scholarly journals Insights into the evolutionary origin of the pineal color discrimination mechanism from the river lamprey

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Seiji Wada ◽  
Emi Kawano-Yamashita ◽  
Tomohiro Sugihara ◽  
Satoshi Tamotsu ◽  
Mitsumasa Koyanagi ◽  
...  
Keyword(s):  
Visible Light ◽  
Ganglion Cells ◽  
Glutamate Transporter ◽  
Sensory Information ◽  
Color Discrimination ◽  
Photoreceptor Cells ◽  
Cell System ◽  
Neural Firing ◽  
Electrophysiological Recordings ◽  
Color Opponency

Abstract Background Pineal-related organs in cyclostomes, teleosts, amphibians, and reptiles exhibit color opponency, generating antagonistic neural responses to different wavelengths of light and thereby sensory information about its “color”. Our previous studies suggested that in zebrafish and iguana pineal-related organs, a single photoreceptor cell expressing both UV-sensitive parapinopsin and green-sensitive parietopsin generates color opponency in a “one-cell system.” However, it remains unknown to what degree these opsins and the single cell-based mechanism in the pineal color opponency are conserved throughout non-mammalian vertebrates. Results We found that in the lamprey pineal organ, the two opsins are conserved but that, in contrast to the situation in other vertebrate pineal-related organs, they are expressed in separate photoreceptor cells. Intracellular electrophysiological recordings demonstrated that the parietopsin-expressing photoreceptor cells with Go-type G protein evoke a depolarizing response to visible light. Additionally, spectroscopic analyses revealed that parietopsin with 11-cis 3-dehydroretinal has an absorption maximum at ~570 nm, which is in approximate agreement with the wavelength (~560 nm) that produces the maximum rate of neural firing in pineal ganglion cells exposed to visible light. The vesicular glutamate transporter is localized at both the parietopsin- and parapinopsin-expressing photoreceptor terminals, suggesting that both types of photoreceptor cells use glutamate as a transmitter. Retrograde tracing of the pineal ganglion cells revealed that the terminal of the parietopsin-expressing cells is located close enough to form a neural connection with the ganglion cells, which is similar to our previous observation for the parapinopsin-expressing photoreceptor cells and the ganglion cells. In sum, our observations point to a “two-cell system” in which parietopsin and parapinopsin, expressed separately in two different types of photoreceptor cells,  contribute to the generation of color opponency in the pineal ganglion cells. Conclusion Our results indicate that the jawless vertebrate, lamprey, employs a system for color opponency that differes from that described previously in jawed vertebrates. From a physiological viewpoint, we propose an evolutionary insight, the emergence of pineal “one-cell system” from the ancestral “multiple (two)-cell system,” showing the opposite evolutionary direction to that of the ocular color opponency.

scholarly journals Color opponency with a single kind of bistable opsin in the zebrafish pineal organ

2018 ◽  
Vol 115 (44) ◽  
pp. 11310-11315 ◽  
Author(s):  
Seiji Wada ◽  
Baoguo Shen ◽  
Emi Kawano-Yamashita ◽  
Takashi Nagata ◽  
Masahiko Hibi ◽  
...  
Keyword(s):  
Visible Light ◽  
Incident Light ◽  
Spectral Composition ◽  
Color Discrimination ◽  
Calcium Signal ◽  
Lower Vertebrate ◽  
Cone Opsin ◽  
Color Opponency ◽  
Visible Wavelengths ◽  
Pineal Photoreceptors

Lower vertebrate pineal organs discriminate UV and visible light. Such color discrimination is typically considered to arise from antagonism between two or more spectrally distinct opsins, as, e.g., human cone-based color vision relies on antagonistic relationships between signals produced by red-, green-, and blue-cone opsins. Photosensitive pineal organs contain a bistable opsin (parapinopsin) that forms a signaling-active photoproduct upon UV exposure that may itself be returned to the signaling-inactive “dark” state by longer-wavelength light. Here we show the spectrally distinct parapinopsin states (with antagonistic impacts on signaling) allow this opsin alone to provide the color sensitivity of this organ. By using calcium imaging, we show that single zebrafish pineal photoreceptors held under a background light show responses of opposite signs to UV and visible light. Both such responses are deficient in zebrafish lacking parapinopsin. Expressing a UV-sensitive cone opsin in place of parapinopsin recovers UV responses but not color opponency. Changes in the spectral composition of white light toward enhanced UV or visible wavelengths respectively increased vs. decreased calcium signal in parapinopsin-sufficient but not parapinopsin-deficient photoreceptors. These data reveal color opponency from a single kind of bistable opsin establishing an equilibrium-like mixture of the two states with different signaling abilities whose fractional concentrations are defined by the spectral composition of incident light. As vertebrate visual color opsins evolved from a bistable opsin, these findings suggest that color opponency involving a single kind of bistable opsin might have been a prototype of vertebrate color opponency.

