Quantum Catch Research Articles

Photoreceptors, visual pigments, and ellipsosomes in the killifish, Fundulus heteroclitus: a microspectrophotometric and histological study.

The photoreceptor layer of F. heteroclitus was examined by light and electron microscopy. We identified four cone visual pigments with maximum absorbance (lambda(max)) in the UV (363 nm), short (400 nm), middle (463 nm), and long (563 nm) wavelength regions of the spectrum and a rod visual pigment that peaked in the middle wavelengths (503 nm). Electron-dense bodies, ellipsosomes and pseudoellipsosomes, were present in the distal ellipsoids of long/middle (L/M) and long/long (L/L) wavelength double cones and in single short wavelength (S) cones, respectively. The light absorption of ellipsosomes indicated the presence of reduced cytochrome-c with the highest optical densities found in the M members of L/M double cones. By contrast, S cones contained pseudo-ellipsosomes which had very low optical density. UV cones were present everywhere as part of square or row mosaics in the retina of F. heteroclitus. Cone packing was on average higher for locations in the upper half of the retina while the highest cone density was found in the centro-ventral retina. An analysis of potential quantum catches for each cone type as a function of retinal sector and underwater irradiance characteristics revealed higher overall quantum catches for cones in the upper retina when the light field was assumed homogeneous, and higher quantum catches for cones in the lower retina when downwelling, horizontal, and upwelling irradiances were considered separately. At dusk, quantum catch was highest for M cones and the contribution to the overall retinal quantum catch by UV and S cones was much greater than during daylight hours. We propose that UV and S cones may be used to detect targets of interest against the background irradiance sensed by double cones.

Colourful objects through animal eyes

To understand how bees, birds, and fish may use colour vision for food selection and mate choice, we reconstructed views of biologically important objects taking into account the receptor spectral sensitivities. Reflectance spectra a of flowers, bird plumage, and fish skin were used to calculate receptor quantum catches. The quantum catches were then coded by red, green, and blue of a computer monitor; and powers, birds, and fish were visualized in animal colours. Calculations were performed for different illumination conditions. To simulate colour constancy, we used a von Kries algorithm, i.e., the receptor quantum catches were scaled so that the colour of illumination remained invariant. We show that on land this algorithm compensates reasonably well for changes of object appearance caused by natural changes of illumination, while in water failures of von Kries colour constancy are prominent. (C) 2000 John Wiley & Sons, Inc

Photoreceptor performance and the co-ordination of achromatic and chromatic inputs in the fly visual system

White noise techniques are used to compare the two photoreceptor sub-types in blowfly retina, the short visual fibres (R1-6) that code achromatic contrast, and the long visual fibres (R7 and R8) that together code wavelength distribution and polarisation plane. Measurements of signal and noise spectra and contrast gain, taken across a broad intensity range, permit a detailed comparison of coding efficiency under natural conditions of illumination. As a function of excitation (effective photons per photoreceptor per second; hυ/rec per s), adaptive changes in the long and short visual fibres are similar, suggesting that post-rhodopsin their phototransduction cascades are identical. Under identical natural daylight conditions (photons per cm 2 per second; hυ/cm 2 per s) short visual fibres catch more photons, thus operating with a higher signal to noise ratio and faster response, to consistently outperform the long visual fibres. Long visual fibres compensate for their poor quantum catch by having a higher absolute gain (mV/hυ) which at low light intensities enables them to achieve a level of contrast gain (mV/unit contrast) similar to the short visual fibres. Differences in signal to noise ratios are related to known differences in photoreceptor structure and synaptic frequency among visual interneurons. The principles of matching sensitivity and synapse number to quantum catch described here could explain analogous differences between chromatic and achromatic pathways in mammalian and amphibian retinas.

Trichromatic colour vision in the hummingbird hawkmoth, Macroglossum stellatarum L.

