Neural differentiation in the retina of the larval sea lamprey (Petromyzon marinus)

1989 ◽  
Vol 3 (3) ◽  
pp. 241-248 ◽  
Author(s):  
Kalman Rubinson ◽  
Hilary Cain

AbstractThe peripheral retina of the sea lamprey develops in a 5-year-long process in which only certain neurons differentiate each year. The growth of cell layers, the differentiation of the neurons, and the morphology of their dendrites and axons were studied with normal, HRP, and Golgi preparations. Ganglion cells are differentiated in 3-year-old larvae, amacrine and horizontal cells in 4-year-old larvae, photoreceptor cells in stage I transformers, and bipolar cells in stage III transformers. Each new development is expressed as a radial gradient of differentiation. As a result of this protracted and stepped process, lamprey retinal neurons, particularly ganglion cells, differentiate in the absence of other cells to which they will ultimately be connected and may express their individual genetic programs more fully than in other vertebrate retinas. This could account for the unusual relationship of the ganglion cell, inner plexiform, and optic nerve layers and for the very high ratio of displaced to orthotopic ganglion cells.

1994 ◽  
Vol 11 (2) ◽  
pp. 379-387 ◽  
Author(s):  
Elena V. Grigorenko ◽  
Hermes H. Yeh

AbstractThis study profiled the expression of the family of GABAA receptor β-subunits in the adult rat retina. Using a combination of reverse transcriptase reaction followed by polymerase chain reaction (RT-PCR) with gene-specific primers, the expression of mRNAs encoding the β1, β2, and β3 subunits was first examined in the intact retina and then in separated retinal nuclear layers. However, it was found that a critical analysis. had to be carried out at the level of the single cell in order to resolve the differential patterns of expression among the retinal cell types. When cells were isolated and identified following acute dissociation, RT-PCR revealed that individual rod photoreceptor cells expressed consistently the β1 and β2 messages while the bipolar cells expressed the β1 and β3 messages. Ganglion cells displayed considerable variability in β-subunit expression, perhaps reflecting their functional and morphological heterogeneity in the retina. In contrast, the nonneuronal Mueller cells did not express any of the β-subunit messages. These results indicate that the expression of GABAA receptor subunits is cell-type dependent. Furthermore, as the expression of other families of GABAA receptor subunits are profiled and the patterns of subunit assembly are better understood, our results raise the possibility that GABAA receptors with different subunit compositions can be expected to be coexpressed within a single retinal neuron.


2020 ◽  
Author(s):  
Emily M. Dong ◽  
W. Ted Allison

SUMMARYHagfish eyes are markedly basic compared to the eyes of other vertebrates, lacking a pigmented epithelium, a lens, and a retinal architecture built of three cell layers – the photoreceptors, interneurons & ganglion cells. Concomitant with hagfish belonging to the earliest-branching vertebrate group (the jawless Agnathans), this lack of derived characters has prompted competing interpretations that hagfish eyes represent either a transitional form in the early evolution of vertebrate vision, or a regression from a previously elaborate organ. Here we show the hagfish retina is not extensively degenerating during its ontogeny, but instead grows throughout life via a recognizable Pax6+ ciliary marginal zone. The retina has a distinct layer of photoreceptor cells that appear to homogeneously express a single opsin of the rh1 rod opsin class. The epithelium that encompasses these photoreceptors is striking because it lacks the melanin pigment that is universally associated with animal vision; notwithstanding, we suggest this epithelium is a homolog of gnathosome Retinal Pigment Epithelium (RPE) based on its robust expression of RPE65 and its engulfment of photoreceptor outer segments. We infer that the hagfish retina is not entirely rudimentary in its wiring, despite lacking a morphologically distinct layer of interneurons: multiple populations of cells exist in the hagfish inner retina that differentially express markers of vertebrate retinal interneurons. Overall, these data clarify Agnathan retinal homologies, reveal characters that now appear to be ubiquitous across the eyes of vertebrates, and refine interpretations of early vertebrate visual system evolution.HIGHLIGHTSHagfish eyes are degenerate but not degenerating, i.e. rudimentary but growingRetinal interneurons discovered implying ancestral hagfish had derived retinas & visionDespite lacking pigment, a Retinal Pigmented Epithelium homolog functions in hagfishRevised synapomorphies illuminate the dimly lit origins of vertebrate eye evolutionGRAPHICAL ABSTRACT


