ventral lateral geniculate nucleus. Labeled cells were also seen in the thalamic reticular nucleus and the zona incerta. Within the cerebral cortex, labeled cells were prominent in the retrosplenial areas (areas 29b, 29c, and 29d) and the presubiculum. Labeled cells were also seen in areas 17 and 18 of occipital cortex. Peroxidase injections in the dorsal lateral part of the lateral dorsal nucleus result in labeled neurons in all of the ipsilateral pretectal nuclei, but especially those that receive direct retinal afferents. Labeled cells were also seen in the ventral lateral geniculate nucleus and the rostral tip of laminae IV-VI of the superior colliculus. In contrast, peroxidase injections in ventral medial portions of the lateral dorsal nucleus result in fewer labeled pretectal cells, and these labeled cells are found exclusively in the pretectal nuclei that do not receive retinal afferents. Other labeled cells following injections in the rostral and medial portions of the lateral dorsal nucleus are seen contralaterally in the medial pretectal region and nucleus of the posterior commissure, and bilaterally in the rostral tips of laminae IV and V of the superior colliculus. Camera lucida drawings of HRP labeled cells reveal that projecting cells in each pretectal nucleus have a characteristic soma size and dendritic branching pattern. These results are discussed with regard to the type of sensory information that may reach the lateral dorsal nucleus and then be relayed on to the medial limbic cortex.     

The projections of different morphological types of ganglion cells in the cat retina.

The central projections of the retinal ganglion cells of the cat were examined using the method of retrograde transport of horseradish peroxidase. Peroxidase was injected into the lateral geniculate nucleus and into the superior colliculus by means of a recording micropipette. After injections at retinotopically homologous points in these two structures in separate animals, tha patterns of retinal ganglion cell labeling were compared. We found that there were three populations of ganglion cells: small cells, that projected predominantly to the superior colliculus; medium-sized cells, that projected predominantly to the lateral geniculate nucleus; and large cells, some of which projected to both structures, and some of which projected to the lateral geniculate nucleus alons. Quantitative studies showed that the average size of the cells in each population was smaller at the area centralis than in the periphery. These results could be directly related to physiological classifications of retinal ganglion cells proposed by other authors.     

Thalamic connections of the ground squirrel superior colliculus and their topographic relations

The connections of the superior colliculus (SC) of the ground squirrel Spermophilus tridecemlineatus were studied with the horseradish peroxidase (HRP) method. Multiple pressure injections of HRP served to define the total pattern of SC projections while iontophoretic injections allowed differentiation of connections of the deep and superficial layers and determination of topographic relations of SC with its associated nuclei. The deep laminae were mainly connected with auditory, somatosensory and reticular regions of the brain, including the inferior colliculus, zona incerta, substantia nigra, mesencephalic central grey, pontine nuclei, spinal trigeminal nucleus, nucleus of the posterior commissure, thalamic reticular nucleus, raphe nuclei, lateral vestibular nucleus, the lateral superficial reticular formation of the medulla, the mesencephalic reticular formation, nucleus gracilis and the cervical spinal cord. The superficial laminae were connected with visual system structures. They were reciprocally connected with the dorsal and ventral lateral geniculate nuclei, the pretectum, nucleus lateralis posterior (LP), the parabigeminal nucleus and the contralateral SC. Connections between the SC and the dorsal lateral geniculate were topologic. LP was found to consist of three divisions: rostrolateral, rostromedial and caudal. SC was interconnected with the rostrolateral and caudal divisions. The connections between the SC and the rostrolateral division were topologic; those with the caudal division were not. The connections of the deep collicular layers in ground squirrels were similar to those which have been reported for cats and monkeys. The connections of the superficial laminae were more extensive than has been reported in other species. These elaborate interconnections indicate extensive interaction between primary retinal projection nuclei in the processing of visual information.     

