Structural basis of the functional development of the retina in the cichlid Tilapia leucosticta (teleostei)

Development ◽  
1975 ◽  
Vol 33 (1) ◽  
pp. 243-257
Author(s):  
Gerd Grün

The differentiation of retinal cells has been studied with special reference to the formation of functionally important structures. Three phases could be revealed: from day 3 to day 6 retinal cells in the mostly advanced central part show signs of general cell differentiation (formation of ribosomes, endoplasmic reticulum, mitochondria). In the second phase from day 6 to day 9 characteristic nerve cell structures appear (neurites, dendrites, synapses, receptor outer and inner segments). In the last phase from day 9 to day 12 these special structures attain their final, mature appearance, synapses seem ready for function, dendritic invaginations and synaptic ribbons are formed, twin cones become arranged in mosaic patterns. This developmental order conforms to a gradient running from the ganglion cells to the receptors. Neurites and dendrites appear in the ganglion cells on day 3, in the intermediate neuron layer not before day 4. The horizontal cells are the last ones to differentiate out of the intermediate neurons. The inner plexiform layer synapses are structurally mature before those from the outer plexiform layer. The receptor inner and outer segments differentiate from the 5th day up to the time the young fish is able to see (day 13). The last structures to appear are dendritic invaginations and synaptic ribbons in the receptor terminals, and the twin cone mosaic. It is assumed that the ability to see is achieved only when these structures have been formed.

Development ◽  
1975 ◽  
Vol 33 (4) ◽  
pp. 915-940
Author(s):  
S. H. Chung ◽  
R. Victoria Stirling ◽  
R. M. Gaze

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.


1992 ◽  
Vol 9 (3-4) ◽  
pp. 279-290 ◽  
Author(s):  
Dennis M. Dacey ◽  
Sarah Brace

AbstractIntracellular injections of Neurobiotin were used to determine whether the major ganglion cell classes of the macaque monkey retina, the magnocellular-projecting parasol, and the parvocellular-projecting midget cells showed evidence of cellular coupling similar to that recently described for cat retinal ganglion cells. Ganglion cells were labeled with the fluorescent dye acridine orange in an in vitro, isolated retina preparation and were selectively targeted for intracellular injection under direct microscopic control. The macaque midget cells, like the beta cells of the cat's retina, showed no evidence of tracer coupling when injected with Neurobiotin. By contrast, Neurobiotin-filled parasol cells, like cat alpha cells, showed a distinct pattern of tracer coupling to each other (homotypic coupling) and to amacrine cells (heterotypic coupling).In instances of homotypic coupling, the injected parasol cell was surrounded by a regular array of 3–6 neighboring parasol cells. The somata and proximal dendrites of these tracer-coupled cells were lightly labeled and appeared to costratify with the injected cell. Analysis of the nearest-neighbor distances for the parasol cell clusters showed that dendritic-field overlap remained constant as dendritic-field size increased from 100–400 μm in diameter.At least two amacrine cell types showed tracer coupling to parasol cells. One amacrine type had a small soma and thin, sparsely branching dendrites that extended for 1–2 mm in the inner plexiform layer. A second amacrine type had a relatively large soma, thick main dendrites, and distinct, axon-like processes that extended for at least 2–3 mm in the inner plexiform layer. The main dendrites of the large amacrine cells were closely apposed to the dendrites of parasol cells and may be the site of Neurobiotin transfer between the two cell types. We suggest that the tracer coupling between neighboring parasol cells takes place indirectly via the dendrites of the large amacrine cells and provides a mechanism, absent in midget cells, for increasing parasol cell receptive-field size and luminance contrast sensitivity.


2001 ◽  
Vol 18 (4) ◽  
pp. 559-570 ◽  
Author(s):  
B.E. REESE ◽  
M.A. RAVEN ◽  
K.A. GIANNOTTI ◽  
P.T. JOHNSON

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.