Hymenopterans have long been shown to choose colours by means of the spectral distribution and independently of the intensity (true colour vision). The same ability has only very recently been proven for two butterfly species. We present evidence for the existence of true colour vision in the European hummingbird hawkmoth, Macroglossum stellatarum. Moths were trained in dual-choice situations to spectral lights of a rewarding and an unrewarding wavelength. After training, unrewarded tests were performed during which the intensities of the lights were changed. The results confirm that the species has three spectral receptor types and uses true colour vision when learning the colour of a food source. If colour vision is not possible since only one receptor type is receiving input from both stimuli, the moths learn to associate some achromatic cue correlated to the receptor quantum catch, with the reward. The moths learn spectral cues rapidly and choose correctly after one to several rewarded visits even when trained to different colours in sequence.

Morphological changes in the retina of Aequidens pulcher (Cichlidae) after rearing in monochromatic light

We investigate the processing of chromatic information in the outer retina of a cichlid fish, Aequidens pulcher. The colour opponent response characteristics of some classes of cone-specific horizontal cells in the fish retina are the result of feedforward–feedback loops with cone photoreceptors. To interfere with the reciprocal transmissions of signals, animals were reared in monochromatic lights which preferentially stimulated the spectrally different cone types. Here we report the effects on the cones. Their absorbance spectra were largely unaffected, indicating no change in photopigment gene expression. Significant changes were observed in the cone outer segment lengths and the frequencies of spectral cone types. Quantum catch efficiency and survival of cones appear to be controlled in a spectrally selective way. Our results suggest that the retina responds to spectral deprivation in a compensatory fashion aimed at balancing the input from the different cone types to second order neurons.

Statistics of cone responses to natural images: implications for visual coding

We gathered hyperspectral images of natural, foliage-dominated scenes and converted them to human cone quantal catches to characterize the second-order redundancy present within the retinal photoreceptor array under natural conditions. The data are expressed most simply in a logarithmic response space, wherein an orthogonal decorrelation robustly produces three principal axes, one corresponding to simple changes in radiance and two that are reminiscent of the blue–yellow and red–green chromatic-opponent mechanisms found in the primate visual system. Further inclusion of spatial stimulus dimensions demonstrates a complete spatial decorrelation of these three cone-space axes in natural cone responses.

Circadian rhythms in the horseshoe crab lateral eye: signal transduction and photostasis

The visual system of the horseshoe crab has been an important model system for studies of basic visual processes. It has been particularly useful for understanding the role of efferent feedback and circadian rhythms in vision. Among the many retinal effects of circadian efferent activity is the priming of the daily shedding of photosensitive membrane. This daily event is triggered from the absorption of light by rhodopsin through the phospholipase C/diacylglycerol/protein kinase C cascade also requiring elevated cytosolic calcium released by inositol trisphosphate. The purpose of the daily shedding of photoreceptive rhabdomeral membrane, however, is far from clear. Recently, animals have been discovered at hydrothermal vents in the deep sea that have large photoreceptors and copious amounts of rhabdom but no apparent mechanisms for shedding and synthesizing this membrane array. Since these animals see no cyclic lighting from daylight, the absence of rhabdom shedding is consistent with the suggestion that rhabdom shedding is a homeostatic mechanism for maintaining photostasis (constancy of daily quantum catch). This hypothesis is also consistent with recent experimental data from ongoing studies in the horseshoe crab.

Equivalence of background and bleaching desensitization in isolated rod photoreceptors of the larval tiger salamander.

