Early dendritic outgrowth of primate retinal ganglion cells

AbstractThe pattern of dendritic stratification of retinal ganglion cells in the fetal monkey (Macaca mulatta) was examined using horseradish peroxidase and retinal explants. Ganglion cells in the rhesus monkey are born between embryonic day (E) 30–70 (La Vail et al., 1983). At E60, E67, and E68, approximately 50% of all ganglion cells within the central 3.0 mm of the retina had dendritic arbors that were unistratified within the inner plexiform layer (IPL), while the remaining 50% had bistratified arbors. Unistratified cells had relatively flat arbors that ramified within a restricted portion of the IPL. In contrast, bistratified cells had one portion of the arbor that branched in the inner half of the IPL and a second portion that branched in the outer half of the IPL. Relatively few bistratified cells were encountered in the central 1.0 mm of the retina but were more numerous with increasing eccentricity. At E81, E90, and E110, the dendritic arbors of ganglion cells increased in both area and complexity, but occupied a relatively small percentage of the total depth of the IPL. The bistratified cells encountered at these fetal ages were typically located in the far retinal periphery. Between E125-E140, the dendritic arbors of individual ganglion cells increased in area and depth to occupy a greater proportion of the total IPL than at earlier fetal ages.These observations suggest that ganglion cells in the macaque undergo at least three stages of dendritic stratification: (1) an initial period of dendritic growth during which the cells have either unistratified or bistratified dendritic arbors; (2) a loss of the majority of bistratified cells through cell death or remodeling of the arbor; and (3) growth or expansion of the arbor to occupy a greater percentage of the total depth of the IPL. The first two stages are similar to recent observations in the fetal cat (Maslim & Stone, 1988) with the exception that dendritic development in the primate lacks an initial diffuse ingrowth to the IPL. Additionally, primate ganglion cells undergo a third stage of dendritic growth in late fetal development during which the arbor occupies a greater proportion of the depth of the IPL.

Download Full-text

Retinal ganglion cells projecting to the optic tectum and visual thalamus of lizards

Visual Neuroscience ◽

10.1017/s0952523802195034 ◽

2002 ◽

Vol 19 (5) ◽

pp. 575-581 ◽

Cited By ~ 4

Author(s):

ALINO MARTINEZ-MARCOS ◽

ENRIQUE LANUZA ◽

FERNANDO MARTINEZ-GARCIA

Keyword(s):

Ganglion Cell ◽

Retinal Ganglion Cells ◽

Optic Tectum ◽

Ganglion Cells ◽

Plexiform Layer ◽

Cell Types ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Visual Thalamus ◽

Podarcis Hispanica

Retinal ganglion cells projecting to the optic tectum and visual thalamus have been investigated in the lizard, Podarcis hispanica. Injections of biotinylated dextran-amine in the optic tectum reveal seven morphological cell varieties including one displaced ganglion cell type. Injections in the visual thalamus yield similar ganglion cell classes plus four giant ganglion cells, including two displaced ganglion cell types. The present study constitutes the first comparison of tectal versus thalamic ganglion cell types in reptiles. The situation found in lizards is similar to that reported in mammals and birds where some cell types projecting to the thalamus are larger than those projecting to the mesencephalic roof. The presence of giant retino-thalamic ganglion cells with specific dendritic arborizations in sublaminae A and B of the inner plexiform layer suggests that parts of the visual thalamus of lizards could be implicated in movement detection, a role that might be played by the ventral lateral geniculate nucleus, which is involved in our tracer injections.

Download Full-text

Disruption of transient photoreceptor targeting within the inner plexiform layer following early ablation of cholinergic amacrine cells in the ferret

Visual Neuroscience ◽

10.1017/s095252380118507x ◽

2001 ◽

Vol 18 (5) ◽

pp. 741-751 ◽

Cited By ~ 11

Author(s):

P.T. JOHNSON ◽

M.A. RAVEN ◽

B.E. REESE

Keyword(s):

Retinal Ganglion Cells ◽

Amacrine Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Subcutaneous Injections ◽

Cell Processes ◽

Cholinergic Amacrine Cells

Photoreceptors in the ferret's retina have been shown to project transiently to the inner plexiform layer (IPL) prior to their differentiation of an outer segment. On postnatal day 15 (P-15), when this projection achieves maximal density, the photoreceptors projecting into the IPL extend primarily to one of two depths, coincident with the processes of cholinergic amacrine cells. The present study has used an excitotoxic approach employing subcutaneous injections of l-glutamate to ablate these cholinergic amacrine cells on P-7, in order to see whether their elimination alters this targeting of photoreceptor terminals within the IPL. The near-complete elimination of cholinergic amacrine cells at P-15 was confirmed, although the population of retinal ganglion cells was also affected, being depleted by roughly 50%. The rod opsin-immunopositive terminals in such treated ferrets no longer showed a stratified distribution, being found throughout the depth of the IPL, as well as extending into the ganglion cell layer. This effect should not be due to the partial loss of retinal ganglion cells, however, since optic nerve transection at P-2, which eliminates the ganglion cells entirely while leaving the cholinergic amacrine cell population intact, was shown not to affect the stratification pattern of the photoreceptors within the IPL. These results strongly suggest that the targeting of the photoreceptor terminals to discrete strata within the IPL is dependent upon the cholinergic amacrine cell processes.

