From Riemannian Trichromacy to Quantum Color Opponency via Hyperbolicity

We have shown in the accompanying paper that optical imaging of macaque striate cortex reveals patches that are preferentially activated by equiluminant chromatic gratings compared with luminance gratings. These imaged color patches are highly correlated, although not always in one-to-one correspondence, with the cytochrome-oxidase (CO) blobs. In the present study, we have investigated the electrophysiological properties of neurons in the imaged color patches and the CO blobs. Our results indicate that individual blobs tend to contain cells of only one type of color opponency: either red/green or blue/yellow. Individual imaged color patches, however, can bridge blobs of similar opponency or differing opponency. When imaged color patches contain two blobs of differing opponency, the cells in the bridge region exhibit mixed color properties that are not opponent along the two cardinal color axes (either red/green or blue/yellow). Two blobs within a single imaged color patch receive input from the same eye or from different eyes. In the latter case, the bridge region between blobs contains binocular cells that are color selective. Because the cells recorded in imaged color patches were more color selective and unoriented than cells outside of color patches, color properties appear to be organized in a clustered and segregated fashion in primate V1.

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

BMC Biology ◽

10.1186/s12915-021-01121-1 ◽

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.

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Chromatic clocks: Color opponency in non-image-forming visual function

Neuroscience & Biobehavioral Reviews ◽

10.1016/j.neubiorev.2017.04.016 ◽

2017 ◽

Vol 78 ◽

pp. 24-33 ◽

Cited By ~ 19

Author(s):

Manuel Spitschan ◽

Robert J. Lucas ◽

Timothy M. Brown

Keyword(s):

Visual Function ◽

Color Opponency

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Spectral sensitivities of elementary color-coded neurons in butterfly larva

Journal of Neurophysiology ◽

10.1152/jn.1990.64.6.1861 ◽

1990 ◽

Vol 64 (6) ◽

pp. 1861-1872 ◽

Cited By ~ 6

Author(s):

T. Ichikawa

Keyword(s):

Synergistic Effect ◽

Compound Eye ◽

Functional Class ◽

The Other ◽

White Background ◽

Swallowtail Butterfly ◽

Color Opponency ◽

Distinct Color ◽

Different Color ◽

Excitatory Responses

1. Response properties and spectral sensitivities of a functional class of medulla neurons that received dominant input from a single stemma in the swallowtail butterfly larva were examined with regard to neutral and chromatic backgrounds. 2. Eight types of neurons were dominated by a dichromatic stemma with blue and green receptors. Six showed specific color-opponent responses mediated by two receptors on different backgrounds; one showed strong color opponency because of fairly balanced antagonistic input on the neutral (dark and white) background; the other five usually had weak or concealed color opponency on a neutral background but became strongly color opponent when appropriate chromatic illumination was present on the background. The most complex neuron gave excitatory responses on a dark background, inhibitory responses on a white background, and color-opponent responses on a chromatic (yellow) background. 3. The remaining two types of neurons dominated by the dichromatic stemma showed non-color-opponent and broad action spectra ascribable to a synergistic effect of the two classes of photoreceptors. 4. All eight types of neurons dominated by a trichromatic stemma (with UV, blue, and green receptors) were color opponent. Five showed strong color-opponent responses with the mediation of the three classes of receptors or only two (UV and green) on a neutral background. The others revealed distinct color opponency in the presence of UV or green illumination on the background. 5. The larval medulla neurons described may form parallel, elementary color-coded channels in the medulla neuropile to combine the outputs of the different color receptors in a single visual unit (stemma) into specific color-opponent signals. They probably correspond to columnar relay neurons in the medulla of the adult insects with a compound eye.

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Light adaptation and color opponency of horizontal cells in the turtle retina

Visual Neuroscience ◽

10.1017/s0952523803204090 ◽

2003 ◽

Vol 20 (4) ◽

pp. 437-452 ◽

Cited By ~ 2

Author(s):

GILAD TWIG ◽

HANNA LEVY ◽

ELITE WEINER ◽

IDO PERLMAN

Keyword(s):

Light Adaptation ◽

Light Sensitivity ◽

Horizontal Cells ◽

Background Illumination ◽

Voltage Range ◽

Background Adaptation ◽

Color Opponency ◽

Light Stimuli ◽

Type C

Chromaticity-type (C-type) horizontal cells of the turtle retina receive antagonistic inputs from cones of different spectral types, and therefore their response to background illumination is expected to reflect light adaptation of the cones and the interactions between their antagonistic inputs. Our goal was to study the behavior of C-type horizontal cells during background illumination and to evaluate the role of wavelength in background adaptation. The photoresponses of C-type horizontal cells were recorded intracellularly in the everted eyecup preparation of the turtleMauremys caspicaduring chromatic background illuminations. The voltage range of operation was either reduced or augmented, depending upon the wavelengths of the background and of the light stimuli, while the sensitivity to light was decreased by any background. The response–intensity curves were shifted to brighter intensities and became steeper as the background lights were made brighter regardless of wavelength. Comparing the effects of cone iso-luminant backgrounds on the Red/Green C-type horizontal cells indicated that background desensitization in these cells could not solely reflect background adaptation of cones but also depend upon response compression/expansion and changes in synaptic transmission. This leads to wavelength dependency of background adaptation in C-type horizontal cells, that is expressed as increased light sensitivity (smaller threshold elevation) and improved suprathreshold contrast detection when the wavelengths of the background and light stimuli were chosen to exert opponent effects on membrane potential.

