A frog's eye view: Foundational revelations and future promises.

From the mid-19th century until the 1980's, frogs and toads provided important research models for many fundamental questions in visual neuroscience. In the present century, they have been largely neglected. Yet they are animals with highly developed vision, a complex retina built on the basic vertebrate plan, an accessible brain, and an experimentally useful behavioural repertoire. They also offer a rich diversity of species and life histories on a reasonably restricted physiological and evolutionary background. We suggest that important insights may be gained from revisiting classical questions in anurans with state-of-the-art methods. At the input to the system, this especially concerns the molecular evolution of visual pigments and photoreceptors, at the output, the relation between retinal signals, brain processing and behavioural decision-making.

Temporal vision: measures, mechanisms and meaning.

Time is largely a hidden variable in vision. It is the condition for seeing interesting things such as spatial forms and patterns, colours and movements in the external world, and yet is not meant to be noticed in itself. Temporal aspects of visual processing have received comparatively little attention in research. Temporal properties have been made explicit mainly in measurements of resolution and integration in simple tasks such as detection of spatially homogeneous flicker or light pulses of varying duration. Only through a mechanistic understanding of their basis in retinal photoreceptors and circuits can such measures guide modelling of natural vision in different species and illuminate functional and evolutionary trade-offs. Temporal vision research would benefit from bridging traditions that speak different languages. Towards that goal, I here review studies from the fields of human psychophysics, retinal physiology and neuroethology, with a focus on fundamental constraints set by early vision.

Dark-adaptation in the eyes of a lake and a sea population of opossum shrimp (Mysis relicta): retinoid isomer dynamics, rhodopsin regeneration, and recovery of light sensitivity.

We have studied dark-adaptation at three levels in the eyes of the crustacean Mysis relicta over 2-3 weeks after exposing initially dark-adapted animals to strong white light: regeneration of 11-cis retinal through the retinoid cycle (by HPLC), restoration of native rhodopsin in photoreceptor membranes (by MSP), and recovery of eye photosensitivity (by ERG). We compare two model populations ("Sea", Sp, and "Lake", Lp) inhabiting, respectively, a low light and an extremely dark environment. 11-cis retinal reached 60-70% of the pre-exposure levels after 2 weeks in darkness in both populations. The only significant Lp/Sp difference in the retinoid cycle was that Lp had much higher levels of retinol, both basal and light-released. In Sp, rhodopsin restoration and eye photoresponse recovery parallelled 11-cis retinal regeneration. In Lp, however, even after 3 weeks only ca. 25% of the rhabdoms studied had incorporated new rhodopsin, and eye photosensitivity showed only incipient recovery from severe depression. The absorbance spectra of the majority of the Lp rhabdoms stayed constant around 490-500 nm, consistent with metarhodopsin II dominance. We conclude that sensitivity recovery of Sp eyes was rate-limited by the regeneration of 11-cis retinal, whilst that of Lp eyes was limited by inertia in photoreceptor membrane turnover.

Photoreceptors and eyes of pikeperch Sander lucioperca, pike Esox lucius, perch Perca fluviatilis and roach Rutilus rutilus from a clear and a brown lake.

The photoreceptors and eyes of four fish species commonly cohabiting Fennoscandian lakes with different light transmission properties were compared: pikeperch Sander lucioperca, pike Esox lucius, perch Perca fluviatilis and roach Rutilus rutilus. Each species was represented by individuals from a clear (greenish) and a humic (dark brown) lake in southern Finland: Lake Vesijärvi (LV; peak transmission around 570 nm) and Lake Tuusulanjärvi (LT; peak transmission around 630 nm). In the autumn, all species had almost purely A2-based visual pigments. Rod absorption spectra peaked at c.526 nm (S. lucioperca), c. 533 nm (E. lucius) and c. 540 nm (P. fluviatilis and R. rutilus), with no differences between the lakes. Esox lucius rods had remarkably long outer segments, 1.5-2.8-fold longer than those of the other species. All species possessed middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) cone pigments in single, twin or double cones. Rutilus rutilus also had two types of short-wavelength sensitive (SWS) cones: UV-sensitive [SWS1] and blue-sensitive (SWS2) cones, although in the samples from LT no UV cones were found. No other within-species differences in photoreceptor cell complements, absorption spectra or morphologies were found between the lakes. However, E. lucius eyes had a significantly lower focal ratio in LT compared with LV, enhancing sensitivity at the expense of acuity in the dark-brown lake. Comparing species, S. lucioperca was estimated to have the highest visual sensitivity, at least two times higher than similar-sized E. lucius, thanks to the large relative size of the eye (pupil) and the presence of a reflecting tapetum behind the retina. High absolute sensitivity will give a competitive edge also in terms of short reaction times and long visual range.