Psychophysical experiments have shown an equivalence between sensitivity reduction by background light and by bleaches for the human scotopic system. We have compared the effects of backgrounds and bleaches on the light-sensitive membrane-current responses of isolated rod photoreceptors from the salamander Ambystoma tigrinum. The quantum catch loss was factored out from the desensitization due to bleaching to give the fraction of "extra" desensitization due to adaptation. For backgrounds, desensitization is well described by the Weber/Fechner equation. The extra desensitization after bleaches can also be described by the Weber/Fechner equation, if an "equivalent" background produced by bleaching is made linearly proportional to the fraction of pigment bleached. A background which produces an extra desensitization of a factor of two is equivalent to a fractional bleach of approximately 6%. Equivalent background and bleaching desensitizations were associated with similar reductions in circulating current. There is a linear relation between log flash sensitivity and decrease in circulating current. Equivalent background and bleaching desensitizations were associated with similar increases in cGMP phosphodiesterase and guanylate cyclase activity. These were inferred from membrane current changes after steps into lithium or IBMX solutions. There were also similar reductions in the integration times of dim flash responses for equivalent desensitizations produced by backgrounds and bleaches. These results suggest that the equivalence between background and bleaching found psychophysically may arise at the very earliest stages of visual processing and that these two processes of desensitization have similar underlying mechanisms.

A new psychophysical method for determining the photopic spectral-luminosity function of the human eye.

Using an 8 mm pupil, 2AFC-method, and 2 x 2 deg2 grating at 2 c/deg we measured contrast sensitivity as a function of integrated radiance for a series of interference filters with peak wavelengths at 400-700 nm. Irrespective of the radiance level, contrast sensitivity was highest when wavelength was at and around 550 nm. It decreased towards longer and shorter wavelengths, reflecting the variation of the probability of quantal catch with light wavelength. When contrast sensitivity functions plotted in double logarithmic coordinates were shifted horizontally by multiplying the integrated radiances of each filter by an appropriate scaling factor, the functions superimposed onto a single curve. Contrast sensitivity at lower levels of relative radiance (R) increased in proportion to square root of R, obeying DeVries-Rose law, but at higher levels contrast sensitivity was constant, obeying Weber's law. Scaling factors plotted as a function of wavelength provided an estimate of V(lambda) quite similar to the standard 2 deg photopic spectral-luminosity function of CIE 1924.

Role of cytoplasmic calcium concentration in the bleaching adaptation of salamander cone photoreceptors.

1. In order to study the possible involvement of Ca2+ in the bleaching adaptation of cones isolated from the retina of the salamander Ambystoma tigrinum, changes in cytoplasmic calcium concentration ([Ca2+]i were opposed by exposing the outer segment to a low-Ca(2+)-O Na+ solution designed to minimize Ca2+ fluxes across the outer segment membrane. 2. When a cone was exposed in normal Ringer solution to bright light bleaching a significant fraction of the photopigment, the circulating current was initially suppressed completely and then recovered to a maintained value less than the value in darkness before the bleach. When the outer segment of the cone was stepped to low-Ca(2+)-O Na+ solution before the bleach was delivered, the circulating current recovered more slowly or (for large bleaches) remained completely suppressed for the duration of the solution exposure. 3. If, during the period for which the current was suppressed in low-Ca(2+)-O Na+ solution, the cone outer segment was exposed to the phosphodiesterase inhibitor 3-isobutyl-1-methylxanthine (IBMX), the circulating current was restored. The dim flash response recorded under these conditions exhibited kinetics and integration times similar to those recorded in low-Ca(2+)-O Na+ solution in darkness before the bleach. If, instead, the outer segment was returned to Ringer solution after the bleach, thereby allowing [Ca2+]i to fall from its dark-adapted level to the appropriate bleach-adapted level, the kinetics of the response in low-Ca(2+)-O Na+ solution were greatly accelerated, and the integration time considerably reduced. This was true regardless of whether or not the low-Ca(2+)-O Na+ solution included IBMX. 4. The role of Ca2+ in bleaching adaptation appeared to resemble its role in background adaptation, since in both cases exposure to low-Ca(2+)-O Na+ solution suppressed the acceleration of response kinetics. Responses recorded from cones in low-Ca(2+)-O Na+ solution were nearly identical in waveform and sensitivity during background light or after bleaches, provided that IBMX was used to restore sufficient photocurrent so that responses to flashes could be recorded, and sensitivity was corrected for loss in quantum catch. 5. These results indicate that the fall in [Ca2+]i in cones after a bleach is necessary both for the acceleration of the flash response and the adaptational decrease in sensitivity, as is the case for adaptation by background light.

