Seeing Beyond Violet : UV Cones Guide High-Resolution Prey-Capture Behavior in Fish

How can fish see tiny underwater prey invisible to human eyes? In this issue of Neuron, Yoshimatsu et al. (2020) show that ultraviolet light and a rich set of fine-tuned anatomical and neural specializations originating in ultraviolet-sensitive cones underlie high-resolution prey-capture behavior in larval zebrafish.Non peer reviewe

The relation between spectral and thermal properties of vertebrate visual pigments

This thesis investigates the relation between three important functional properties of visual pigments: 1) the absorbance spectrum, 2) the energy needed for activation and 3) the thermal stability. The study is based on measurement of spectral absorbance and spectral sensitivity in 10 visual pigments in rod and cone photoreceptor cells from the retinas of 6 vertebrate species and on data from the literature. Absorbance spectra were recorded by single-cell mictrospectrophotometry (MSP) and spectral sensitivities by electroretinogram recording (ERG) across the isolated retina. For each pigment, measurements were conducted at two or more temperatures in the range 0-40 °C. The photoactivation energies of the visual pigments were determined from the temperature-dependence of spectral sensitivity in the long-wavelength range. Thermal activation rates of rod and cone pigments were collected from the literature. One objective was to test the hypothesis that there is a strict coupling between the energy needed for photoactivation (Ea) and the wavelength of maximum absorbance (λmax) of visual pigments. The greater goal was to clarify the relation between the energies required for thermal and photic activation and thus explain the experimentally observed correlation between λmax and the rate of spontaneous, thermal activation of pigments. The measurements showed that there is no necessary physical coupling between Ea and λmax. A strict inverse proportionality (Ea ∝ 1/λmax) holds only in the simple case where spectral tuning is achieved by a change of chromophore, with no change in the protein (opsin) part of the pigment. On the other hand, a significant correlation between Ea and 1/λmax was found in the full set of 12 visual pigments considered (including two invertebrate pigments). A new model for thermal activation is proposed, with a consequent dependence of the activation rate on λmax. The crucial point is that the statistics of thermal activation is determined by the presence of internal energy in a large number of vibrational modes of the visual pigment molecule. The great discrepancy between photoactivation energies and thermal activation energies as estimated in earlier work then disappears as an analytical artifact. The main conclusion is that thermal and photic activation of visual pigments may follow the same molecular route from a very early stage (isomerization of the chromophore in the native conformation of rhodopsin). Furthermore, the model accurately predicts the correlation between the wavelength of maximum absorbance and the rate of thermal activation observed in the whole set of visual pigments studied.reviewe

Mice Reach Higher Visual Sensitivity at Night by Using a More Efficient Behavioral Strategy

Circadian clocks predictively adjust the physiology of organisms to the day/night cycle. The retina has its own clock, and many diurnal changes in its physiology have been reported. However, their implications for retinal functions and visually guided behavior are largely unresolved. Here, we study the impact of diurnal rhythm on the sensitivity limit of mouse vision. A simple photon detection task allowed us to link well-defined retinal output signals directly to visually guided behavior. We show that visually guided behavior at its sensitivity limit is strongly under diurnal control, reaching the highest sensitivity and stability at night. The diurnal differences in visual sensitivity did not arise in the retina, as assessed by spike recordings from the most sensitive retinal ganglion cell types: ON sustained, OFF sustained, and OFF transient alpha ganglion cells. Instead, we found that mice, as nocturnal animals, use a more efficient search strategy for visual cues at night. Intriguingly, they can switch to the more efficient night strategy even at their subjective day after first having performed the task at night. Our results exemplify that the shape of visual psychometric functions depends robustly on the diurnal state of the animal, its search strategy, and even its diurnal history of performing the task. The results highlight the impact of the day/night cycle on high-level sensory processing, demonstrating a direct diurnal impact on the behavioral strategy of the animal.Peer reviewe

Processing of single-photon responses in the mammalian On and Off retinal pathways at the sensitivity limit of vision

