scholarly journals The visual system of the genetically tractable crustacean Parhyale hawaiensis: diversification of eyes and visual circuits associated with low-resolution vision

2019 ◽  
Author(s):  
Ana Patricia Ramos ◽  
Ola Gustafsson ◽  
Nicolas Labert ◽  
Iris Salecker ◽  
Dan-Eric Nilsson ◽  
...  

AbstractBackgroundArthropod eyes have diversified during evolution to serve multiple needs, such as finding mates, hunting prey, and navigating in complex surroundings under varying light conditions. This diversity is reflected in the optical apparatus, photoreceptors and neural circuits that underpin vision. While this diversity has been extensively documented, our ability to genetically manipulate the visual system to investigate its function is largely limited to a single species, the fruitfly Drosophila melanogaster. Here, we describe the visual system of Parhyale hawaiensis, an amphipod crustacean for which we have established tailored genetic tools.ResultsAdult Parhyale have apposition-type compound eyes made up of ∼50 ommatidia. Each ommatidium contains four photoreceptor cells with large rhabdomeres (R1-4), expected to be sensitive to the polarisation of light, and one photoreceptor cell with a smaller rhabdomere (R5). The two types of photoreceptors express different opsins, belonging to families with distinct wavelength sensitivities. Using the cis.-regulatory regions of opsin genes, we established transgenic reporters expressed in each photoreceptor cell type. Based on these reporters, we show that R1-4 and R5 photoreceptors extend axons to the first optic lobe neuropil, revealing striking differences compared with the photoreceptor projections found in related crustaceans and insects. Investigating visual function, we show that Parhyale has a positive phototactic response and is capable of adapting its eyes to different levels of light intensity.ConclusionsWe propose that the visual system of Parhyale serves low-resolution visual tasks, such as orientation and navigation, based on broad gradients of light intensity and polarisation. Optic lobe structure and photoreceptor projections point to significant divergence from the conserved visual circuits found in other malacostracan crustaceans and insects, which could be associated with a shift to low-resolution vision. Our study provides the foundation for research in the visual system of this genetically tractable species.

Development ◽  
1978 ◽  
Vol 45 (1) ◽  
pp. 55-83
Author(s):  
Hilary Anderson

The visual system of the locust, Schistocerca gregaria, has a highly ordered and predictable arrangement of neurons. The retina and the outermost layer, or lamina, of the optic lobe are each composed of repeating units, ommatidia and cartridges respectively. Each ommatidium has eight photoreceptor cells, which send axons directly to a group of five neurons in the lamina to form the cartridge. The importance, for the development of this precise pattern, of the mode of growth of the two arrays and of interactions between them was investigated. The spatial and temporal sequences of cell proliferation, differentiation and death in the developing retina and optic lobe were examined quantitatively under normal and experimental conditions. The retina grows from its anterior margin by addition of new ommatidia formed from recruited epidermal cells. The lamina also grows by addition of new neurons to its anterior margin, but these neurons are derived from a stem cell population. The parallel pattern of growth of the retina and lamina may be important for the formation of neuronal connexions between them. The retina grows and differentiates even when deprived of the underlying lamina. In laminae deprived of the ingrowth of new axons from the retina, the production of new neurons is also autonomous, but these neurons do not differentiate, but degenerate. A limited amount of cell death occurs in the laminae of control insects. These two observations suggest that a plausible mechanism for coordinating the sizes of the two arrays during normal development might be production of lamina neurons in excess of requirements and death of those remaining non-innervated.