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Regional topography of rod and immunocytochemically characterized “blue” and “green” cone photoreceptors in rabbit retina

Visual Neuroscience ◽

10.1017/s0952523800006799 ◽

1995 ◽

Vol 12 (6) ◽

pp. 1151-1175 ◽

Cited By ~ 43

Author(s):

E. V. Famiglietti ◽

S. J. Sharpe

Keyword(s):

Ganglion Cells ◽

Bipolar Cells ◽

Wide Field ◽

Rabbit Retina ◽

Double Labeling ◽

Peak Density ◽

Visual Streak ◽

Color Opponency ◽

Dorsal Retina ◽

Cone Density

AbstractEvidence from several sources indicates that the photoreceptors of rabbit retina include rods, green cones and blue cones, and that blue-green color opponency occurs in select retinal ganglion cells. One of us (Famiglietti) has identified wide-field cone bipolar cells as probable blue-cone-selective bipolars, and type C horizontal cells as possibly connected to blue cones. We wished to extend the analysis of blue cone pathways in rabbit retina and to characterize the topographic distribution of blue and green cones. Two monoclonal antibodies raised against chicken visual pigments are reported to label medium- and long-wavelength cones (COS-1) and short-wavelength cones (OS-2) in all mammalian retinas studied thus far (Szél and colleagues). Using selective labeling with these two antibodies and a nonselective method in nasal and temporal halves of the same retinas, we have found that densities of photoreceptors vary systematically, depending upon the size of the eye and age of the animal. In ‘standard’ New Zealand rabbits of 2–3 kg (2–3 months old), rods reached a peak density of about 300,000/mm2 just dorsal to the visual streak, while cones exhibit peak density at mid-visual streak of about 18,000/mm2. Published measurements of visual acuity in rabbit are less than predicted by this calculation. The ratio of cones to rods is significantly higher in ventral retina, where the density of cones declines to a plateau of 10,000–12,000/mm2, when compared to dorsal retina, where cones are uniformly distributed at a density of about 7000/mm2. The density of OS-2 labeled (presumably “blue”) cones is uniformly low, 1000–1500/mm2, in a wide expanse that includes dorsal retina, the visual streak, and much of ventral retina, except for a region of higher density along the vertical midline. We confirm that there is a far ventral horizontal region near the perimeter that is populated exclusively by a high density (about 13,000/mm2) of OS-2-positive cones (Juliusson and colleagues). This region does not extend to the ventral retinal margin, however, where cone density drops precipitously. Transitional zones between COS-1 and OS-2 labeling, in a region of relatively high and uniform cone density, where sums of COS-1 and OS-2 labeling are higher than expected and in which weakly and strongly labeled cones are intermixed, raise questions about the identities of the visual pigment epitopes, the possibility of double labeling, and therefore the possibility of dual expression of pigments in single cones. The “inverted- T -shaped” topography of higher density OS-2 labeling raises doubts about the significance of a ventral concentration of blue cones for visual function in rabbit retina.

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Different types of synapses with different spectral types of cones underlie color opponency in a bipolar cell of the turtle retina

Visual Neuroscience ◽

10.1017/s0952523899164186 ◽

1999 ◽

Vol 16 (5) ◽

pp. 801-809 ◽

Cited By ~ 17

Author(s):

SILKE HAVERKAMP ◽

WOLFGANG MÖCKEL ◽

JOSEF AMMERMÜLLER

Keyword(s):

Bipolar Cell ◽

Metabotropic Glutamate Receptors ◽

Horizontal Cell ◽

Bipolar Cells ◽

Horizontal Cells ◽

Color Processing ◽

Ionotropic Receptors ◽

Metabotropic Glutamate ◽

Different Types ◽

Color Opponency

Electrophysiologically, color-opponent retinal bipolar cells respond with opposite polarities to stimulation with different wavelengths of light. The origin of these different polarities in the same bipolar cell has always been a mystery. Here we show that an intracellularly recorded and HRP-injected, red-ON, blue/green-OFF bipolar cell of the turtle retina made invaginating (ribbon associated) synapses exclusively with L-cones. Non-invaginating synapses resembling wide-cleft basal junctions were made exclusively with M-cones. Input from S-cones was not seen. From these results we suggest sign-inverting transmission from L-cones at invaginating synapses via metabotropic glutamate receptors, and sign-conserving transmission from M-cones at wide-cleft basal junctions via ionotropic receptors. To explain the pronounced blue sensitivity of the bipolar cell, computer simulations were performed using a sign-conserving input from a yellow/blue chromaticity-type (H3) horizontal cell. The response properties of the red-ON, blue/green-OFF bipolar cell could be quantitatively reproduced by this means. The simulation also explained the asymmetry in L- and M-cone inputs to the bipolar cell as found in the ultrastructural analysis and assigned a putative role to H3 horizontal cells in color processing in the turtle retina.

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