Increasing the illumination slowly over several weeks protects against light damage in the eyes of the crustacean Mysis relicta.

The eyes of two glacial-relict populations of opossum shrimp Mysis relicta inhabiting the different photic environments of a deep, dark-brown freshwater lake and a variably lit bay of the Baltic Sea differ in their susceptibility to functional depression from strong light exposures. The lake population is much more vulnerable than the sea population. We hypothesized that the difference reflects physiological adaptation mechanisms operating on long time scales rather than genetically fixed differences between the populations. To test this, we studied how acclimation to ultra-slowly increased illumination (on time scales of several weeks to months) affected the resilience of the eyes to bright-light exposures. Light responses of whole eyes were measured by electroretinography, the visual-pigment content of single rhabdoms by microspectrophotometry and the structural integrity of photoreceptor cells by electron microscopy (EM). Slow acclimation mitigated and even abolished the depression of photoresponsiveness caused by strong light exposures, making a dramatic difference especially in the lake animals. Still, acclimation in the sea animals was faster and the EM studies suggested intrinsic differences in the dynamics of microvillar membrane cycling. In conclusion, we report a novel form of physiological adaptation to general light levels, effective on the time scale of seasonal changes. It explains part but not all of the differences in light tolerance between the lake and sea populations.

Eye spectral sensitivity in fresh- and brackish-water populations of three glacial-relict Mysis species (Crustacea): physiology and genetics of differential tuning.

Absorbance spectra of single rhabdoms were studied by microspectrophotometry (MSP) and spectral sensitivities of whole eyes by electroretinography (ERG) in three glacial-relict species of opossum shrimps (Mysis). Among eight populations from Fennoscandian fresh-water lakes (L) and seven populations from the brackish-water Baltic Sea (S), L spectra were systematically red-shifted by 20-30 nm compared with S spectra, save for one L and one S population. The difference holds across species and bears no consistent adaptive relation to the current light environments. In the most extensively studied L-S pair, two populations of M. relicta (L(p) and S(p)) separated for less than 10,000 years, no differences translating into amino acid substitutions have been found in the opsin genes, and the chromophore of the visual pigments as analyzed by HPLC is pure A1. However, MSP experiments with spectrally selective bleaching show the presence of two rhodopsins (λ(max) ≈ 525-530 nm, MWS, and 565-570 nm, LWS) expressed in different proportions. ERG recordings of responses to "red" and "blue" light linearly polarized at orthogonal angles indicate segregation of the pigments into different cells differing in polarization sensitivity. We propose that the pattern of development of LWS and MWS photoreceptors is governed by an ontogenetic switch responsive to some environmental signal(s) other than light that generally differ(s) between lakes and sea, and that this reaction norm is conserved from a common ancestor of all three species.

Opsin gene sequence variation across phylogenetic and population histories in Mysis (Crustacea: Mysida) does not match current light environments or visual-pigment absorbance spectra.

The hypothesis that selection on the opsin gene is efficient in tuning vision to the ambient light environment of an organism was assessed in 49 populations of 12 Mysis crustacean species, inhabiting arctic marine waters, coastal littoral habitats, freshwater lakes ('glacial relicts') and the deep Caspian Sea. Extensive sequence variation was found within and among taxa, but its patterns did not match expectations based on light environments, spectral sensitivity of the visual pigment measured by microspectrophotometry or the history of species and populations. The main split in the opsin gene tree was between lineages I and II, differing in six amino acids. Lineage I was present in marine and Caspian Sea species and in the North American freshwater Mysis diluviana, whereas lineage II was found in the European and circumarctic fresh- and brackish-water Mysis relicta, Mysis salemaai and Mysis segerstralei. Both lineages were present in some populations of M. salemaai and M. segerstralei. Absorbance spectra of the visual pigment in nine populations of the latter three species showed a dichotomy between lake (λ(max) =554-562 nm) and brackish-water (Baltic Sea) populations (λ(max) = 521-535 nm). Judged by the shape of spectra, this difference was not because of different chromophores (A2 vs. A1), but neither did it coincide with the split in the opsin tree (lineages I/II), species identity or current light environments. In all, adaptive evolution of the opsin gene in Mysis could not be demonstrated, but its sequence variation did not conform to a neutral expectation either, suggesting evolutionary constraints and/or unidentified mechanisms of spectral tuning.