Role of target tissue in regulating the development of retinal ganglion cells in the albino rat: effects of kainate lesions in the superior colliculus

Kainic acid or ibotenic acid was injected unilaterally into the major target regions of the axons of retinal ganglion cells--the superior colliculus (SC) or dorsal lateral geniculate nucleus (DLG)--of rat pups ranging in age from postnatal day 0 to postnatal day 10 (P0 - P10). While the collicular or geniculate neurons within the injection site died within 48 hours of the injection, damage to axons and terminals of extrinsic origin within the injected region was not apparent. The neuronal degeneration induced by the neurotoxins, observed at both the light and electron microscopic levels, resembled the neuronal degeneration that occurs in the colliculus during normal development. Macrophages were identified in the regions containing degenerating cells. Two to three weeks after the injections of neurotoxin, massive injections of the enzyme, horseradish peroxidase (HRP), were made into the retinorecipient nuclei. After about 24-hour survival time the numbers of retinal ganglion cells were estimated by counting the number of neurons containing HRP reaction products in sample areas distributed in a regular rectangular array across the entire retinal surface. In the animals in which the neurotoxin was injected into the SC during the first 4 postnatal days, there was a substantial reduction (on average 41.5%; the range: 27.5-65.5%) in the normal number (mean value of 113,000--Potts et al.: Dev. Brain Res. 3:481-486, '82) of retinal ganglion cells surviving the period of "naturally occurring ganglion cell death" in the retinae contralateral to the injected SC. By contrast, injections of neurotoxins into the DLG and/or the optic tract of newborn rats did not result in a significant reduction in the numbers of retinal ganglion cells surviving the period of naturally occurring ganglion cell death. The period of sensitivity of retinal ganglion cells to the injection of neurotoxin into the colliculi extends from birth to about the end of the first postnatal week; the greatest sensitivity seems to be restricted to the first 3-4 postnatal days. In the retinae in which the total number (and density) of ganglion cells was substantially reduced by the selective destruction of their target cells, the centro-peripheral difference in the somal diameters of the ganglion cells (apparent in normal animals) was abolished, both amongst the whole population of ganglion cells and amongst the ganglion cells with the largest somata, relatively thick axons, and large-gauge primary dendrites (Class I cells). The number and distribution of the Class I cells in the depleted retinae were, however, unaltered.(ABSTRACT TRUNCATED AT 400 WORDS)     

Fibre organization of the monkey's optic tract: I. Segregation of functionally distinct optic axons

The fibre organization of the monkey's optic tract was examined by implanting pellets of horseradish peroxidase into different locations within the tract, or into the superior colliculus and pretectum. Retinae were examined for the distribution, size, and morphological types of retrogradely labelled ganglion cells; optic tracts were examined for the distribution of anterogradely and retrogradely labelled axonal profiles; and lateral geniculate nuclei were examined for the distribution of anterogradely labelled processes within distinct geniculate laminae. Localized implants in the optic tract produced retrograde labelling of ganglion cells across wide regions of the retinal surface. The maximum density of labelled cells was always substantially less than the total ganglion cell density known to be present at those retinal loci. Distinct retinal ganglion cell types were labelled from differing regions within the optic tract: implants into the deep (dorsal) portion of the tract, far removed from the outer, pial, surface, retrogradely labelled predominantly P beta retinal ganglion cells, whereas implants into the superficial (ventral), subpial, part of the tract retrogradely labelled primarily the other retinal ganglion cell types, i.e., the P alpha, P gamma, and P epsilon cells. Within any given class of axon, there is a mapping of the centroperipheral retinal axis across the deep-to-superficial dimension of the tract, but this retinotopy is extremely coarse. Anterograde labelling of axonal terminations within the lateral geniculate nucleus showed a corresponding specificity for distinct geniculate laminae, the deep implants labelling the parvocellular laminae, superficial implants labelling the magnocellular laminae. Implants into the visual centres of the midbrain produced retrograde axonal labelling rostral to the lateral geniculate nucleus only in the superficial part of the optic tract. These results demonstrate that the monkey's optic tract is not a simple topographic mapping of retinal eccentricity. Rather, the primary organizational principle is that of a segregation of functionally distinct optic axon classes. As fibre order in the mammalian optic tract is also a chronological index of axonal arrival during development, the present results provide specific predictions about the temporal order of ganglion call genesis and axonal addition within the visual pathway. They also provide an anatomical basis for the functionally selective visual impairments that may arise following local damage to the optic tract in humans.     