2001 ◽  
Vol 18 (5) ◽  
pp. 781-787 ◽  
Author(s):  
TATIANA GRÜNDER ◽  
KONRAD KOHLER ◽  
ELKE GUENTHER

To determine how a progressive loss of photoreceptor cells and the concomitant loss of glutamatergic input to second-order neurons can affect inner-retinal signaling, glutamate receptor expression was analyzed in the Royal College of Surgeons (RCS) rat, an animal model of retinitis pigmentosa. Immunohistochemistry was performed on retinal sections of RCS rats and congenic controls between postnatal (P) day 3 and the aged adult (up to P350) using specific antibodies against N-methyl-D-aspartate (NMDA) subunits. All NMDA subunits (NR1, NR2A–2D) were expressed in control and dystrophic retinas at all ages, and distinct patterns of labeling were found in horizontal cells, subpopulations of amacrine cells and ganglion cells, as well as in the outer and inner plexiform layer (IPL). NR1 immunoreactivity in the inner plexiform layer of adult control retinas was concentrated in two distinct bands, indicating a synaptic localization of NMDA receptors in the OFF and ON signal pathways. In the RCS retina, these bands of NR1 immunoreactivity in the IPL were much weaker in animals older than P40. In parallel, NR2B immunoreactivity in the outer plexiform layer (OPL) of RCS rats was always reduced compared to controls and vanished between P40 and P120. The most striking alteration observed in the degenerating retina, however, was a strong expression of NR1 immunoreactivity in Müller cell processes in the inner retina which was not observed in control animals and which was present prior to any visible sign of photoreceptor degeneration. The results suggest functional changes in glutamatergic receptor signaling in the dystrophic retina and a possible involvement of Müller cells in early processes of this disease.


1985 ◽  
Vol 224 (1237) ◽  
pp. 475-488 ◽  

When cat retina is incubated in vitro with the fluorescent dye, 4',6- diamidino-2-phenyl-indole (DAPI), a uniform population of neurons is brightly labelled at the inner border of the inner nuclear layer. The dendritic morphology of the DAPI-labelled cells was defined by iontophoretic injection of Lucifer yellow under direct microscopic control: all the filled cells had the narrow-field bistratified morphology that is distinctive of the A ll amacrine cells previously described from Golgistained retinae. Although the A ll amacrines are principal interneurons in the rod-signal pathway, their density distribution does not follow the topography of the rod receptors, but peaks in the central area like the cone receptors and the ganglion cells. There are some 512000 A ll amacrines in the cat retina and their density ranges from 500 cells per square millimetre at the superior margin to 5300 cells per square millimetre in the centre (retinal area is 450 mm2). The isodensity contours are kite-shaped, particularly at intermediate densities, with a horizontal elongation towards nasal retina. The cell body size and the dendritic dimensions of A ll amacrines increase with decreasing cell density. The lobular dendrites in sublamina a of the inner plexiform layer span a restricted field of 16—45 pm diameter, while the arboreal dendrites in sublamina b form a varicose tree of 18—95 pm diameter. The dendritic field coverage of the lobular appendages is close to 1.0 (+ 0.2) at all eccentricities whereas the coverage of the arboreal dendrites doubles within the first 1.5 mm and then remains constant at 3.8 ( + 0.7) throughout the periphery.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Thomas A Ray ◽  
Suva Roy ◽  
Christopher Kozlowski ◽  
Jingjing Wang ◽  
Jon Cafaro ◽  
...  

A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers.


2002 ◽  
Vol 88 (2) ◽  
pp. 1026-1039 ◽  
Author(s):  
Steven F. Stasheff ◽  
Richard H. Masland

We recorded from on-off direction-selective ganglion cells (DS cells) in the rabbit retina to investigate in detail the inhibition that contributes to direction selectivity in these cells. Using paired stimuli moving sequentially across the cells' receptive fields in the preferred direction, we directly confirmed the prediction of Wyatt and Daw (1975) that a wave of inhibition accompanies any moving excitatory stimulus on its null side, at a fixed spatial offset. Varying the interstimulus distance, stimulus size, luminance, and speed yielded a spatiotemporal map of the strength of inhibition within this region. This “null” inhibition was maximal at an intermediate distance behind a moving stimulus: ½ to 1½ times the width of the receptive field. The strength of inhibition depended more on the distance behind the stimulus than on stimulus speed, and the inhibition often lasted 1–2 s. These spatial and temporal parameters appear to account for the known spatial frequency and velocity tuning of on-off DS cells to drifting contrast gratings. Stimuli that elicit distinct onand off responses to leading and trailing edges revealed that an excitatory response of either polarity could inhibit a subsequent response of either polarity. For example, an offresponse inhibited either an on or off response of a subsequent stimulus. This inhibition apparently is conferred by a neural element or network spanning the on andoff sublayers of the inner plexiform layer, such as a multistratified amacrine cell. Trials using a stationary flashing spot as a probe demonstrated that the total amount of inhibition conferred on the DS cell was equivalent for stimuli moving in either the null or preferred direction. Apparently the cell does not act as a classic “integrate and fire” neuron, summing all inputs at the soma. Rather, computation of stimulus direction likely involves interactions between excitatory and inhibitory inputs in local regions of the dendrites.