Spectral tuning by selective chromophore uptake in rods and cones of eight populations of nine-spined stickleback (Pungitius pungitius).

The visual pigments of rods and cones were studied in eight Fennoscandian populations of nine-spined stickleback (Pungitius pungitius). The wavelength of maximum absorbance of the rod pigment (λ(max)) varied between populations from 504 to 530 nm. Gene sequencing showed that the rod opsins of all populations were identical in amino acid composition, implying that the differences were due to varying proportions of chromophores A1 and A2. Four spectral classes of cones were found (two S-cones, M-cones and L-cones), correlating with the four classes of vertebrate cone pigments. For quantitative estimation of chromophore proportions, we considered mainly rods and M-cones. In four populations, spectra of both photoreceptor types indicated A2 dominance (population mean λ(max)=525-530 nm for rods and 535-544 nm for M-cones). In the four remaining populations, however, rod spectra (mean λ(max)=504-511 nm) indicated strong A1 dominance, whereas M-cone spectra (mean λ(max)=519-534 nm) suggested substantial fractions of A2. Quantitative analysis of spectra by three methods confirmed that rods and cones in these populations use significantly different chromophore proportions. The outcome is a shift of M-cone spectra towards longer wavelengths and a better match to the photic environment (light spectra peaking >560 nm in all the habitats) than would result from the chromophore proportions of the rods. Chromophore content was also observed to vary partly independently in M- and L-cones with potential consequences for colour discrimination. This is the first demonstration that selective processing of chromophore in rods and cones, and in different cone types, may be ecologically relevant.

Rod phototransduction determines the trade-off of temporal integration and speed of vision in dark-adapted toads.

Human vision is approximately 10 times less sensitive than toad vision on a cool night. Here, we investigate (1) how far differences in the capacity for temporal integration underlie such differences in sensitivity and (2) whether the response kinetics of the rod photoreceptors can explain temporal integration at the behavioral level. The toad was studied as a model that allows experimentation at different body temperatures. Sensitivity, integration time, and temporal accuracy of vision were measured psychophysically by recording snapping at worm dummies moving at different velocities. Rod photoresponses were studied by ERG recording across the isolated retina. In both types of experiments, the general timescale of vision was varied by using two temperatures, 15 and 25 degrees C. Behavioral integration times were 4.3 s at 15 degrees C and 0.9 s at 25 degrees C, and rod integration times were 4.2-4.3 s at 15 degrees C and 1.0-1.3 s at 25 degrees C. Maximal behavioral sensitivity was fivefold lower at 25 degrees C than at 15 degrees C, which can be accounted for by inability of the "warm" toads to integrate light over longer times than the rods. However, the long integration time at 15 degrees C, allowing high sensitivity, degraded the accuracy of snapping toward quickly moving worms. We conclude that temporal integration explains a considerable part of all variation in absolute visual sensitivity. The strong correlation between rods and behavior suggests that the integration time of dark-adapted vision is set by rod phototransduction at the input to the visual system. This implies that there is an inexorable trade-off between temporal integration and resolution.

Individual variation in rod absorbance spectra correlated with opsin gene polymorphism in sand goby (Pomatoschistus minutus).

Rod absorbance spectra, characterized by the wavelength of peak absorbance (lambda(max)) were related to the rod opsin sequences of individual sand gobies (Pomatoschistus minutus) from four allopatric populations [Adriatic Sea (A), English Channel (E), Swedish West Coast (S) and Baltic Sea (B)]. Rod lambda(max) differed between populations in a manner correlated with differences in the spectral light transmission of the respective water bodies [lambda(max): (A) approximately 503 nm; (E and S) approximately 505-506 nm; (B) approximately 508 nm]. A distinguishing feature of B was the wide within-population variation of lambda(max) (505.6-511.3 nm). The rod opsin gene was sequenced in marked individuals whose rod absorbance spectra had been accurately measured. Substitutions were identified using EMBL/GenBank X62405 English sand goby sequence as reference and interpreted using two related rod pigments, the spectrally similar one of the Adriatic P. marmoratus (lambda(max) approximately 507 nm) and the relatively red-shifted Baltic P. microps (lambda(max) approximately 515 nm) as outgroups. The opsin sequence of all E individuals was identical to that of the reference, whereas the S and B fish all had the substitution N151N/T or N151T. The B fish showed systematic within-population polymorphism, the sequence of individuals with lambda(max) at 505.6-507.5 nm were identical to S, but those with lambda(max) at 509-511.3 nm additionally had F261F/Y. The substitution F261Y is known to red-shift the rod pigment and was found in all P. microps. We propose that ambiguous selection pressures in the Baltic Sea and/or gene flow from the North Sea preserves polymorphism and is phenotypically evident as a wide variation in lambda(max).