2012 ◽  
Vol 29 (3) ◽  
pp. 157-168 ◽  
Author(s):  
CARLA J. ABBOTT ◽  
KUMIKO A. PERCIVAL ◽  
PAUL R. MARTIN ◽  
ULRIKE GRÜNERT

AbstractRetinal ganglion cells receive excitatory synapses from bipolar cells and inhibitory synapses from amacrine cells. Previous studies in primate suggest that the strength of inhibitory amacrine input is greater to cells in peripheral retina than to foveal (central) cells. A comprehensive study of a large number of ganglion cells at different eccentricities, however, is still lacking. Here, we compared the amacrine and bipolar input to midget and parasol ganglion cells in central and peripheral retina of marmosets (Callithrix jacchus). Ganglion cells were labeled by retrograde filling from the lateral geniculate nucleus or by intracellular injection. Presumed amacrine input was identified with antibodies against gephyrin; presumed bipolar input was identified with antibodies against the GluR4 subunit of the AMPA receptor. In vertical sections, about 40% of gephyrin immunoreactive (IR) puncta were colocalized with GABAA receptor subunits, whereas immunoreactivity for gephyrin and GluR4 was found at distinct sets of puncta. The density of gephyrin IR puncta associated with ganglion cell dendrites was comparable for midget and parasol cells at all eccentricities studied (up to 2 mm or about 16 degrees of visual angle for midget cells and up to 10 mm or >80 degrees of visual angle for parasol cells). In central retina, the densities of gephyrin IR and GluR4 IR puncta associated with the dendrites of midget and parasol cells are comparable, but the average density of GluR4 IR puncta decreased slightly in peripheral parasol cells. These anatomical results indicate that the ratio of amacrine to bipolar input does not account for the distinct functional properties of parasol and midget cells or for functional differences between cells of the same type in central and peripheral retina.


1991 ◽  
Vol 6 (3) ◽  
pp. 229-238 ◽  
Author(s):  
Thomas E. Hughes ◽  
Ulrike Grönert ◽  
Harvey J. Karten

AbstractGamma-aminobutyric acid (GABA) is an inhibitory neurotransmitter used by many neurons of the mammalian retina. To identify the synaptic targets of these cells, we undertook an immunohistochemical study with a monoclonal antibody that recognizes the GABAAreceptors (62−3G1, generously donated by A. de Blas). This antibody labels the somata of at least one group of amacrine cells in the inner nuclear layer. It also labels two groups of somata in the ganglion cell layer: one small and the other much larger. The small cells are likely to be displaced amacrine cells based on their size, although some could be gamma ganglion cells. The much larger receptor-positive cells are clearly ganglion cells, based both on their size and the antibody labeling of the initial portion of their axon. In the peripheral retina, the size of these large somata suggests that many are beta ganglion cells. However, at any point across the retina the density of these cells never exceeded 50% of the density of beta cells as a whole.The antibody also labels a dense plexus of processes that extends throughout the inner plexiform layer (IPL), with a marked concentration in the inner third of the layer. This is the portion of the IPL in which the rod bipolar cells terminate. It is difficult to recognize processes of individual cells in the IPL, so retinae were dissociated. The rod bipolar cells were identified by protein kinase C immunoreactivity (Negishi et al., 1988; Karschin & Wässle, 1990). They were not labeled by the GABAAreceptor antibody. This is surprising in light of tight-seal, whole cell voltage-clamp recordings that have shown that the rod bipolars express functional GABAAreceptors. One possible explanation is that the antibody recognizes only a subset of the GABAAreceptors.


