Displaced Ganglion Cells Research Articles

Long-term survival of centrally projecting axons in the optic nerve of the frog following destruction of the retina.

A significant number of unmyelinated axons and their synaptic endings in the frog, Rana pipiens, were found to retain a normal morphology long after separation from their cell bodies. At the end of various survival periods following unilateral removal of the retina, horseradish peroxidase (HRP) was administered to the optic nerve stump by a fiber-filling method. In frogs maintained at 20 degrees C, unmyelinated optic nerve axons conducted HRP from the site of application in the orbit to layers A, C, and E of the contralateral optic tectum, even though their retinas had been removed up to 69 days earlier. Such fiber-filling was absent beyond 19 days in other frogs surviving at 35 degrees C. No labeled fibers were continuous with any intracerebral neurons. The HRP was always localized intraaxonally, and the marked axons and terminals were ultrastructurally normal. Counts of surviving axons from electron micrographs of the optic nerves showed that, at 20 degrees C, more than half of the normal complement of unmyelinated axons disappeared in the first 10 days. All the myelinated axons degenerated during the first 6 weeks survival. However, approximately 55,000 normal-appearing unmyelinated axons (12% of the unmyelinated fiber population) persisted in the optic nerve at 10 weeks following removal of the retina. The survival rate was lower at 35 degrees C. In other frogs, one eye was injected with 3H-leucine to initiate axonal transport into the retinal ganglion cell axons. That eye was removed 48 hours later. Autoradiographic analysis of brain sections of frog surviving an additional 31 to 61 days at 20 degrees C showed strong labeling of the optic tract and layers A, C, and E of the contralateral optic tectum. The absence of displaced ganglion cells that might exist within the optic nerve was verified by other observations. It is hypothesized that the potential shown by frog optic axons for long-term survival in the absence of the cell-body expresses a general property of vertebrate (and invertebrate) axons, rather than a special property of the frog optic nerve.

Displaced ganglion cells and the accessory optic system of pigeon

The central projection and retinal distribution of displace ganglion cells (DGC's) are described for the pigeon. Discrete, localized injections of horseradish peroxidase (HRP) into the nucleus of the basal optic root (nBOR) complex labeled as many as 4,800 DGC's in the contralateral retina. The greatest densities of DGC's were observed in the more peripheral regions of the middle and inferior temporal regions of the retina, with lowest densities occurring in the inferior nasal, red field, and foveal areas. Large HRP injections of the tectal lobes, which did not include the pretectal, accessory optic (nBOR), hypothalamic, or thalamic visual nuclei, labeled only ganglion cells within the ganglion cells layer. An HRP injection centered within the nucleus lentiformis mesencephali, also including portions of the optic tectum and optic tract, labeled only ganglion cells within the ganglion cell layer of the contralateral retina. DGC's thus appear to be the primary, if not exclusive, source of retinal afferents to the nBOR complex in pigeon. The observed retinal distribution of DGC's indicates that the areas of retina with the greatest density of cells in the receptor layer, inner nuclear layer, and ganglion cell layer are relatively devoid of DGC's. Since the nBOR complex projects directly upon the vestibulocerebellum and oculomotor nuclei, DGC's would thus appear to be involved in neural circuits that mediate oculomotor reflexes and visuomotor behavior.

A projection of displaced ganglion cells and giant ganglion cells to the accessory optic nuclei in turtle

The retinal projection to the accessory optic nuclei (AON) of turtles was found to arise from a distinctive set of giant ganglion cells whose dendrites ramify widely in outer portions of the inner plexiform layer. The majority (80%) of these cells had their perikaryon located in the ganglion cell layer, though displaced ganglion cells (DGCs) were also observed. In contrast, the retinal projection to the avian AON has been reported to arise exclusively from DGCs.

Origins of crossed and uncrossed retinal projections in pigmented and albino mice.

The extent of the binocular cortical field in albino mice, as revealed by recording from single cells, was almost normal; although the input from the ipsilateral eye was weaker than normal, most cells were driven from both eyes. By backfilling retinal ganglion cells from one optic tract with horseradish peroxidase we examined the origins of the retinofugal projections. Filled cells ipsilateral to the injected tract were concentrated in a crescent-shaped area bordering the inferior temperal retina. In black mice this area constituted 20% of the total retinal area, in albinos 17%. In black mice we counted nearly 1,000 labeled cells in the ipsilateral retina, or 2.6% of all cells filled in both eyes. Albinos had about one-third fewer filled cells ipsilaterally than black mice. Four percent of all ipsilaterally filled cells in black mice and 8% in albinos were scattered outside of the crescent region. The density of ipsilaterally projecting cells was uniform throughout the crescent region in black mice, but decreased toward the central retina in albinos. In retinas contralateral to the injection up to 39,000 cells were filled-about two-thirds of the cells in the ganglion-cell layer whose cytoplasm contained conspicuous Nissl substance. Depending on classification of unfilled cells as ganglion cells or interneurons, we estimated a total of 48,000 to 65,000 ganglion cells to exist in the retina. The size distribution of ipsilaterally projecting ganglion cells was similar in albinos and normals. Ipsilaterally projecting ganglion cells were on average 1.8-3 times larger in volume than contralaterally projecting ones in both types of mice. Displaced ganglion cells were relatively more common in ipsilateral retinofugal projections: 21% of all ipsilateral ganglion cells were displaced versus less than 1% of all the contralateral ganglion cells in black mice. In albinos only 13% of the ganglion cells in the ipsilateral retina were displaced. The overall reduction in ipsilaterally projecting cells in albinos was reflected twice as much in displaced ganglion cells as in normally placed ones.