Genetics ◽  
1994 ◽  
Vol 138 (4) ◽  
pp. 1137-1150 ◽  
Author(s):  
M A Serikaku ◽  
J E O'Tousa

Abstract The somda (sine oculis-medusa) mutant is the result of a P element insertion at position 43C on the second chromosome. somda causes aberrant development of the larval photoreceptor (Bolwig's) organ and the optic lobe primordium in the embryo. Later in development, adult photoreceptors fail to project axons into the optic ganglion. Consequently optic lobe development is aborted and photoreceptor cells show age-dependent retinal degeneration. The so gene was isolated and characterized. The gene encodes a homeodomain protein expressed in the optic lobe primordium and Bolwig's organ of embryos, in the developing adult visual system of larvae, and in photoreceptor cells and optic lobes of adults. In addition, the SO product is found at invagination sites during embryonic development: at the stomadeal invagination, the cephalic furrow, and at segmental boundaries. The mutant somda allele causes severe reduction of SO embryonic expression but maintains adult visual system expression. Ubiquitous expression of the SO gene product in 4-8-hr embryos rescues all somda mutant abnormalities, including the adult phenotypes. Thus, all deficits in adult visual system development and function results from failure to properly express the so gene during embryonic development. This analysis shows that the homeodomain containing SO gene product is involved in the specification of the larval and adult visual system development during embryogenesis.


1979 ◽  
Vol 73 (4) ◽  
pp. 121-126 ◽  
Author(s):  
Natalie C. Barraga ◽  
Marcia E. Collins

The rationale for a comprehensive program in visual functioning is based upon an assumed interaction between: (a) functions performed by the visual system, (b) developmental visual tasks organized in keeping with perceptual/cognitive milestones, and (c) a variety of indoor and outdoor environments.


Development ◽  
2002 ◽  
Vol 129 (9) ◽  
pp. 2247-2258 ◽  
Author(s):  
Amanda T. Pickup ◽  
Michele L. Lamka ◽  
Qi Sun ◽  
Man Lun R. Yip ◽  
Howard D. Lipshitz

We report that the hindsight (hnt) gene, which encodes a nuclear zinc-finger protein, regulates cell morphology, cell fate specification, planar cell polarity and epithelial integrity during Drosophila retinal development. In the third instar larval eye imaginal disc, HNT protein expression begins in the morphogenetic furrow and is refined to cells in the developing photoreceptor cell clusters just before their determination as neurons. In hnt mutant larval eye tissue, furrow markers persist abnormally posterior to the furrow, there is a delay in specification of preclusters as cells exit the furrow, there are morphological defects in the preclusters and recruitment of cells into specific R cell fates often does not occur. Additionally, genetically mosaic ommatidia with one or more hnt mutant outer photoreceptor cells, have planar polarity defects that include achirality, reversed chirality and misrotation. Mutants in the JNK pathway act as dominant suppressors of the hnt planar polarity phenotype, suggesting that HNT functions to downregulate JUN kinase (JNK) signaling during the establishment of ommatidial planar polarity. HNT expression continues in the photoreceptor cells of the pupal retina. When an ommatidium contains four or more hnt mutant photoreceptor cells, both genetically mutant and genetically wild-type photoreceptor cells fall out of the retinal epithelium, indicating a role for HNT in maintenance of epithelial integrity. In the late pupal stages, HNT regulates the morphogenesis of rhabdomeres within individual photoreceptor cells and the separation of the rhabdomeres of adjacent photoreceptor cells. Apical F-actin is depleted in hnt mutant photoreceptor cells before the observed defects in cellular morphogenesis and epithelial integrity. The analyses presented here, together with our previous studies in the embryonic amnioserosa and tracheal system, show that HNT has a general role in regulation of the F-actin-based cytoskeleton, JNK signaling, cell morphology and epithelial integrity during development.


Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 132-132
Author(s):  
S Edelman ◽  
S Duvdevani-Bar

To recognise a previously seen object, the visual system must overcome the variability in the object's appearance caused by factors such as illumination and pose. It is possible to counter the influence of these factors, by learning to interpolate between stored views of the target object, taken under representative combinations of viewing conditions. Routine visual tasks, however, typically require not so much recognition as categorisation, that is making sense of objects not seen before. Despite persistent practical difficulties, theorists in computer vision and visual perception traditionally favour the structural route to categorisation, according to which forming a description of a novel shape in terms of its parts and their spatial relationships is a prerequisite to the ability to categorise it. In comparison, we demonstrate that knowledge of instances of each of several representative categories can provide the necessary computational substrate for the categorisation of their new instances, as well as for representation and processing of radically novel shapes, not belonging to any of the familiar categories. The representational scheme underlying this approach, according to which objects are encoded by their similarities to entire reference shapes (S Edelman, 1997 Behavioral and Brain Sciences in press), is computationally viable, and is readily mapped onto the mechanisms of biological vision revealed by recent psychophysical and physiological studies.