Ventral lateral geniculate nucleus projects to the dorsal lateral geniculate nucleus in the cat

The lamina C3 of the dorsal lateral geniculate nucleus of the cat does not receive retinal projections but instead receives visual information from the small subpopulation of W-type ganglion cells via the upper substratum of the stratum griseum superficiale of the superior colliculus. We herein report a projection from the lateral division of the ventral lateral geniculate nucleus into the lamina C3 of the dorsal lateral geniculate nucleus. As the lateral division receives projections from the contralateral retina and the ipsilateral upper stratum griseum superficiale of the superior colliculus, we suggest that these regions make up a small cell type W-cell neuronal network that provides visual information to layer I of the striate cortex via the lamina C3.     

Genesis of neurons in the retinal ganglion cell layer of the monkey.

We have analyzed the genesis of various neuronal classes and subclasses in the ganglion cell layer of the primate retina. Neurons were classified according to their size and the time of their origin was determined by pulse labeling with 3H-thymidine administered to female monkeys 38 to 70 days pregnant. All offspring were sacrificed postnatally, and their retinas processed for autoradiography. The somata of cells in the retinal ganglion cell layer generated on embryonic day (E) 38 ranged from 9 to 14 microns in diameter. Between E40 and E56, the minimum soma diameter remained around 8-9 microns, while the maximum gradually increased to 22 microns. As a consequence, the means of the distributions of labeled cells also increased with age, from 11.8 microns diameter for cells generated on E38 to 14.6 microns diameter at E56. Over this period the percentage of labeled cells in the 10.5-16.5 microns and greater than 16.5 microns diameter range gradually increased. The proportion of the labeled cells in the less than 10.5 microns diameter range decreased from E38 to E45, but subsequently increased rapidly. At the end of neurogenesis in the retinal ganglion cell layer, around E70, most labeled cells were considerably smaller (7-9 microns) than those generated earlier. Our results indicate that within the ganglion cell layer of the macaque, neurons of small caliber are generated first, followed successively by medium sized cells. Large, putative P alpha cells are generated late. The production between E56 and E70 of cells with the smallest somata suggests that the last-generated neurons in the ganglion cell layer are predominantly displaced amacrine cells. Within the same sector of retina, different classes of neurons in the ganglion cell layer of the rhesus monkey appear to have a sequential schedule of production.     

Axonal transport of proteins in retinal ganglion cells. Characterization of the transport to the superior colliculus

The axonal transport of protein in the retinal ganglion cells of the adult rabbit was followed after intra-ocular injections of [³H]leucine. The labelled protein reached the nerve terminals in the superior colliculus in at least 4 phases. Compared with the lateral geniculate body, the superior colliculus received a considerable portion of the transported protein, and relatively more of this protein was carried to the superior colliculus with rapid phases of axonal transport. Radioautography showed that the label was localized to the 3 most dorsal layers of the superior colliculus. Cell fractionation of the superior colliculus indicated that the axonal terminals of optic origin did not easily form stable synaptosomes during a conventional homogenization and centrigation procedure.     

Cholecystokinin-like immunoreactive retinal ganglion cells project to the ventral lateral geniculate nucleus in pigeons

A subpopulation of retinal ganglion cells projecting to the pigeon ventral lateral geniculate nucleus was shown to contain cholecystokinin-like immunoreactivity. These ganglion cells were mainly distributed in the peripheral retina, and their somata sizes were medium to large (14-23 microns). Taken together with previous findings, these results indicate that the retinal input to the ventral geniculate is chemically heterogeneous.     