Projections of the nucleus of the basal optic root in the pigeon: an autoradiographic and horseradish peroxidase study.

The efferent projections of the nBOR complex, have been studied with both anterograde autoradiographic and retrograde horseradish peroxidase (HRP) techniques. The nBOR complex includes three distinct subdivisions: the nucleus of the basal optic root (nBOR), the nBOR pars dorsalis (nBORd) and the nBOR pars lateralis (nBOR1). Unilateral injections of 3H-leucine or 3H-proline/3H-leucine mixtures into the nBOR complex have demonstrated prominent bilateral projections upon (1) the vestibulocerebellum, (2) the inferior olivary complex, (3) the oculomotor nuclear complex, (4) the nucleus interstitialis, contralateral projections upon (5) the contralateral nBOR complex and ipsilateral projections upon (6) a pretectal nucleus, the nucleus lentiformis mesencephali, pars magnocellularis. Unilateral injections of HRP confined to folia IXc,d and paraflocculus of the cerebellum, the contralateral nBOR complex or the nucleus lentiformis mesencephali resulted in retrograde labeling of predominantly medium and large size cells within the entire nBOR complex. Unilateral injections of HRP within the inferior olive resulted in retrograde labeling of small, spindle-shaped cells within nBOR and nBORd. Unilateral injections of the oculomotor complex which included the trochlear nucleus resulted in retrograde labeling of small cells within the ipsilateral nBORd and predominantly medium and large cells in the contralateral nBOR. The displaced ganglion cells of the retina give rise to a prominent and distinct projection upon the nBOR complex (Karten et al., '77). The nBOR complex in turn projects upon the oculomotor nuclear complex, the nucleus interstitialis and the vestibulocerebellum, regions which have been implicated in oculomotor function. These findings strongly suggest that the displaced ganglion cells and the accessory optic system have a major influence upon oculomotor reflexes including eye and head movements.

A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken

The displaced ganglion cells of Dogiel are a class of retinal ganglion cells whose perikarya are located along the inner margin of the inner nuclear layer. Found in all vertebrate classes, they are particularly conspicuous in avians. Recently, Karten, Fite & Brecha (1977) found that these cells in the pigeon gave rise to a seemingly exclusive projection to the contralateral nucleus of the basal optic root, the major component of the avian accessory optic system. In the present work, the projections of displaced ganglion cells were investigated in hatchling and adult chickens. The cells were found to project to the nucleus of the basal optic root but not to the tectum. Labeled displaced ganglion cells following injections of horseradish peroxidase into the nucleus of the basal optic root were 15 × 20μm in size in both hatchlings and adults. Labeled cells tended to have a higher concentration in the peripheral than in the central retina. Cells were widely but irregularly spaced, with adjacent cells seldom closer than 100 μm. Up to 7700 displaced ganglion cells were labeled in the adult chicken. These results, together with those of Karten et al. (1977) , suggest that in birds, displaced ganglion cells may constitute a unique class of retinal ganglion cells that project exclusively to the nucleus of the basal optic root. In light of the projections of the nucleus of the basal optic root to the oculomotor complex and vestibulocerebellum, the displaced ganglion cells may be an initial link in a visual pathway involved in the control of oculomotor reflexes.

The displaced ganglion cell in the avian retina: developmental and comparative considerations.

Quantitative and qualitative aspects of the retinal displaced ganglion cells (DGC's) were studied in the chick embryo, hatchling and adult, using retrograde labeling techniques. Retrograde axonal transport following discrete injections of horseradish peroxidase into the dorsolateral optic tectum was demonstrated from day 10.5 of incubation. The labeled retinae revealed numerous DGC's at all stages studied, with an average of 1183 cells labeled in 10.5 day embryos and as many as 9500 labeled in hatchlings. These population estimates imply that at least this many DGC's were present at these ages (many cells could have gone unlabeled by our procedures). More localized injections in adults, revealed an average of 2238 cells. In every instance in which orthotopic ganglion cells were labeled, numerous DGC's were similarly labeled. The DGC's were distributed throughout the retinae in embryos and hatchlings, but often tended to be most numerous in the peripapillary regions. In adults, this tendency was even more marked. These results demonstrate that the DGC, has a direct tectal projection in the chicken, in contrast to the almost exclusive, ectomamillary (EM) projection which has been demonstrated in the pigeon. It is speculated that this disparity may be due to species differences, which could be manifested by a dual tectal-EM projection in the chicken. The differential distribution of the DGC in these species (peripheral in the pigeon, peripapillary or panretinal in the chicken) supports this speculation.