Download Full-text

Adeno-associated virus-RNAi of GlyRα1 and characterization of its synapse-specific inhibition in OFF alpha transient retinal ganglion cells

Journal of Neurophysiology ◽

10.1152/jn.00505.2014 ◽

2014 ◽

Vol 112 (12) ◽

pp. 3125-3137 ◽

Cited By ~ 5

Author(s):

C. Zhang ◽

S. B. Rompani ◽

B. Roska ◽

M. A. McCall

Keyword(s):

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Glutamate Release ◽

Plexiform Layer ◽

Resting Membrane Potential ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Decay Kinetics ◽

Adeno Associated Virus ◽

Α Subunit

In the central nervous system, inhibition shapes neuronal excitation. In spinal cord glycinergic inhibition predominates, whereas GABAergic inhibition predominates in the brain. The retina uses GABA and glycine in approximately equal proportions. Glycinergic crossover inhibition, initiated in the On retinal pathway, controls glutamate release from presynaptic OFF cone bipolar cells (CBCs) and directly shapes temporal response properties of OFF retinal ganglion cells (RGCs). In the retina, four glycine receptor (GlyR) α-subunit isoforms are expressed in different sublaminae and their synaptic currents differ in decay kinetics. GlyRα1, expressed in both On and Off sublaminae of the inner plexiform layer, could be the glycinergic isoform that mediates On-to-Off crossover inhibition. However, subunit-selective glycine contributions remain unknown because we lack selective antagonists or cell class-specific subunit knockouts. To examine the role of GlyRα1 in direct inhibition in mature RGCs, we used retrogradely transported adeno-associated virus (AAV) that performed RNAi and eliminated almost all glycinergic spontaneous and visually evoked responses in PV5 (OFFαTransient) RGCs. Comparisons of responses in PV5 RGCs infected with AAV-scrambled-short hairpin RNA (shRNA) or AAV- Glra1-shRNA confirm a role for GlyRα1 in crossover inhibition in cone-driven circuits. Our results also define a role for direct GlyRα1 inhibition in setting the resting membrane potential of PV5 RGCs. The absence of GlyRα1 input unmasked a serial and a direct feedforward GABAAergic modulation in PV5 RGCs, reflecting a complex interaction between glycinergic and GABAAergic inhibition.

Download Full-text

Recurrent axon collaterals of intrinsically photosensitive retinal ganglion cells

Visual Neuroscience ◽

10.1017/s0952523813000199 ◽

2013 ◽

Vol 30 (4) ◽

pp. 175-182 ◽

Cited By ~ 45

Author(s):

HANNAH R. JOO ◽

BETH B. PETERSON ◽

DENNIS M. DACEY ◽

SAMER HATTAR ◽

SHIH-KUO CHEN

Keyword(s):

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Plexiform Layer ◽

Small Subset ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Light Responses ◽

Genetic Method ◽

Axon Collaterals ◽

The Brain

AbstractRetinal ganglion cells (RGCs), the output neurons of the retina, have axons that project via the optic nerve to diverse targets in the brain. Typically, RGC axons do not branch before exiting the retina and thus do not provide it with synaptic feedback. Although a small subset of RGCs with intraretinal axon collaterals has been previously observed in human, monkey, cat, and turtle, their function remains unknown. A small, more recently identified population of RGCs expresses the photopigment melanopsin. These intrinsically photosensitive retinal ganglion cells (ipRGCs) transmit an irradiance-coding signal to visual nuclei in the brain, contributing both to image-forming vision and to several nonimage-forming functions, including circadian photoentrainment and the pupillary light reflex. In this study, using melanopsin immunolabeling in monkey and a genetic method to sparsely label the melanopsin cells in mouse, we show that a subgroup of ipRGCs have axons that branch en route to the optic disc, forming intraretinal axon collaterals that terminate in the inner plexiform layer of the retina. The previously described collateral-bearing population identified by intracellular dye injection is anatomically indistinguishable from the collateral-bearing melanopsin cells identified here, suggesting they are a subset of the melanopsin-expressing RGC type and may therefore share its functional properties. Identification of an anatomically distinct subpopulation in mouse, monkey, and human suggests this pathway may be conserved in these and other species (turtle and cat) with intraretinal axon collaterals. We speculate that ipRGC axon collaterals constitute a likely synaptic pathway for feedback of an irradiance signal to modulate retinal light responses.