Modelling the effect of microsaccades on retinal responses to stationary contrast patterns.

We have modelled the effect of microsaccades on retinal responses to achromatic borders and lines using physiologically realistic parameters. Typical microsaccade movement sequences were applied to the retinal image of stationary spatial contrast patterns as projected on the foveal cone mosaic after being passed through the optical transfer function of the eye. The resulting temporal contrast modulation over a cone receptive field was convolved with an analytical expression for the response waveform of primate cones (photocurrent: [Schnapf, J. L., Nunn, B. J., Meister, M. & Baylor, D. A. (1990). Visual transduction in cones of the monkey Macaca fascicularis. Journal of Physiology, 427, 681-713]; photovoltage: [Schneeweis, D. M. & Schnapf, J. L. (1999). The photovoltage of macaque cone photoreceptors: Adaptation, noise, and kinetics. Journal of Neuroscience, 19, 1203-1216]). The input to the ganglion cell was derived from the cone responses by the difference-of-Gaussians receptive field model of Donner and Hemilä [Donner, K. & Hemilä, S. (1996). Modelling the spatio-temporal modulation response of ganglion cells with difference-of-Gaussians receptive fields: Relation to photoreceptor response kinetics. Visual Neuroscience, 13, 173-186]. The modelled response waveforms suggest that microsaccades may significantly enhance sensitivity to edges, "re-sharpen" the image and, most interestingly, improve resolution of two closely spaced lines. The reason is that fine spatial structure of the retinal image when moving at suitable velocities is translated into a correlated temporal structure of responses of single cones and ganglion cells. The information content of the signal is not strongly dependent on positional accuracy and the effect is thus distinct from the presumed retinal basis of vernier acuity. Other eye movements (drift) with velocity distributions similar to that of the microsaccade's slow return phase might be similarly useful, although the microsaccade has some distinguishing features that could be functionally significant, e.g., the neural motor control and the biphasic movement pattern.

Time course of suppression by surround gratings: highly contrast-dependent, but consistently fast.

Timing is critical for the effectiveness of a modulating surround signal. In this study, the optimal timing of a suppressing surround signal was measured psychophysically in human subjects. The perceived contrast of a fixated 1-deg circular patch of vertical sinusoidal grating (the target: 4 cpd, Michelson contrast 0.2) was measured as a function of the onset asynchrony between the target and an annular "surround" grating with the same orientation and spatial frequency. The contrast and area of the surround stimulus were varied parametrically. The suppressive signal peaked at earlier times the higher the surround contrast (0.1-0.4), following a function consistent with the contrast-dependence of retinal response dynamics. Increasing the area of the surround grating also moved peak suppression to earlier times. At ca. 2 deg annulus outer diameter the time to peak of the suppressive signal was shortest, although its amplitude grew with annulus area even beyond that. When both the contrast and the area of the centre and surround gratings were equal, suppression was maximal if the surround stimulus was presented ca. 5 ms before the target. Such a short delay of suppression is consistent with a neural implementation based on feedforward-feedback connections, but not with horizontal connections.

The dual rod system of amphibians supports colour discrimination at the absolute visual threshold.

The presence of two spectrally different kinds of rod photoreceptors in amphibians has been hypothesized to enable purely rod-based colour vision at very low light levels. The hypothesis has never been properly tested, so we performed three behavioural experiments at different light intensities with toads (Bufo) and frogs (Rana) to determine the thresholds for colour discrimination. The thresholds of toads were different in mate choice and prey-catching tasks, suggesting that the differential sensitivities of different spectral cone types as well as task-specific factors set limits for the use of colour in these behavioural contexts. In neither task was there any indication of rod-based colour discrimination. By contrast, frogs performing phototactic jumping were able to distinguish blue from green light down to the absolute visual threshold, where vision relies only on rod signals. The remarkable sensitivity of this mechanism comparing signals from the two spectrally different rod types approaches theoretical limits set by photon fluctuations and intrinsic noise. Together, the results indicate that different pathways are involved in processing colour cues depending on the ecological relevance of this information for each task.This article is part of the themed issue 'Vision in dim light'.

