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

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.

Color and cellular selectivity of retinal ganglion cell subtypes through frequency modulation of electrical stimulation

Epiretinal prostheses aim at electrically stimulating the inner most surviving retinal cells—retinal ganglion cells (RGCs)—to restore partial sight to the blind. Recent tests in patients with epiretinal implants have revealed that electrical stimulation of the retina results in the percept of color of the elicited phosphenes, which depends on the frequency of stimulation. This paper presents computational results that are predictive of this finding and further support our understanding of the mechanisms of color encoding in electrical stimulation of retina, which could prove pivotal for the design of advanced retinal prosthetics that elicit both percept and color. This provides, for the first time, a directly applicable “amplitude-frequency” stimulation strategy to “encode color” in future retinal prosthetics through a predictive computational tool to selectively target small bistratified cells, which have been shown to contribute to “blue-yellow” color opponency in the retinal circuitry. The presented results are validated with experimental data reported in the literature and correlated with findings in blind patients with a retinal prosthetic implant collected by our group.

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

In 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.

How Convolutional Neural Network Architecture Biases Learned Opponency and Color Tuning

Recent work suggests that changing convolutional neural network (CNN) architecture by introducing a bottleneck in the second layer can yield changes in learned function. To understand this relationship fully requires a way of quantitatively comparing trained networks. The fields of electrophysiology and psychophysics have developed a wealth of methods for characterizing visual systems that permit such comparisons. Inspired by these methods, we propose an approach to obtaining spatial and color tuning curves for convolutional neurons that can be used to classify cells in terms of their spatial and color opponency. We perform these classifications for a range of CNNs with different depths and bottleneck widths. Our key finding is that networks with a bottleneck show a strong functional organization: almost all cells in the bottleneck layer become both spatially and color opponent, and cells in the layer following the bottleneck become nonopponent. The color tuning data can further be used to form a rich understanding of how color a network encodes color. As a concrete demonstration, we show that shallower networks without a bottleneck learn a complex nonlinear color system, whereas deeper networks with tight bottlenecks learn a simple channel opponent code in the bottleneck layer. We develop a method of obtaining a hue sensitivity curve for a trained CNN that enables high-level insights that complement the low-level findings from the color tuning data. We go on to train a series of networks under different conditions to ascertain the robustness of the discussed results. Ultimately our methods and findings coalesce with prior art, strengthening our ability to interpret trained CNNs and furthering our understanding of the connection between architecture and learned representation. Trained models and code for all experiments are available at https://github.com/ecs-vlc/opponency .

Functional Organization for Color Appearance Mechanisms in Primary Visual Cortex

Studies of color perception have led to mechanistic models of how signals from cone-opponent retinal ganglion cells are integrated to generate color appearance. But it is not known where or how these hypothesized mechanisms occur in the brain. Here we show that cone opponent signals transmitted from the retina to primary visual cortex (V1) are integrated through highly organized circuits within V1 to generate the color opponent mechanisms that underlie color appearance. Combining intrinsic signal optical imaging (ISI) and 2-photon calcium imaging (2PCI) at single cell resolution, we demonstrate cone-opponent functional domains (COFDs) that combine L/M cone-opponent and S/L+M cone-opponent signals in precisely the combinations predicted from psychophysical studies of color perception. These give rise to an orderly organization of hue preferences of the neurons within the COFDs and the generation of hue “pinwheels”. COFDs occupy regions corresponding to both high and low cytochrome oxidase intensity (“blobs” and “interblobs”) but have a bias toward blobs. Thus, neural circuits in the primary visual cortex establish the boundary conditions for color opponency and unique hues.One Sentence SummaryCone-opponent functional domains generate color opponent functional architecture in primary visual cortex.

Geometry of color perception. Part 2: perceived colors from real quantum states and Hering’s rebit

Inspired by the pioneer work of H.L. Resnikoff, which is described in full detail in the first part of this two-part paper, we give a quantum description of the space $\mathcal{P}$ P of perceived colors. We show that $\mathcal{P}$ P is the effect space of a rebit, a real quantum qubit, whose state space is isometric to Klein’s hyperbolic disk. This chromatic state space of perceived colors can be represented as a Bloch disk of real dimension 2 that coincides with Hering’s disk given by the color opponency mechanism. Attributes of perceived colors, hue and saturation, are defined in terms of Von Neumann entropy.

Color preference of the spotted wing Drosophila, Drosophila suzukii

Drosophila suzukii Matsumura (Diptera: Drosophilidae) is a significant invasive pest in soft-skin fruits and berries in Asia, Europe, and North and South America. Many herbivorous insects use multiple cues for host selection, particularly olfactory and visual stimuli. The visual system of closely-related Drosophila melanogaster is well-documented, expressing strong sensitivity to short-wavelength colors (ultraviolet to green) and only limited sensitivity to long-wavelength colors (red to infrared). Our results suggest that D. suzukii have limited ability to distinguish red consistent with visual sensitivity range within the melanogaster subgroup. We propose that color contrast rather than color appearance may be of greater importance in orientation and attraction. We propose that differences in reflectance between light wavelengths important for color opponency are key to color discrimination to provide color contrast between foreground and background, as occurs between fruit and foliage, during host-finding.