Visually guided behaviour at its sensitivity limit relies on single-photon responses originating in a small number of rod photoreceptors. For decades, researchers have debated the neural mechanisms and noise sources that underlie this striking sensitivity. To address this question, we need to understand the constraints arising from the retinal output signals provided by distinct retinal ganglion cell types. It has recently been shown in the primate retina that On and Off parasol ganglion cells, the cell types likely to underlie light detection at the absolute visual threshold, differ fundamentally not only in response polarity, but also in the way they handle single-photon responses originating in rods. The On pathway provides the brain with a thresholded, low-noise readout and the Off pathway with a noisy, linear readout. We outline the mechanistic basis of these different coding strategies and analyse their implications for detecting the weakest light signals. We show that high-fidelity, nonlinear signal processing in the On pathway comes with costs: more single-photon responses are lost and their propagation is delayed compared with the Off pathway. On the other hand, the responses of On ganglion cells allow better intensity discrimination compared with the Off ganglion cell responses near visual threshold. This article is part of the themed issue 'Vision in dim light'.Peer reviewe

Thermal Activation and Photoactivation of Visual Pigments

A visual pigment molecule in a retinal photoreceptor cell can be activated not only by absorption of a photon but also ‘‘spontaneously’’ by thermal energy. Current estimates of the activation energies for these two processes in vertebrate rod and cone pigments are on the order of 40–50 kcal/mol for activation by light and 20–25 kcal/mol for activation by heat, which has forced the conclusion that the two follow quite different molecular routes. It is shown here that the latter estimates, derived from the temperature dependence of the rate of pigment-initiated ‘‘dark events’’ in rods, depend on the unrealistic assumption that thermal activation of a complex molecule like rhodopsin (or even its 11-cis retinaldehyde chromophore) happens through a simple process, somewhat like the collision of gas molecules. When the internal energy present in the many vibrational modes of the molecule is taken into account, the thermal energy distribution of the molecules cannot be described by Boltzmann statistics, and conventional Arrhenius analysis gives incorrect estimates for the energy barrier. When the Boltzmann distribution is replaced by one derived by Hinshelwood for complex molecules with many vibrational modes, the same experimental data become consistent with thermal activation energies that are close to or even equal to the photoactivation energies. Thus activation by light and by heat may in fact follow the same molecular route, starting with 11-cis to all-trans isomerization of the chromophore in the native (resting) configuration of the opsin. Most importantly, the same model correctly predicts the empirical correlation between the wavelength of maximum absorbance and the rate of thermal activation in the whole set of visual pigments studied

Retinal OFF ganglion cells allow detection of quantal shadows at starlight

Perception of light in darkness requires no more than a handful of photons, and this remarkable behavioral performance can be directly linked to a particular retinal circuit???the retinal ON pathway. However, the neural limits of shadow detection in very dim light have remained unresolved. Here, we unravel the neural mecha-nisms that determine the sensitivity of mice (CBA/CaJ) to light decrements at the lowest light levels by measuring signals from the most sensitive ON and OFF retinal ganglion cell types and by correlating their sig-nals with visually guided behavior. We show that mice can detect shadows when only a few photon absorp-tions are missing among thousands of rods. Behavioral detection of such ???quantal???shadows relies on the retinal OFF pathway and is limited by noise and loss of single-photon signals in retinal processing. Thus, in the dim-light regime, light increments and decrements are encoded separately via the ON and OFF retinal pathways, respectively.Peer reviewe