Displaced ganglion cells in carp retina revealed by the horseradish peroxidase technique

Displaced ganglion cells were identified in the carp retina by the retrograde axonal transport of horseradish peroxidase injected into the optic tectum. Cells in the ganglion cell layer were all labelled, while in the amacrine cell layer only 1/4000 cells were labelled. Because of such low population, it is unlikely to penetrate displaced ganglion cells by microelectrodes. The present finding suggests that the spiking cells frequently recorded in the inner nuclear layer are genuine amacrine cells.

Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon (Columbia livia).

In the pigeon, the nucleus of the basal optic root, a component of the accessory optic system, projects directly upon the vestibulo-cerebellum. This nucleus receives a prominent projection composed of large-diameter retinal axons, known as the basal optic root. The cells of origin of this tract were identified using horseradish peroxidase (donor:hydrogen-peroxide oxidoreductase, EC 1.11.1.7) as a retrograde marker. Injections of horseradish peroxidase confined primarily to the basal optic root nucleus labeled displaced ganglion cells of the contralateral retina. Cell sizes were 18-30 micronm and the dendrites of these cells were confined to the first stratum of the inner plexiform layer. Approximately 3700 displaced ganglion cells were labeled after injections of horseradish peroxidase into basal optic root. In contrast, no displaced ganglion cells were labeled after injections of horseradish peroxidase into the optic tectum, which labeled only cells in the ganglion cell layer proper. These findings indicate that displaced ganglion cells constitute a unique population of retinal neurons that give rise to a bisynaptic pathway directed to the cerebellum via the nucleus of the basal optic root. These displaced ganglion cells may play a major role inoculomotor reflexes.

Retrograde axonal transport of horseradish peroxidase by ganglion cells of the albino rat retina

After introduction of small amounts of horseradish peroxidase (HRP) into known visual centers of the brain, retinal ganglion cells projecting to these regions were detected by the accumulation of HRP-positive granules in their somata. Control experiments indicated that the HRP-positive granules had reached the ganglion cell somata by retrograde axonal transport, and did not represent blood-borne or endogenous peroxidase. Using this technique, it has been determined that axons of both large and medium-sized neurons in the ganglion cell layer of adult and immature rat retinae terminate in the superior colliculus and lateral geniculate body, and that characteristic displaced ganglion cells with axonal connections to these visual centers occur regularly in these retinae. In addition, certain small cells in the retinal ganglion cell layer are described which may represent glia or interneurons, or ganglion cells which lack the ability to transport peroxidase or which lack central connections to these visual centers of the brain.

Retinal structure in the smooth dogfish, Mustelus canis: general description and light microscopy of giant ganglion cells.

AbstractGiant ganglion cells (GGC) were demonstrated in retinas of adult dogfish by Golgi impregnation, reduced silver and vital methylene blue staining. All GGC have large, flattened perikarya, and dendrites which radiate in a single horizontal plane of the inner synaptic (plexiform) layer. They are identifiable as ganglion cells by their axons, which after a tortuous initial course enter the nerve fiber layer. We divide the GGC into three varieties: (1) ordinary, with perikarya in the layer of ganglion cells and nerve fibers, and with dendrites radiating in the inner (proximal) one‐fourth of the inner synaptic layer; (2) displaced or Dogiel's cells, with perikarya in the amacrine cell layer and dendrites radiating in the outer (distal) one‐fourth of the inner synaptic layer; and (3) intermediate, with both perikarya and dendritic trees at intermediate levels in the inner synaptic layer.Only the ordinary and displaced GGC in the ventral portion of retinas stained with methylene blue were studied in detail. Cells of both types are arranged in irregular patterns with perikarya about 0.8–1.0 mm apart. Dendrites of the ordinary GGC spread within an elliptical field having a major axis of about 1.7 mm (2.0 mm max) and a minor axis of about 1.5 mm (1.7 mm max). The major axis is vertical in the eye. Dendrites of the displaced GGC spread within a circular field having a diameter of about 1.9–2.0 mm (2.2 mm max). Quantitative comparison of the dendritic trees of ordinary and displaced GGC shows that they differ also in details of dendritic morphology, the dendrites of the ordinary GGC being on the average more numerous and highly branched but shorter than those of the displaced GGC. Ordinary and displaced GGC, therefore, comprise distinct populations which must be presumed to differ functionally.For both ordinary and displaced GGC, the dendritic density and, therefore, the total available postsynaptic surface per unit retinal area decline exponentially with distance from the center to the edge of the dendritic tree. In contrast, the sensitivity to light is constant throughout the receptive field centers of comparable diameter which have been analysed in parallel electrophysiological studies. While the diameters of the largest ganglion cell dendritic fields and receptive field centers are similar, therefore, more detailed correlations of structure and function cannot be made at present.

Synaptic connections of the centrifugal fibers in the pigeon retina.

The centrifugal fibers in the pigeon retina end in the inner nuclear layer and form two kinds of terminals, convergent and divergent. In the inner nuclear layer the fibers synapse with amnacrine and displaced ganglion cells. Because of their great number and their even distribution these fibers appear to constitute a system for the localized centrifugal control of the retinal functions.