scholarly journals Functional identification of an opsin kinase underlying inactivation of the pineal bistable opsin parapinopsin in zebrafish

2021 ◽  
Vol 7 (1) ◽  
Author(s):  
Baoguo Shen ◽  
Seiji Wada ◽  
Haruka Nishioka ◽  
Takashi Nagata ◽  
Emi Kawano-Yamashita ◽  
...  
Keyword(s):  
Visible Light ◽  
Photoreceptor Cells ◽  
Light Sensitivity ◽  
Functional Identification ◽  
Remarkable Effect ◽  
Zebrafish Larvae ◽  
Cone Opsin ◽  
Cone Type ◽  
Color Opponency ◽  
Cone Opsins

AbstractIn the pineal organ of zebrafish larvae, the bistable opsin parapinopsin alone generates color opponency between UV and visible light. Our previous study suggested that dark inactivation of the parapinopsin photoproduct, which activates G-proteins, is important for the regulation of the amount of the photoproduct. In turn, the photoproduct is responsible for visible light sensitivity in color opponency. Here, we found that an opsin kinase or a G-protein-coupled receptor kinase (GRK) is involved in inactivation of the active photoproduct of parapinopsin in the pineal photoreceptor cells of zebrafish larvae. We investigated inactivation of the photoproduct in the parapinopsin cells of various knockdown larvae by measuring the light responses of the cells using calcium imaging. We found that GRK7a knockdown slowed recovery of the response of parapinopsin photoreceptor cells, whereas GRK1b knockdown or GRK7b knockdown did not have a remarkable effect, suggesting that GRK7a, a cone-type GRK, is mainly responsible for inactivation of the parapinopsin photoproduct in zebrafish larvae. We also observed a similar knockdown effect on the response of the parapinopsin photoreceptor cells of mutant larvae expressing the opsin SWS1, a UV-sensitive cone opsin, instead of parapinopsin, suggesting that the parapinopsin photoproduct was inactivated in a way similar to that described for cone opsins. We confirmed the immunohistochemical distribution of GRK7a in parapinopsin photoreceptor cells by comparing the immunoreactivity to GRK7 in GRK7a-knockdown and control larvae. These findings suggest that in pineal photoreceptor cells, the cone opsin kinase GRK7a contributes greatly to the inactivation of parapinopsin, which underlies pineal color opponency.

scholarly journals The visual ecology of a deep-sea fish, the escolar Lepidocybium flavobrunneum (Smith, 1843)

2014 ◽  
Vol 369 (1636) ◽  
pp. 20130039 ◽  
Author(s):  
Eva Landgren ◽  
Kerstin Fritsches ◽  
Richard Brill ◽  
Eric Warrant
Keyword(s):  
Surface Waters ◽  
Deep Sea ◽  
Ganglion Cells ◽  
Optical Path Length ◽  
Predatory Fish ◽  
Flicker Fusion Frequency ◽  
Optical Sensitivity ◽  
Light Levels ◽  
Electrophysiological Recordings ◽  
Maximal Absorption

Escolar ( Lepidocybium flavobrunneum , family Gempylidae) are large and darkly coloured deep-sea predatory fish found in the cold depths (more than 200 m) during the day and in warm surface waters at night. They have large eyes and an overall low density of retinal ganglion cells that endow them with a very high optical sensitivity. Escolar have banked retinae comprising six to eight layers of rods to increase the optical path length for maximal absorption of the incoming light. Their retinae possess two main areae of higher ganglion cell density, one in the ventral retina viewing the dorsal world above (with a moderate acuity of 4.6 cycles deg −1 ), and the second in the temporal retina viewing the frontal world ahead. Electrophysiological recordings of the flicker fusion frequency (FFF) in isolated retinas indicate that escolar have slow vision, with maximal FFF at the highest light levels and temperatures (around 9 Hz at 23°C) which fall to 1–2 Hz in dim light or cooler temperatures. Our results suggest that escolar are slowly moving sit-and-wait predators. In dim, warm surface waters at night, their slow vision, moderate dorsal resolution and highly sensitive eyes may allow them to surprise prey from below that are silhouetted in the downwelling light.