2018 ◽  
Author(s):  
Lauren E Wool ◽  
Orin S Packer ◽  
Qasim Zaidi ◽  
Dennis M Dacey

AbstractIn the trichromatic primate retina, the ‘midget’ retinal ganglion cell is the classical substrate for red-green color signaling, with a circuitry that enables antagonistic responses between long (L)- and medium (M)-wavelength sensitive cone inputs. Previous physiological studies show that some OFF midget ganglion cells may receive sparse input from short (S)-wavelength sensitive cones, but the effect of S-cone inputs on the chromatic tuning properties of such cells has been unexplored. Moreover, anatomical evidence for a synaptic pathway from S cones to OFF midget ganglion cells through OFF-midget bipolar cells remains ambiguous. In this study we address both questions for the macaque monkey retina. First, we used serial block-face electron microscopy (SBEM) to show that every S-cone in the parafoveal retina synapses principally with a single OFF-midget bipolar cell which in turn forms a private-line connection with an OFF midget ganglion cell. Second, we used patch electrophysiology to characterize the chromatic tuning of OFF midget ganglion cells in the near peripheral retina that receive combined input from L, M and S cones. These ‘S-OFF’ midget cells have a characteristic S-cone spatial signature, but demonstrate heterogeneous color properties due to variable strength of L, M, and S cone input across the receptive field. Together these findings strongly support the hypothesis that the OFF midget pathway is the major conduit for S-OFF signals in primate retina, and redefines the pathway as a chromatically complex substrate that encodes color signals beyond the classically recognized L vs. M and S vs. L+M cardinal mechanisms.Significance statementThe first step of color processing in the visual pathway of primates occurs when signals from short- (S), middle- (M) and long- (L) wavelength sensitive cone types interact antagonistically within the retinal circuitry to create color-opponent pathways. The midget (L vs. M or ‘red-green’) and small bistratified (S vs. L+M, or ‘blue-yellow’) appear to provide the physiological origin of the cardinal axes of human color vision. Here we confirm the presence of an additional S-OFF midget circuit in the macaque monkey fovea with scanning block-face electron microscopy (SBEM) and show physiologically that a subpopulation of S-OFF midget cells combine S, L and M cone inputs along non-cardinal directions of color space, expanding the retinal role in color coding.


2021 ◽  
Vol 288 (1942) ◽  
pp. 20202187
Author(s):  
Emily M. Dong ◽  
W. Ted Allison

Hagfish eyes are markedly basic compared to the eyes of other vertebrates, lacking a pigmented epithelium, a lens and a retinal architecture built of three cell layers: the photoreceptors, interneurons and ganglion cells. Concomitant with hagfish belonging to the earliest-branching vertebrate group (the jawless Agnathans), this lack of derived characters has prompted competing interpretations that hagfish eyes represent either a transitional form in the early evolution of vertebrate vision, or a regression from a previously elaborate organ. Here, we show the hagfish retina is not extensively degenerating during its ontogeny, but instead grows throughout life via a recognizable PAX6 + ciliary marginal zone. The retina has a distinct layer of photoreceptor cells that appear to homogeneously express a single opsin of the RH1 rod opsin class. The epithelium that encompasses these photoreceptors is striking because it lacks the melanin pigment that is universally associated with animal vision; notwithstanding, we suggest this epithelium is a homologue of gnathosome retinal pigment epithelium (RPE) based on its robust expression of RPE65 and its engulfment of photoreceptor outer segments. We infer that the hagfish retina is not entirely rudimentary in its wiring, despite lacking a morphologically distinct layer of interneurons: multiple populations of cells exist in the hagfish inner retina and subsets of these express markers of vertebrate retinal interneurons. Overall, these data clarify Agnathan retinal homologies, reveal characters that now appear to be ubiquitous across the eyes of vertebrates, and refine interpretations of early vertebrate visual system evolution.


2021 ◽  
Vol 14 ◽  
Author(s):  
Jinae N. Roa ◽  
Yuliang Ma ◽  
Zbigniew Mikulski ◽  
Qianlan Xu ◽  
Ronit Ilouz ◽  
...  