Turning Cones Off: the Role of the 9-Methyl Group of Retinal in Red Cones

Our ability to see in bright light depends critically on the rapid rate at which cone photoreceptors detect and adapt to changes in illumination. This is achieved, in part, by their rapid response termination. In this study, we investigate the hypothesis that this rapid termination of the response in red cones is dependent on interactions between the 9-methyl group of retinal and red cone opsin, which are required for timely metarhodopsin (Meta) II decay. We used single-cell electrical recordings of flash responses to assess the kinetics of response termination and to calculate guanylyl cyclase (GC) rates in salamander red cones containing native visual pigment as well as visual pigment regenerated with 11-cis 9-demethyl retinal, an analogue of retinal in which the 9-methyl group is missing. After exposure to bright light that photoactivated more than ∼0.2% of the pigment, red cones containing the analogue pigment had a slower recovery of both flash response amplitudes and GC rates (up to 10 times slower at high bleaches) than red cones containing 11-cis retinal. This finding is consistent with previously published biochemical data demonstrating that red cone opsin regenerated in vitro with 11-cis 9-demethyl retinal exhibited prolonged activation as a result of slowed Meta II decay. Our results suggest that two different mechanisms regulate the recovery of responsiveness in red cones after exposure to light. We propose a model in which the response recovery in red cones can be regulated (particularly at high light intensities) by the Meta II decay rate if that rate has been inhibited. In red cones, the interaction of the 9-methyl group of retinal with opsin promotes efficient Meta II decay and, thus, the rapid rate of recovery

The 9-methyl group of retinal is essential for rapid Meta II decay and phototransduction quenching in red cones

Cone photoreceptors of the vertebrate retina terminate their response to light much faster than rod photoreceptors. However, the molecular mechanisms underlying this rapid response termination in cones are poorly understood. The experiments presented here tested two related hypotheses: first, that the rapid decay rate of metarhodopsin (Meta) II in red-sensitive cones depends on interactions between the 9-methyl group of retinal and the opsin part of the pigment molecule, and second, that rapid Meta II decay is critical for rapid recovery from saturation of red-sensitive cones after exposure to bright light. Microspectrophotometric measurements of pigment photolysis, microfluorometric measurements of retinol production, and single-cell electrophysiological recordings of flash responses of salamander cones were performed to test these hypotheses. In all cases, cones were bleached and their visual pigment was regenerated with either 11-cis retinal or with 11-cis 9-demethyl retinal, an analogue of retinal lacking the 9-methyl group. Meta II decay was four to five times slower and subsequent retinol production was three to four times slower in red-sensitive cones lacking the 9-methyl group of retinal. This was accompanied by a significant slowing of the recovery from saturation in cones lacking the 9-methyl group after exposure to bright (>0.1% visual pigment photoactivated) but not dim light. A mathematical model of the turn-off process of phototransduction revealed that the slower recovery of photoresponse can be explained by slower Meta decay of 9-demethyl visual pigment. These results demonstrate that the 9-methyl group of retinal is required for steric chromophore–opsin interactions that favor both the rapid decay of Meta II and the rapid response recovery after exposure to bright light in red-sensitive cones

Visual Cycle: Dependence of Retinol Production and Removal on Photoproduct Decay and Cell Morphology

The visual cycle is a chain of biochemical reactions that regenerate visual pigment following exposure to light. Initial steps, the liberation of all-trans retinal and its reduction to all-trans retinol by retinol dehydrogenase (RDH), take place in photoreceptors. We performed comparative microspectrophotometric and microfluorometric measurements on a variety of rod and cone photoreceptors isolated from salamander retinae to correlate the rates of photoproduct decay and retinol production. Metapigment decay rate was spatially uniform within outer segments and 50–70 times faster in the cells that contained cone-type pigment (SWS2 and M/LWS) compared to cells with rod-type pigment (RH1). Retinol production rate was strongly position dependent, fastest at the base of outer segments. Retinol production rate was 10–40 times faster in cones with cone pigments (SWS2 and M/LWS) than in the basal OS of rods containing rod pigment (RH1). Production rate was approximately five times faster in rods containing cone pigment (SWS2) than the rate in basal OS of rods containing the rod pigment (RH1). We show that retinol production is defined either by metapigment decay rate or RDH reaction rate, depending on cell type or outer segment region, whereas retinol removal is defined by the surface-to-volume ratio of the outer segment and the availability of retinoid binding protein (IRBP). The more rapid rates of retinol production in cones compared to rods are consistent with the more rapid operation of the visual cycle in these cells

Suomen maatalous ja maaseutuelinkeinot 1998

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