Light adaptation and the rising phase of the flash photocurrent of salamander retinal rods.

1. Both theory and analysis of photocurrents in retinal rods show that phosphodiesterase activity after a flash rises initially as a delayed ramp. 2. The effect of light adaptation on the flash-induced rise in phosphodiesterase activity deduced from photocurrent responses was investigated. 3. Background adaptation reduces the deduced rate of rise of phosphodiesterase activity. The effect is most prominent for bright backgrounds and moderate flashes. There is little reduction for bright flashes, even in bright backgrounds. There is no effect for weak backgrounds. 4. Light adaptation after bleaching visual pigment produces a reduction in the deduced rise of phosphodiesterase activity for all flashes. For bright flashes, the reduction is explained by the reduction in quantum catch. For moderate flashes, there is an extra reduction, similar to the reduction produced by the equivalent background. 5. The results provide support for the idea that a reduction in the amplification step of phototransduction functions as part of the mechanism of light adaptation in rods. The dependence on flash intensity of the background-induced reduction in phosphodiesterase activation could imply a feedback mechanism on the activation steps of phototransduction.

Dark-adapted thresholds at 10- and 30-deg eccentricities in 10-week-old infants.

We tested the hypothesis that the dark-adapted sensitivity of the near central retina is lower than that of peripheral retina in 10-week-old infants. A spatial two alternative forced-choice psychophysical method was used to estimate the threshold for 2-deg spots presented 10 deg and 30 deg from the center of a screen. Each 10-week-old infant (n = 11) and adult (n = 5) subject was tested at both eccentricities. Every infant's threshold at 10 deg is higher than that at 30 deg. The median difference between the infants' thresholds at 10 deg and 30 deg is about 0.5 log unit. Whereas the scotopic thresholds of adults at 10 deg and 30 deg are virtually identical, the thresholds of infants' near central retina are higher than those in more peripheral retina. Delayed maturation of the near central rod outer segments with consequent lower quantum catch may be the primary determinant of this infantile sensitivity pattern.

Color constancy. I. Basic theory of two-stage linear recovery of spectral descriptions for lights and surfaces.

Changing a scene's illuminant causes the chromatic properties of reflected lights to change. This change in the lights from surfaces provides spectral information about surface reflectances and illuminants. We examine conditions under which these properties may be recovered by using bilinear models. Necessary conditions that follow from comparing the number of equations and the number of unknowns in the recovery procedure are not sufficient for unique recovery. Necessary and sufficient conditions follow from demanding a one-to-one relationship between quantum catch data and sets of lit surfaces. We present an algorithm for determining whether spectral descriptions of lights and surfaces can be recovered uniquely from reflected lights.

Visual pigment bleaching in isolated salamander retinal cones. Microspectrophotometry and light adaptation.

Visual pigment bleaching desensitizes rod photoreceptors greatly in excess of that due to loss of quantum catch. Whether this phenomenon also occurs in cone photoreceptors was investigated for isolated salamander red-sensitive cones. In parallel experiments, (a) visual pigment depletion by steps of bleaching light was measured by microspectrophotometry, and (b) flash sensitivity was measured by recording light-sensitive membrane current. In isolated cones, visual pigment bleaching permanently reduced flash sensitivity significantly below that due to the reduction in quantum catch, and there was little spontaneous recovery of visual pigment. The "extra" desensitization due to bleaching was most prominent up to bleaches of approximately 80% visual pigment and reached a level approximately 1 log unit beyond that due to loss of quantum catch. At higher bleaches, the effect of loss of quantum catch became more important. Bleaching did not greatly reduce the maximum light-suppressible membrane current. A 99% reduction of the visual pigment permanently reduced the circulating current by only 30%. Visual pigment bleaching speeded up the kinetics of dim flash responses. All electrical effects of bleaching were reversed on exposure to 11-cis retinal, which probably caused visual pigment regeneration. Light adaptation in photopic vision is known to involve significant visual pigment depletion. The present results indicate that cones operate with a maintained circulating current even after a large pigment depletion. It is shown how Weber/Fechner behavior may still be observed in photopic vision when the contributions of bleaching to adaptation are included.