Download Full-text

Exclusionary dendritic interactions in the retina of the goldfish

Development ◽

10.1242/dev.106.3.589 ◽

1989 ◽

Vol 106 (3) ◽

pp. 589-598 ◽

Cited By ~ 1

Author(s):

P.F. Hitchcock

Keyword(s):

Propidium Iodide ◽

Dendritic Growth ◽

Ganglion Cells ◽

Lucifer Yellow ◽

Plexiform Layer ◽

Inner Plexiform Layer ◽

Branching Pattern ◽

Central Retina ◽

Dendritic Arbors

The retina of the goldfish grows throughout its life, in part, by the addition of new neurons at the margin. New ganglion cells added at the margin tend not to grow their dendritic arbors into the older, central retina. Hitchcock and Easter (J. Neurosci. 6, 1037–1050 (1986)) proposed that the dendrites of the new cells were prevented from extending centrally within the inner plexiform layer by the dendrites of the previous generations of cells. This proposal was tested by first killing existing ganglion cells with a retrogradely transported neurotoxin (propidium iodide; PI), and then observing the orientation and branching pattern of the dendrites of ganglion cells added subsequently at the margin. Dendrites were stained in retinal wholemounts by intracellular injections of Lucifer yellow. The data showed that cells added subsequent to the PI treatment grew their dendritic arbors preferentially toward central retina consistent with the hypothesis. It is concluded that interactions among adjacent ganglion cells regulates dendritic growth.

Download Full-text

Development of cholinergic amacrine cell stratification in the ferret retina and the effects of early excitotoxic ablation

Visual Neuroscience ◽

10.1017/s0952523801184063 ◽

2001 ◽

Vol 18 (4) ◽

pp. 559-570 ◽

Cited By ~ 20

Author(s):

B.E. REESE ◽

M.A. RAVEN ◽

K.A. GIANNOTTI ◽

P.T. JOHNSON

Keyword(s):

Ganglion Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Cell Types ◽

Retinal Cell ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Outer Border ◽

Cholinergic Amacrine Cells

The present study has examined the emergence of cholinergic stratification within the developing inner plexiform layer (IPL), and the effect of ablating the cholinergic amacrine cells on the formation of other stratifications within the IPL. The population of cholinergic amacrine cells in the ferret's retina was identified as early as the day of birth, but their processes did not form discrete strata until the end of the first postnatal week. As development proceeded over the next five postnatal weeks, so the positioning of the cholinergic strata shifted within the IPL toward the outer border, indicative of the greater ingrowth and elaboration of processes within the innermost parts of the IPL. To examine whether these cholinergic strata play an instructive role upon the development of other stratifications which form within the IPL, one-week-old ferrets were treated with l-glutamate in an attempt to ablate the population of cholinergic amacrine cells. Such treatment was shown to be successful, eliminating all of the cholinergic amacrine cells as well as the alpha retinal ganglion cells in the central retina. The remaining ganglion cell classes as well as a few other retinal cell types were partially reduced, while other cell types were not affected, and neither retinal histology nor areal growth was compromised in these ferrets. Despite this early loss of the cholinergic amacrine cells, which are eliminated within 24 h, other stratifications within the IPL formed normally, as they do following early elimination of the entire ganglion cell population. While these cholinergic amacrine cells are present well before other cell types have differentiated, apparently neither they, nor the ganglion cells, play a role in determining the depth of stratification for other retinal cell types.

Download Full-text

The structural and functional development of the retina in larval Xenopus

Development ◽

10.1242/dev.33.4.915 ◽

1975 ◽

Vol 33 (4) ◽

pp. 915-940

Author(s):

S. H. Chung ◽

R. Victoria Stirling ◽

R. M. Gaze

Keyword(s):

Ganglion Cells ◽

Single Layer ◽

Plexiform Layer ◽

Distinct Pattern ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Response Characteristics ◽

Functional Development ◽

New Type ◽

Plexiform Layers

The structural transformations of the larval Xenopus retina at successive stages of development, and concomitant changes in response characteristics of retinal ganglion cells, were studied using histological and electrophysiological techniques. The first sign of visually evoked electrical responses appears at about the time when the ganglion cells spread out into a single layer and shortly after the inner and outer plexiform layers become discernible. Initially giving simple ‘on’ responses, the cells progressively change their response characteristics and become ‘event’ units. Subsequently, ‘dimming’ units can be identified. Throughout larval life, response properties of these two types become more distinct from one another and approximate to those found in the adult. So do the arborization patterns of the dendritic trees of the ganglion cells. Two types of branching patterns are identifiable in Golgi preparations. Around metamorphic climax, a new type of ganglion cell appears, coinciding with the emergence of ‘sustained’ units electrophysiologically. After metamorphosis, the retina still grows both in thickness (mainly in the inner plexiform layer) and diameter. The three unit types change such that they come to show pronounced inhibitory effects from the peripheral visual field on the receptive field and each unit type acquires a distinct pattern of endogenous discharge.