1997 ◽  
Vol 14 (6) ◽  
pp. 1109-1127 ◽  
Author(s):  
K. M. Shamim ◽  
F. Scalia ◽  
P. Tóth ◽  
J. E. Cook

AbstractPopulation-based studies of ganglion cells in retinal flatmounts have helped to reveal some of their natural types in mammals, teleost fish and, recently, the aquatic mesobatrachian frog Xenopus laevis. Here, ganglion cells of the semiterrestrial neobatrachian frogs Rana esculenta and Rana pipiens have been studied similarly. Ganglion cells with large somata and thick dendrites could again be divided into three mosaic-forming types with distinctive stratification patterns. Cell dimensions correlated inversely with density, being smallest in the visual streak. Cells of the αa mosaic (<0.2% of all ganglion cells) had the largest somata at each location (often displaced) and their trees were confined to one shallow plane within sublamina a of the inner plexiform layer. In regions of high regularity, many trees were symmetric. Elsewhere, asymmetric, irregular trees predominated and their dendrites, although sparsely branched, achieved consistent coverage by intersecting in complex ways. Cells of the αab mosaic were more numerous (≈0.7%) and had large somata, smaller (but still large) trees, and dendrites that branched extensively in two separate shallow planes in sublaminae a and b. The subtrees did not always match in symmetry, and each subtree tessellated independently with its neighbors. Cells of the αc mosaic (≈0.1%) had large, orthotopic somata and large, sparse trees (often asymmetric and irregular) close to the ganglion cell layer. Nearest-neighbor analyses and spatial correlograms confirmed that each mosaic was regular and independent. Densities, proportions, sizes, and mosaic statistics are tabulated for all three types, which are compared with types defined by size and symmetry in R. pipiens, by discriminant analysis in R. temporaria, by physiological response in both, and by mosaic analysis in Xenopus and several teleosts. The variable stratification of these otherwise similar types across species is consistent with other evidence that stratification may be determined, in part, by functional interactions.


PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5646 ◽  
Author(s):  
Alexandra H. Ranski ◽  
Ashley C. Kramer ◽  
Gregory W. Morgan ◽  
Jennifer L. Perez ◽  
Ryan Thummel

Müller glia in the zebrafish retina respond to retinal damage by re-entering the cell cycle, which generates large numbers of retinal progenitors that ultimately replace the lost neurons. In this study we compared the regenerative outcomes of adult zebrafish exposed to one round of phototoxic treatment with adult zebrafish exposed to six consecutive rounds of phototoxic treatment. We observed that Müller glia continued to re-enter the cell cycle to produce clusters of retinal progenitors in zebrafish exposed to multiple rounds of phototoxic light. Some abnormalities were noted, however. First, we found that retinas exposed to multiple rounds of damage exhibited a greater loss of photoreceptors at 36 hours of light damage than retinas that were exposed to their first round of light damage. In addition, we found that Müller glia appeared to have an increase in the acute gliotic response in retinas exposed to multiple rounds of light treatment. This was evidenced by cellular hypertrophy, changes in GFAP cellular localization, and transient increases in stat3 and gfap expression. Finally, following the sixth round of phototoxic lesion, we observed a significant increase in mis-localized HuC/D-positive amacrine and ganglion cells in the inner plexiform layer and outer retina, and a decreased number of regenerated blue cone photoreceptors. These data add to recent findings that retinal regeneration in adult zebrafish occurs concomitant with Müller glia reactivity and can result in the generation of aberrant neurons. These data are also the first to demonstrate that Müller glia appear to modify their phenotype in response to multiple rounds of phototoxic lesion, exhibiting an increase in acute gliosis while maintaining a remarkable capacity for long-term regeneration of photoreceptors.


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