Analysis of Rayleigh match data with psychometric functions.

Color matches have been used for a variety of purposes, yet the psychometric properties of color-matching data have not been thoroughly investigated. A method is given for generating psychometric functions for the two ends of the color-matching range by use of a perceptual dimension for stimulus magnitude based on ratios of cone quantal catches. The analysis was applied to Rayleigh match data gathered from 250 naïve observers with an automated protocol. Slopes of the psychometric functions were significantly shallower for anomalous trichromats than for normal trichromats, consistent with the assumption that stimulus magnitude is based on ratios of cone quantal catches. These results indicate that the tester's criterion for response consistency can strongly affect Rayleigh match widths. The analysis may also be useful for other perceptual tasks, such as contrast matching and spatial alignment.

Foveal cone detection statistics in color-normals and dichromats

We measured for six male observers, the psychometric functions for the detection of two simultaneously presented points of light. The test stimuli were two 1 min point sources separated by 17 min arc, and pulsed for 0.5 msec. The stimuli varied in wavelength from 500 to 620 nm. The psychometric functions were fit with a model that assumes ideal detection and the following properties: (1) Poisson-distributed quantal absorptions; (2) binomial sampling of foveal long-wavelength-sensitive (LWS) and middle-wavelength-sensitive (MWS) cones; (3) independent responses of the LWS and MWS cones; and (4) the Smith-Pokorny fundamentals for cone spectral sensitivies. Based on χ 2 fits to the psychometric functions for detecting neither, one or both of the two-point stimuli presented, estimates were derived for the minimum quantal catch by a single cone for detection ( C), the number of effective cones illuminated by a point stimulus at threshold ( N) and the proportion of central foveal cones of the LWS type ( P L ). Three observers were color-normal, two were protanopes and one was a deuteranope. A second deuteranope was included in the design but his data were too unreliable for an unambigous solution. The estimated quantal requirement C was consistently near 5 (4–6), and the effective number of illuminated cones always was 1 or 2. The plausible range of P L (98% confidence interval) for the color-normal observers was 0.48–0.68 (observer YY), 0.76–0.90 (observer MW) and 0.77–0.95 (observer DF). The best fitting P L solution for these observers were 0.61, 0.82 and 0.88, respectively. These were comparable to the values obtained from flicker photometric data. The best P L value for each of the protanopes was 0.00 and for the deuteranope the best P L value was 0.98.

Effect of bleached rhodopsin on signal amplification in rod visual receptors

Bleaching of rhodopsin markedly desensitizes the vertebrate visual system during a subsequent period of dark adaptation. Previous studies have indicated an origin of bleaching desensitization in the visual pigment itself, but have not identified the mechanism of action. A candidate for the site at which densensitization is initially expressed is the activation of transducin (formation of T*) on the rod disk membranes; this reaction directly involves rhodopsin in its photoactivated (R*) form and mediates initial amplification of the visual signal (reviewed in refs 7-9). We have analysed the effect of bleaching on the sensitivity of a flash-induced light-scattering signal known to monitor the disk-based amplifier, and which has been established as specifically monitoring transducin activation. We have recorded this signal from functioning retinal rods in situ ('ATR' signal) and find that bleaches inducing a pronounced, sustained loss in rod electrophysiological sensitivity do not alter the sensitivity of the ATR response after correction for reduced quantum catch. Our results indicate that the biochemical gain of the R*----T* transduction stage remains unchanged in the presence of bleached pigment and implicate a subsequent reaction as the first to show a sustained, bleaching-dependent gain reduction.