Retinal X-afferents bifurcate to lateral geniculate X-cells and to the pretectum or superior colliculus in cats

The question of whether retinal X-type ganglion cell axons project via axonal bifurcation to both the dorsal lateral geniculate nucleus (LGN) and the pretectum (PT) or the superior colliculus (SC) in the cat, was studied by examining the effects of PT and/or SC stimulation on the LGN cells. X-cells that responded monosynaptically to PT or SC stimulation were encountered as follows: 29%, 26%, and 4% of the tested X-cells responded to stimulation of PT, SC, and both, respectively. For the X-cells activated from the PT or SC, the latency tended to be a little longer than optic chiasm latency. The receptive field centers of the X-cells were located within the receptive fields of the multiple units from the SC whose stimulation could activate the corresponding X-cells. The present results demonstrate that a substantial proportion of the X-type LGN cells receive excitatory inputs from the retinal X-type ganglion cell axons that branch to the PT or the SC.     

Identification of ventral lateral geniculate nucleus cells projecting to the pretectum and superior colliculus in the cat

Among 235 histologically identified cells of the ventral lateral geniculate nucleus (LGV) in the cat, 66 responded antidromically to electrical stimulation of the pretectum (PT) and/or superior colliculus (SC): 22 projected to PT, 22 to SC and 22 to both sites. The LGV cells were innervated by optic tract fibers corresponding to axons of X- as well as W-type retinal ganglion cells.     

Four retinal ganglion cell types that project to the superior colliculus in the thirteen-lined ground squirrel (Spermophilus tidecemlineatus)

The morphology of retinal ganglion cells projecting to the superior colliculus (SC) of the thirteen-lined ground squirrel (Spermophilus tridecemlineatus) was studied after retrogradely labeling the cells with cholera toxin subunit B. On the basis of previous reports, labeled cells were classified as small (6–10 μm in soma diameter), medium (11–14 μm), or large (>14 μm). A total of 3,427 cells were studied. Small cells constituted 78% of the population, 21% were medium cells, and only 1% were classified as large. The morphology of medium-sized cells was studied in more detail because large cells were few in number and the staining of the dendritic tree of small cells was not optimal. The best labeled medium-sized cells were classified on the basis of the shape and size of their dendritic tree and the pattern of dendritic ramification. Four types were identified among the medium-sized ganglion cells. Two types were classified as symmetric δ-like and asymmetric δ-like cells considering the relative symmetric or asymmetric distribution of their dendritic branches and their similarities with the δ type of the cat. Approximately 52% of all the medium-sized cells studied were symmetrical δ-like, and 19% were classified as asymmetrical δ-like. These cells were also very similar to the symmetrical and asymmetrical directionally selective ganglion cells described in rabbit retina. Other cells were termed β-like. They had the smallest dendritic tree diameter, and their tree size seemed to be related to retinal eccentricity. Medium β-like cells comprised approximately 21% of all cells projecting to the SC. The fourth type was termed “acute angle” because most of their dendritic branches were relatively straight and formed acute angles (10–45°) at their branching points. These cells were few in number (approximately 8% of all medium-sized cells studied) and did not resemble any reported previously in cats. Thus, a variety of morphological types of retinal ganglion cells projected to the SC. Of these, the symmetrical and asymmetrical δ-like cells appeared to correspond to the directionally selective type described in the ground squirrel (Michael, C.R. [1968] J. Neurophysiol. 31:257–267) and reported in the rabbit retina. J. Comp. Neurol. 396:105–120, 1998. © 1998 Wiley-Liss, Inc.     

Depletion of cortical target induced by prenatal ionizing irradiation: effects on the lateral geniculate nucleus and on the retinofugal pathways.