Protein kinase A (PKA) signaling is essential for numerous processes but the subcellular localization of specific PKA regulatory (R) and catalytic (C) subunits has yet to be explored comprehensively. Additionally, the localization of the Cβ subunit has never been spatially mapped in any tissue even though ∼50% of PKA signaling in neuronal tissues is thought to be mediated by Cβ. Here we used human retina with its highly specialized neurons as a window into PKA signaling in the brain and characterized localization of PKA Cα, Cβ, RIIα, and RIIβ subunits. We found that each subunit presented a distinct localization pattern. Cα and Cβ were localized in all cell layers (photoreceptors, interneurons, retinal ganglion cells), while RIIα and RIIβ were selectively enriched in photoreceptor cells where both showed distinct patterns of co-localization with Cα but not Cβ. Only Cα was observed in photoreceptor outer segments and at the base of the connecting cilium. Cβ in turn, was highly enriched in mitochondria and was especially prominent in the ellipsoid of cone cells. Further investigation of Cβ using RNA BaseScope technology showed that two Cβ splice variants (Cβ4 and Cβ4ab) likely code for the mitochondrial Cβ proteins. Overall, our data indicates that PKA Cα, Cβ, RIIα, and RIIβ subunits are differentially localized and are likely functionally non-redundant in the human retina. Furthermore, Cβ is potentially important for mitochondrial-associated neurodegenerative diseases previously linked to PKA dysfunction.


1996 ◽  
Vol 270 (6) ◽  
pp. C1807-C1814 ◽  
Author(s):  
L. Liu ◽  
S. A. Simon

Nicotine and capsaicin produce many similar physiological responses that include pain, irritation, and vasodilation. To determine whether neuronal nicotine acetylcholine receptors (nAChR) are present on capsaicin-sensitive neurons, whole cell patch-clamp recordings were performed on rat trigeminal ganglion cells. It was found that approximately 20% of the total number of neurons tested was activated by both 100 microM nicotine and 1 nM capsaicin. Other subsets of neurons were activated by only one of these compounds, whereas a fourth subset was not activated by either compound. At -60 mV, the magnitude of the capsaicin-activated currents was about three times larger than the magnitude of the nicotine-activated currents. The current-voltage relationship of the nAChR exhibited marked rectification, such that for voltages > or = 0 mV the current was essentially zero. In contrast, the current-voltage relationship of the capsaicin-activated current was ohmic from +/- 60 mV. These data indicate the existence of subsets of capsaicin-sensitive afferent neurons.


2017 ◽  
Vol 89 (2) ◽  
pp. 84-103 ◽  
Author(s):  
Heidrun Kuhrt ◽  
Andreas Bringmann ◽  
Wolfgang Härtig ◽  
Gudrun Wibbelt ◽  
Leo Peichl ◽  
...  

Elephants are precocial mammals that are relatively mature as newborns and mobile shortly after birth. To determine whether the retina of newborn elephants is capable of supporting the mobility of elephant calves, we compared the retinal structures of 2 newborn elephants (1 African and 1 Asian) and 2 adult animals of both species by immunohistochemical and morphometric methods. For the first time, we present here a comprehensive qualitative and quantitative characterization of the cellular composition of the newborn and the adult retinas of 2 elephant species. We found that the retina of elephants is relatively mature at birth. All retinal layers were well discernible, and various retinal cell types were detected in the newborns, including Müller glial cells (expressing glutamine synthetase and cellular retinal binding protein; CRALBP), cone photoreceptors (expressing S-opsin or M/L-opsin), protein kinase Cα-expressing bipolar cells, tyrosine hydroxylase-, choline acetyltransferase (ChAT)-, calbindin-, and calretinin-expressing amacrine cells, and calbindin-expressing horizontal cells. The retina of newborn elephants contains discrete horizontal cells which coexpress ChAT, calbindin, and calretinin. While the overall structure of the retina is very similar between newborn and adult elephants, various parameters change after birth. The postnatal thickening of the retinal ganglion cell axons and the increase in ganglion cell soma size are explained by the increase in body size after birth, and the decreases in the densities of neuronal and glial cells are explained by the postnatal expansion of the retinal surface area. The expression of glutamine synthetase and CRALBP in the Müller cells of newborn elephants suggests that the cells are already capable of supporting the activities of photoreceptors and neurons. As a peculiarity, the elephant retina contains both normally located and displaced giant ganglion cells, with single cells reaching a diameter of more than 50 µm in adults and therefore being almost in the range of giant retinal ganglion cells found in aquatic mammals. Some of these ganglion cells are displaced into the inner nuclear layer, a unique feature of terrestrial mammals. For the first time, we describe here the occurrence of many bistratified rod bipolar cells in the elephant retina. These bistratified bipolar cells may improve nocturnal contrast perception in elephants given their arrhythmic lifestyle.


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.


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