Download Full-text

Morphogenesis of retinal ganglion cells during formation of the fovea in the Rhesus macaque

Visual Neuroscience ◽

10.1017/s095252380000184x ◽

1992 ◽

Vol 9 (6) ◽

pp. 603-616 ◽

Cited By ~ 15

Author(s):

Michael A. Kirby ◽

Thomas C. Steineke

Keyword(s):

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Primary Dendrite ◽

Dendritic Arbor ◽

Inner Plexiform Layer ◽

Comparative Neurology ◽

Retinal Ganglion ◽

Central Retina ◽

The Future ◽

The Mean

AbstractThe morphology of retinal ganglion cells within the central retina during formation of the fovea was examined in retinal explants with horseradish-peroxidase histochemistry. A foveal depression was first apparent in retinal wholemounts at embryonic day 112 (El 12; gestational term is approximately 165 days). At earlier fetal ages, the site of the future fovea was identified by several criteria that included peak density of ganglion cells, lack of blood vessels in the inner retinal layers, arcuate fiber bundles, and the absence of rod outer segments in the photoreceptor layer. Prior to E112, the terminal dendritic arbor of retinal ganglion cells within the central retina extended into the inner plexiform layer and were located directly beneath their somas of origin or at most were slightly displaced from it. For example, at E90 the mean horizontal displacement of the geometric center of the dendritic arbor from the somas of cells within 600 μm of the estimated center of the future fovea was 4.1 μm (S.D. 2.7, range 1.0-10.0, n = 97). Following formation of the foveal depression the dendritic arbors of cells were significantly displaced from their somas. For example, at E138 the mean displacement was 41.2 μm (S.D. 12.2, range 12.0-56.0, n = 97). The displacement of the dendritic arbor which occurred during this period was not accounted for by areal growth of the dendritic arbor, the somas, or the retina, but was produced by the lengthening of the primary dendritic trunk. Moreover, no significant displacement was observed within the remaining 1.5–6.5 mm of the central retina. These observations provide evidence supporting early speculations that the formation of the foveal pit occurs, in part, by the radial migration of ganglion cells from the center of the fovea during its formation. Our analyses suggest that this migration occurs by the lengthening of the primary dendrite presumably by the addition of membrane. This migration is in a direction opposite to the inward movement of photoreceptors that occurs during late fetal and early postnatal periods (Packer et al., 1990, Journal of Comparative Neurology 298, 472–493).

Download Full-text

Differential Distribution of RBPMS in Pig, Rat, and Human Retina after Damage

International Journal of Molecular Sciences ◽

10.3390/ijms21239330 ◽

2020 ◽

Vol 21 (23) ◽

pp. 9330

Author(s):

Xandra Pereiro ◽

Noelia Ruzafa ◽

J. Haritz Urcola ◽

Sansar C. Sharma ◽

Elena Vecino

Keyword(s):

Rna Binding ◽

Ganglion Cells ◽

Mammalian Species ◽

Plexiform Layer ◽

Inner Plexiform Layer ◽

Fiber Layer ◽

Differential Distribution ◽

Hypoxic Conditions ◽

Retinal Explants ◽

Injury Control

RNA binding protein with multiple splicing (RBPMS) is expressed exclusively in retinal ganglion cells (RGCs) in the retina and can label all RGCs in normal retinas of mice, rats, guinea pigs, rabbits, cats, and monkeys, but its function in these cells is not known. As a result of the limited knowledge regarding RBPMS, we analyzed the expression of RBPMS in the retina of different mammalian species (humans, pigs, and rats), in various stages of development (neonatal and adult) and with different levels of injury (control, hypoxia, and organotypic culture or explants). In control conditions, RBPMS was localized in the RGCs somas in the ganglion cell layer, whereas in hypoxic conditions, it was localized in the RGCs dendrites in the inner plexiform layer. Such differential distributions of RBPMS occurred in all analyzed species, and in adult and neonatal retinas. Furthermore, we demonstrate RBPMS localization in the degenerating RGCs axons in the nerve fiber layer of retinal explants. This is the first evidence regarding the possible transport of RBPMS in response to physiological damage in a mammalian retina. Therefore, RBPMS should be further investigated in relation to its role in axonal and dendritic degeneration.

Download Full-text