Studies using neonatal surgical lesions to reduce the target area of the retina have supported the idea that developing axons show only a limited specificity in their targeting. This investigation tested whether retinogeniculate axons adjust for partial target depletion by repositioning of axons. We used adult Swiss mice exposed to gamma rays at the time when layer IV cells are generated in the ventricular zone (16 days of gestation). Nissl-stained brain sections were used for histological analyses in thalamus and cortex. Retinal ganglion cells were backfilled from the optic tract with horseradish peroxidase. Intraocular injections of horseradish peroxidase were used to study the retinal projections. In the posterior cortex there was a nearly complete absence of layer IV. The irradiated animals showed a 75% reduction of the dorsal lateral geniculate nucleus. The ventral division, superior colliculus, and other visually related nuclei were not affected. The loss in the ganglion cells (15.7%) was significant but clearly smaller than that observed in the dorsal lateral geniculate nucleus (75%). Therefore, the shrinkage of the dorsal lateral geniculate nucleus led to a reduction in the area available for retinal projections. Despite partial target loss, pattern of retinal projections did not differ from that of the controls. The effect on the dorsal lateral geniculate nucleus is discussed in the light of differences between prenatal and neonatal damage of the presumptive visual cortex. The absence of aberrant retinal projections suggests that repositioning of axons is not the first mechanism employed by retinal axons to match connections in numerically disparate populations.     

Neurogenetic gradients in the hamster visual pathway

The dorsal lateral geniculate nucleus, suprachiasmatic nucleus and superior colliculus of the hamster were examined autoradiographically after administration of [3H]thymidine for the presence of spatiotemporal gradients of neuron production and for the relationship between neuron cell body size and birthdate. The dorsal lateral geniculate nucleus had a dorsolateral-to-ventromedial (superficial-to-deep) gradient of neuron production, the suprachiasmatic nucleus had a caudoventral to rostrodorsal gradient, and the superior colliculus had a complex laminar gradient. In the lateral geniculate nucleus and in the superior colliculus, labeled neurons were typically larger than unlabeled neurons at early stages and unlabeled neurons were typically larger than labeled neurons at late stages; however, variation in neuron size does not account for the neurogenetic gradients in hamsters.     

Overlapping Ipsilateral and Contralateral Retinal Projections to the Lateral Geniculate Nucleus and Superior Colliculus in the Cat: A Retrograde Triple Labelling Study

To analyze the relative proportion and distribution of retinal ganglion cells projecting ipsilaterally and contralaterally in the cat, large injections of the fluorescent tracers Fluoro Gold, Fast Blue, and Diamidino Yellow were made in the main layers of the lateral geniculate nucleus (LGN) and superior colliculus (SC). One tracer was injected in both the LGN and SC on one side, and the other two tracers were injected contralaterally, in the LGN and SC, respectively; labelled ganglion cells were charted on retinal whole mounts. Ganglion cells labelled from the LGN and SC were highly intermingled in both the ipsilateral and contralateral retinae. The adopted combinations of tracers allowed the detection of cells double labelled from the SC and LGN, supporting the occurrence of branched retino-thalamic axons to the SC. About one-fourth of the ganglion cells labelled from the LGN and SC was located in the eye ipsilateral to the injection. Retrograde labelling from the ipsilateral side was almost entirely confined to the temporal hemiretina. In the contralateral eye, labelled cells were mainly concentrated in the nasal hemiretina, but more than 10% were also detected in the temporal half of the retina. In the latter area, cells displaying the entire range of sizes of the retinal ganglion cells, labelled from the contralateral LGN and SC, were found throughout the entire hemiretina. However, more than 50% of such “wrong” projecting cells were grouped in a strip of 2 mm closest to the naso-temporal division. Control experiments, in which the tracers injections were restricted to the rostral and dorsal portions of the LGN to avoid optic tract contamination, consistently confirmed the occurrence and distribution of the “wrong” projecting cells in the temporal hemiretina. Thus, these latter cells are not grouped in a central strip, where ganglion cells would have the same chance of projecting to the same or to the opposite side, and sparsely distributed in the temporal periphery, as previously believed. Instead, the present findings indicate that the retinal ganglion cells of origin of contralateral projections are distributed more in a continuum, with a naso-temporal gradient of density, across the temporal hemiretina.