Bipolar cell pathways for color vision in non-primate dichromats

2010 ◽  
Vol 28 (1) ◽  
pp. 51-60 ◽  
Author(s):  
CHRISTIAN PULLER ◽  
SILKE HAVERKAMP
Keyword(s):  
Color Vision ◽  
Bipolar Cell ◽  
Ganglion Cells ◽  
Color Discrimination ◽  
Model Systems ◽  
Retinal Ganglion ◽  
Retinal Pathways ◽  
Retinal Information Processing ◽  
Cone Opsins ◽  
Retinal Information

AbstractColor vision in mammals is based on the expression of at least two cone opsins that are sensitive to different wavelengths of light. Furthermore, retinal pathways conveying color-opponent signals are required for color discrimination. Most of the primates are trichromats, and “color-coded channels” of their retinas are unveiled to a large extent. In contrast, knowledge of cone-selective pathways in nonprimate dichromats is only slowly emerging, although retinas of dichromats like mice or rats are extensively studied as model systems for retinal information processing. Here, we review recent progress of research on color-coded pathways in nonprimate dichromats to identify differences or similarities between di- and trichromatic mammals. In addition, we applied immunohistochemical methods and confocal microscopy to retinas of different species and present data on their neuronal properties, which are expected to contribute to color vision. Basic neuronal features such as the “blue cone bipolar cell” exist in every species investigated so far. Moreover, there is increasing evidence for chromatic OFF channels in dichromats and retinal ganglion cells that relay color-opponent signals to the brain. In conclusion, di- and trichromats share similar retinal pathways for color transmission and processing.

Alterations in NMDA receptor expression during retinal degeneration in the RCS rat

2001 ◽  
Vol 18 (5) ◽  
pp. 781-787 ◽  
Author(s):  
TATIANA GRÜNDER ◽  
KONRAD KOHLER ◽  
ELKE GUENTHER
Keyword(s):  
Ganglion Cells ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Photoreceptor Cells ◽  
Receptor Expression ◽  
Signal Pathways ◽  
Inner Plexiform Layer ◽  
Functional Changes ◽  
Rcs Rat ◽  
Rcs Rats

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.

scholarly journals Luminescence- and nanoparticle-mediated increase of light absorption by photoreceptor cells: Converting UV light to visible light

2016 ◽  
Vol 6 (1) ◽  
Author(s):  
Lei Li ◽  
Sunil K. Sahi ◽  
Mingying Peng ◽  
Eric B. Lee ◽  
Lun Ma ◽  
...  
Keyword(s):  
Visible Light ◽  
Light Absorption ◽  
Uv Light ◽  
Photoreceptor Cells

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
Keyword(s):  
Ganglion Cells ◽  
Photoreceptor Cells ◽  
Sea Lamprey ◽  
High Ratio ◽  
Bipolar Cells ◽  
Peripheral Retina ◽  
Radial Gradient ◽  
New Development ◽  
Cell Layers ◽  
Relationship Of

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.

Lateral visual pathway of giant barnacle

1983 ◽  
Vol 49 (2) ◽  
pp. 516-527 ◽  
Author(s):  
L. A. Oland ◽  
K. A. French ◽  
J. H. Hayashi ◽  
A. E. Stuart
Keyword(s):  
Action Potentials ◽  
Ganglion Cells ◽  
Photoreceptor Cells ◽  
Visual Pathways ◽  
The Other ◽  
Visual Signals ◽  
Ipsilateral Side ◽  
Lateral Eye ◽  
Voltage Change ◽  
Tetraethylammonium Ion