Efficiency of temporal integration of sinusoidal flicker.

PURPOSE: Detection efficiency for flickering stimuli of constant duration decreases with increasing temporal frequency. Increasing frequency in this case also implies increasing number of flicker cycles. The current study was conducted to investigate whether this result could be due to the limited ability of the central detector to integrate flicker cycles. METHODS: Flicker sensitivity was measured at 1 to 20 Hz in strong external temporal noise with increasing stimulus duration. RESULTS: Sensitivity increased with stimulus duration in a nonsaturating manner up to the longest exposure times used, indicating probability summation. When expressed in terms of detection efficiency (eta) as a function of number of cycles presented (n) all data could be modeled as a single decreasing function of the form eta=0.29n(-0.70). CONCLUSIONS: The results show that the number of cycles, not time, is the determinant of probability summation of flicker. The results are consistent with the idea that the central detector is a suboptimal matched filter spanning less than one cycle.

Noise frame duration, masking potency and whiteness of temporal noise.

PURPOSE: Because of the limited contrast range, increasing the duration of the noise frame is often the only option for increasing the masking potency of external, white temporal noise. This, however, reduces the high-frequency cutoff beyond which noise is no longer white. This study was conducted to determine the longest noise frame duration that produces the strongest masking effect and still mimics white noise on the detection of sinusoidal flicker. METHODS: Contrast energy thresholds (E(th)) were measured for flicker at 1.25 to 20 Hz in strong, purely temporal (spatially uniform), additive, external noise. The masking power of white external noise, characterized by its spectral density at zero frequency N0, increases with the duration of the noise frame. RESULTS: For short noise frame durations, E(th) increased in direct proportion to N0, keeping the nominal signal-to-noise ratio [SNR = (E(th)/N0)(0.5)] constant at threshold. The masking effect thus increased with the duration of the noise frame and the noise mimicked white noise. When noise frame duration and N0 increased further, the nominal SNR at threshold started to decrease, indicating that noise no longer mimicked white noise. The minimum number of noise frames per flicker cycle needed to mimic white noise decreased with increasing flicker frequency from 8.3 at 1.25 Hz to 1.6 at 20 Hz. CONCLUSIONS: The critical high-frequency cutoff of detection-limiting temporal noise in terms of noise frames per signal cycle depends on the temporal frequency of the signal. This is opposite to the situation in the spatial domain and must be taken into consideration when temporal signals are masked with temporal noise.

On the relation between the photoactivation energy and the absorbance spectrum of visual pigments.

We relate the collected experimental data on the minimum energy for photoactivation (E(a)) to the wavelengths of peak absorbance (lambda(max)) of 12 visual pigments. The E(a) values have been determined from the temperature-dependence of spectral sensitivity in the long-wavelength range. As shown previously, the simple physical idea E(a) =const. x (1/lambda(max)) (here termed the Stiles-Lewis-Barlow or SLB relation) does not hold strictly. Yet there is a significant correlation between E(a) and 1/lambda(max) (r(2)=0.73) and the regression slope obtained by an unbiased fit is 84% of the predicted value of the best SLB fit. The correlation can be decomposed into effects of A1 --> A2 chromophore change and effects of opsin differences. For a chromophore change in the same opsin, studied in two A1/A2 pigment pairs, the SLB relation holds nearly perfectly. In seven pigments having different opsins but the same (A2) chromophore, the correlation of E(a) and 1/lambda(max) remained highly significant (r(2)=0.78), but the regression coefficient is only 72% of the best SLB fit. We conclude that (1) when the chromophore is exchanged in the same opsin, the lambda(max) shift directly reflects the difference in photoactivation energies, (2) when the opsin is modified by amino acid substitutions, lambda(max) and E(a) can be tuned partly independently, although there is a dominant tendency for inverse proportionality. In four (A1) rhodopsins with virtually the same lambda(max), E(a) varied over a 4.5 kcal/mol range, which may be taken as a measure of the freedom for independent tuning. Assuming that low E(a) correlates with high thermal noise, we suggest that the leeway in lambda(max) - E(a) coupling is used by natural selection to keep E(a) as high as possible in long-wavelength-sensitive pigments, and that this is why the opsin-dependent E(a) (1/lambda(max))-relation is shallower than predicted.