Infant spatiotemporal vision: Dependence of spatial contrast sensitivity on temporal frequency

Effects of temporal frequency on infant spatial contrast sensitivity were studied with forcedchoice preferential looking, using localized 1.0 and 0.35 c/deg grating patches. Between 4 and 8 months, contrast sensitivity at 1.0 c/deg increased significantly at 8–17 Hz but showed little change at 2–4 Hz, so temporal tuning became increasingly bandpass with age. At 4 months, temporal tuning was lowpass at 1.0 c/deg and bandpass at 0.35 c/deg. Control data on adults indicate that the differences between the infant and adult data cannot be accounted for solely by reduced photoreceptor density and quantal catch, and suggest developmental changes in tuning and/or relative sensitivities of spatiotemporal mechanisms.,

The role of sensory adaptation in the retina.

Adaptation, a change in response to a sustained stimulus, is a widespread property of sensory systems, occurring at many stages, from the most peripheral energy-gathering structures to neural networks. Adaptation is also implemented at many levels of biological organization, from the molecule to the organ. Despite adaptation's diversity, it is fruitful to extract some unifying principles by considering well-characterized components of the insect visual system. A major function of adaptation is to increase the amount of sensory information an organism uses. The amount of information available to an organism is ultimately defined by its environment and its size. The amount of information collected depends upon the ways in which an organism samples and transduces signals. The amount of information that is used is further limited by internal losses during transmission and processing. Adaptation can increase information capture and reduce internal losses by minimizing the effects of physical and biophysical constraints. Optical adaptation mechanisms in compound eyes illustrate a common trade-off between energy (quantum catch) and acuity (sensitivity to changes in the distribution of energy). This trade-off can be carefully regulated to maximize the information gathered (i.e. the number of pictures an eye can reconstruct). Similar trade-offs can be performed neurally by area summation mechanisms. Light adaptation in photoreceptors introduces the roles played by cellular constraints in limiting the available information. Adaptation mechanisms prevent saturation and, by trading gain for temporal acuity, increase the rate of information uptake. By minimizing the constraint of nonlinear summation (imposed by membrane conductance mechanisms) a cell's sensitivity follows the Weber-Fechner law. Thus, a computationally advantageous transformation is generated in response to a cellular constraint. The synaptic transfer of signals from photoreceptors to second-order neurones emphasizes that the cellular constraints of nonlinearity, noise and dynamic range limit the transmission of information from cell to cell. Synaptic amplification is increased to reduce the effects of noise but this resurrects the constraint of dynamic range. Adaptation mechanisms, both confined to single synapses and distributed in networks, remove spatially and temporally redundant signal components to help accommodate more information within a single cell. The net effect is a computationally advantageous removal of the background signal. Again, the cellular constraints on information transfer have dictated a computationally advantageous operation.

“Tho’ she kneel’d in that place where they grew…” The uses and origins of primate colour vision

The disabilities experienced by colour-blind people show us the biological advantages of colour vision in detecting targets, in segregating the visual field and in identifying particular objects or states. Human dichromats have especial difficulty in detecting coloured fruit against dappled foliage that varies randomly in luminosity; it is suggested that yellow and orange tropical fruits have co-evolved with the trichromatic colour vision of Old World monkeys. It is argued that the colour vision of man and of the Old World monkeys depends on two subsystems that remain parallel and independent at early stages of the visual pathway. The primordial subsystem, which is shared with most mammals, depends on a comparison of the rates of quantum catch in the short- and middle-wave cones; this system exists almost exclusively for colour vision, although the chromatic signals carry with them a local sign that allows them to sustain several of the functions of spatiochromatic vision. The second subsystem arose from the phylogenetically recent duplication of a gene on the X-chromosome, and depends on a comparison of the rates of quantum catch in the long- and middle-wave receptors. At the early stages of the visual pathway, this chromatic information is carried by a channel that is also sensitive to spatial contrast. The New World monkeys have taken a different route to trichromacy: in species that are basically dichromatic, heterozygous females gain trichromacy as a result of X-chromosome inactivation, which ensures that different photopigments are expressed in two subsets of retinal photoreceptor.