1. We have studied the responses to light, conduction down the axons, and anatomical projections of the photoreceptors of the lateral eye in the giant barnacle, Balanus nubilus. By recording intracellularly from ganglion cells that respond to visual input, we have described convergence of the lateral and median visual pathways. 2. Each lateral eye contains three photoreceptor cells, two large and one small. Cobalt filling of single large lateral receptor axons demonstrated that they end in a restricted ovoid bush on the ipsilateral side of the ganglion in approximately the same region in which the median receptors arborize. 3. The lateral receptors have dark resting potentials and responses to light similar to those previously described for the receptors of the median eye. Like the median receptors, the lateral receptors conduct visual signals decrementally, although their axons may be twice as long (14-25 mm). 4. Passing current of either polarity into either of the large receptors produced no detectable voltage change in the other cell. Action potentials elicited in either cell by stimulating it in the presence of tetraethylammonium ion were not detected in the other cell. Light-induced membrane noise in one cell did not correlate with noise in the other. Thus, like the receptors of the median eye, the large receptors of the lateral eye are not electrically coupled. 5. By shadowing each ocellus individually, we have shown that the signals from the median and lateral photoreceptors converge at the level of the second-order cells described for the median pathway. Shadowing the median or a lateral eye gave rise to synergistic responses in second-, third-, and all higher order ganglion cells studied. No cells were found that were driven solely by the lateral eyes. Thus, the lateral and median visual pathways are highly convergent.

Preferential suppression of the ON pathway by GABAC receptors in the amphibian retina

1995 ◽  
Vol 74 (4) ◽  
pp. 1583-1592 ◽  
Author(s):  
J. Zhang ◽  
M. M. Slaughter
Keyword(s):  
Gabaa Receptor ◽  
Gabab Receptor ◽  
Ganglion Cells ◽  
Chloride Conductance ◽  
Equilibrium Potential ◽  
Resting Membrane Potential ◽  
Gamma Aminobutyric Acid ◽  
Electrophysiological Recordings ◽  
Gabac Receptor ◽  
Gabac Receptors

1. Electrophysiological recordings were obtained from neurons in the amphibian intact retina and retinal slice preparations. The effects of gamma-aminobutyric acid (GABA) were evaluated in the presence of bicuculline or SR95531, which block the GABAA receptor, and baclofen, which saturates the GABAB receptor. 2. Under these conditions, GABA preferentially reduced ON light responses in amacrine and ganglion cells, apparently through a presynaptic mechanism that reduced bipolar cell input. GABA also produced a small hyperpolarization in the resting membrane potential of ganglion cells. 3. Picrotoxin blocked these effects of GABA. The action of GABA was duplicated by muscimol and by trans-aminocrotonic acid. Cis-aminocrotonic acid was neither a potent nor selective agonist. This pharmacology is indicative of the GABAC receptor. 4. In voltage-clamp recordings of ganglion cells in the slice preparation, GABA produced a large chloride conductance that was blocked by bicuculline or SR95531, and a smaller chloride conductance that was not blocked by these GABAA receptor antagonists, but was blocked by picrotoxin. This indicates that ganglion cells possess both GABAA and GABAC receptors. 5. The GABAC receptor current was relatively nondesensitized. Consequently, whereas the peak GABAA receptor current was more than fivefold larger than the GABAC receptor current, after desensitization the latter current was larger. Both currents reversed near the chloride equilibrium potential.

Differential cellular and subcellular distribution of glutamate transporters in the cat retina

2004 ◽  
Vol 21 (4) ◽  
pp. 551-565 ◽  
Author(s):  
BOZENA FYK-KOLODZIEJ ◽  
PU QIN ◽  
ARTURIK DZHAGARYAN ◽  
ROBERTA G. POURCHO
Keyword(s):  
Ganglion Cells ◽  
Excitatory Amino Acid ◽  
Pigment Epithelium ◽  
Glutamate Transporter ◽  
Bipolar Cells ◽  
Amino Acid Transporters ◽  
Cone Photoreceptors ◽  
Glutamatergic Synapses ◽  
Axon Terminals ◽  
Cat Retina

Retrieval of glutamate from extracellular sites in the retina involves at least five excitatory amino acid transporters. Immunocytochemical analysis of the cat retina indicates that each of these transporters exhibits a selective distribution which may reflect its specific function. The uptake of glutamate into Müller cells or astrocytes appears to depend upon GLAST and EAAT4, respectively. Staining for EAAT4 was also seen in the pigment epithelium. The remaining transporters are neuronal with GLT-1α localized to a number of cone bipolar, amacrine, and ganglion cells and GLT-1v in cone photoreceptors and several populations of bipolar cells. The EAAC1 transporter was found in horizontal, amacrine, and ganglion cells. Staining for EAAT5 was seen in the axon terminals of both rod and cone photoreceptors as well as in numerous amacrine and ganglion cells. Although some of the glutamate transporter molecules are positioned for presynaptic or postsynaptic uptake at glutamatergic synapses, others with localizations more distant from such contacts may serve in modulatory roles or provide protection against excitoxic or oxidative damage.

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