BMC Biology ◽  
2019 ◽  
Vol 17 (1) ◽  
Author(s):  
Ana Patricia Ramos ◽  
Ola Gustafsson ◽  
Nicolas Labert ◽  
Iris Salecker ◽  
Dan-Eric Nilsson ◽  
...  

1995 ◽  
Vol 305 (2) ◽  
pp. 605-611 ◽  
Author(s):  
Y Hu ◽  
W P Schilling

The Drosophila proteins, Trp and Trpl, are suggested to be cation channels responsible for depolarization of the receptor potential associated with stimulation of insect photoreceptor cells by light. Consistent with this hypothesis, we recently showed that recombinant Trpl forms Ca(2+)- and Ba(2+)-permeable non-selective cation channels when expressed in Sf9 cells using the baculovirus expression vector. As Trpl may be activated in the photoreceptor cell after stimulation of phospholipase C, we hypothesized that a similar regulation of recombinant Trpl may be observed in the Sf9 cell after activation of heterologous membrane receptors linked to Ca(2+)-signal-transduction pathways. To test this hypothesis, Ca2+ signalling was examined in Fura-2-loaded Sf9 cells infected with baculovirus containing cDNA for the M5 muscarinic receptor alone (M5 cells) or in cells co-infected with both M5 and Trpl-containing baculoviruses (M5-Trpl cells). Addition of carbachol (100 microM) to M5 cells produced an increase in cytosolic free Ca2+ concentration ([Ca2+]i) (mean +/- S.D.; n = 17) from 101 +/- 20 to 762 +/- 178 nM which declined to a sustained elevated level of 384 +/- 102 nM after 3 min. The sustained component was eliminated by removal of extracellular Ca2+ or by addition of La3+ or Gd3+ (10 microM). In M5-Trpl cells, basal [Ca2+]i increased as a function of time after infection. To evaluate the contribution of Ca2+ influx to the overall profile observed, Ba2+, a Ca2+ surrogate that is not a substrate for the Ca2+ pump, was used. The increase in basal [Ca2+]i seen in M5-Trpl cells was associated with an increase in basal Ba2+ influx. Addition of carbachol to M5-Trpl cells at 30-36 h after infection produced a large increase in [Ca2+]i to a sustained value of 677 +/- 143 nM. This change in [Ca2+]i was (1) blocked by atropine, (2) attenuated in the absence of extracellular Ca2+, and (3) relatively insensitive to La3+, but blocked by Gd3+ in the 0.1-1 mM range. In the presence of 10 microM Gd3+ to block the endogenous-receptor-mediated Ca(2+)-influx in M5-Trpl cells. In sharp contrast increase in Ba2+ influx in M5-Trpl cells. In sharp contrast, neither Ca2+ nor Ba2+ influx through Trpl was affected by thapsigargin, a selective inhibitor of the endoplasmic reticulum Ca(2+)-ATPase pump.(ABSTRACT TRUNCATED AT 400 WORDS)


Physiology ◽  
2010 ◽  
Vol 25 (1) ◽  
pp. 8-15 ◽  
Author(s):  
Brian M. Kevany ◽  
Krzysztof Palczewski

Photoreceptor cells maintain a roughly constant length by continuously generating new outer segments from their base while simultaneously releasing mature outer segments engulfed by the retinal pigment epithelium (RPE). Thus postmitotic RPE cells phagocytose an immense amount of material over a lifetime, disposing of photoreceptor cell waste while retaining useful content. This review focuses on current knowledge of outer segment phagocytosis, discussing the steps involved along with their critical participants as well as how various perturbations in outer segment (OS) disposal can lead to retinopathies.


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