Lake and sea populations of Mysis relicta (Crustacea, Mysida) with different visual-pigment absorbance spectra use the same A1 chromophore.

Glacial-relict species of the genus Mysis (opossum shrimps) inhabiting both fresh-water lakes and brackish sea waters in northern Europe show a consistent lake/sea dichotomy in eye spectral sensitivity. The absorbance peak (λmax) recorded by microspectrophotometry in isolated rhabdoms is invariably 20-30 nm red-shifted in "lake" compared with "sea" populations. The dichotomy holds across species, major opsin lineages and light environments. Chromophore exchange from A1 to A2 (retinal → 3,4-didehydroretinal) is a well-known mechanism for red-shifting visual pigments depending on environmental conditions or stages of life history, present not only in fishes and amphibians, but in some crustaceans as well. We tested the hypothesis that the lake/sea dichotomy in Mysis is due to the use of different chromophores, focussing on two populations of M. relicta from, respectively, a Finnish lake and the Baltic Sea. They are genetically very similar, having been separated for less than 10 kyr, and their rhabdoms show a typical lake/sea difference in λmax (554 nm vs. 529 nm). Gene sequencing has revealed no differences translating into amino acid substitutions in the transmembrane parts of their opsins. We determined the chromophore identity (A1 or A2) in the eyes of these two populations by HPLC, using as standards pure chromophores A1 and A2 as well as extracts from bovine (A1) and goldfish (A2) retinas. We found that the visual-pigment chromophore in both populations is A1 exclusively. Thus the spectral difference between these two populations of M. relicta is not due to the use of different chromophores. We argue that this conclusion is likely to hold for all populations of M. relicta as well as its European sibling species.

The effect of mean luminance change and grating pedestals on contrast perception: model simulations suggest a common, retinal, origin.

The percept of a contrast target is substantially affected by co-occurring changes in mean luminance or underlying ("pedestal") contrast elements. These two types of modulatory effects have traditionally been studied as separate phenomena. However, regardless of different higher-level mechanisms, both classes of phenomena will necessarily also depend on shared mechanisms in the first stages of vision, starting with the primary responses of photoreceptors. Here we present model simulations showing that important aspects of both classes may be explained by the temporal dynamics of photoreceptor responses read by integrate-and-fire operators. The model is physiologically justified and all its parameters are constrained by experimental evidence. Although there remains plenty of room for additional mechanisms to shape the exact quantitative realization of the perceptual functions in different situations, we suggest that signature features may be inherited from primary retinal signaling.

Effects of mean luminance changes on human contrast perception: contrast dependence, time-course and spatial specificity.

BACKGROUND: When we are viewing natural scenes, every saccade abruptly changes both the mean luminance and the contrast structure falling on any given retinal location. Thus it would be useful if the two were independently encoded by the visual system, even when they change simultaneously. Recordings from single neurons in the cat visual system have suggested that contrast information may be quite independently represented in neural responses to simultaneous changes in contrast and luminance. Here we test to what extent this is true in human perception. METHODOLOGY/PRINCIPAL FINDINGS: Small contrast stimuli were presented together with a 7-fold upward or downward step of mean luminance (between 185 and 1295 Td, corresponding to 14 and 98 cd/m(2)), either simultaneously or with various delays (50-800 ms). The perceived contrast of the target under the different conditions was measured with an adaptive staircase method. Over the contrast range 0.1-0.45, mainly subtractive attenuation was found. Perceived contrast decreased by 0.052±0.021 (N = 3) when target onset was simultaneous with the luminance increase. The attenuation subsided within 400 ms, and even faster after luminance decreases, where the effect was also smaller. The main results were robust against differences in target types and the size of the field over which luminance changed. CONCLUSIONS/SIGNIFICANCE: Perceived contrast is attenuated mainly by a subtractive term when coincident with a luminance change. The effect is of ecologically relevant magnitude and duration; in other words, strict contrast constancy must often fail during normal human visual behaviour. Still, the relative robustness of the contrast signal is remarkable in view of the limited dynamic response range of retinal cones. We propose a conceptual model for how early retinal signalling may allow this.