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.

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.

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.

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'.

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.

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.

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.

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.

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.

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.

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).

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.

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.

Chromophore switch from 11-cis-dehydroretinal (A2) to 11-cis-retinal (A1) decreases dark noise in salamander red rods.

Dark noise, light-induced noise and responses to brief flashes of light were recorded in the membrane current of isolated rods from larval tiger salamander retina before and after bleaching most of the native visual pigment, which mainly has the 11-cis-3,4-dehydroretinal (A2) chromophore, and regenerating with the 11-cis-retinal (A1) chromophore in the same isolated rods. The purpose was to test the hypothesis that blue-shifting the pigment by switching from A2 to A1 will decrease the rate of spontaneous thermal activations and thus intrinsic light-like noise in the rod. Complete recordings were obtained in five cells (21 degrees C). Based on the wavelength of maximum absorbance, lambda max,A1 = 502 nm and lambda max,A2 = 528 nm, the average A2 : A1 ratio determined from rod spectral sensitivities and absorbances was approximately 0.74 : 0.26 in the native state and approximately 0.09 : 0.91 in the final state. In the native (A2) state, the single-quantum response (SQR) had an amplitude of 0.41 +/- 0.03 pA and an integration time of 3.16 +/- 0.15 s (mean +/- s.e.m.). The low-frequency branch of the dark noise power spectrum was consistent with discrete SQR-like events occurring at a rate of 0.238 +/- 0.026 rod(-1) s(-1). The corresponding values in the final state were 0.57 +/- 0.07 pA (SQR amplitude), 3.47 +/- 0.26 s (SQR integration time), and 0.030 +/- 0.006 rod(-1) s(-1) (rate of dark events). Thus the rate of dark events per rod and the fraction of A2 pigment both changed by ca 8-fold between the native and final states, indicating that the dark events originated mainly in A2 molecules even in the final state. By extrapolating the linear relation between event rates and A2 fraction to 0% A2 (100% A1) and 100% A2 (0% A1), we estimated that the A1 pigment is at least 36 times more stable than the A2 pigment. The noise component attributed to discrete dark events accounted for 73% of the total dark current variance in the native (A2) state and 46% in the final state. The power spectrum of the remaining 'continuous' noise component did not differ between the two states. The smaller and faster SQR in the native (A2) state is consistent with the idea that the rod behaves as if light-adapted by dark events that occur at a rate of nearly one per integration time. Both the decreased level of dark noise and the increased SQR amplitude must significantly improve the reliability of photon detection in dim light in the presence of the A1 chromophore compared to the native (A2) state in salamander rods.

Visual pigments of Baltic Sea fishes of marine and limnic origin.

Absorbance spectra of rods and some cones were measured by microspectrophotometry in 22 fish species from the brackish-water of the Baltic Sea, and when applicable, in the same species from the Atlantic Ocean (3 spp.), the Mediterranean Sea (1 sp.), or Finnish fresh-water lakes (9 spp.). The main purpose was to study whether there were differences suggesting spectral adaptation of rod vision to different photic environments during the short history (<10(4) years) of postglacial isolation of the Baltic Sea and the Finnish lakes. Rod absorbance spectra of the Baltic subspecies/populations of herring (Clupea harengus membras), flounder (Platichthys flesus), and sand goby (Pomatoschistus minutus) were all long-wavelength-shifted (9.8, 1.9, and 5.3 nm, respectively, at the wavelength of maximum absorbance, lambda(max)) compared with their truly marine counterparts, consistent with adaptation for improved quantum catch, and improved signal-to-noise ratio of vision in the Baltic light environment. Judged by the shape of the spectra, the chromophore was pure A1 in all these cases; hence the differences indicate evolutionary tuning of the opsin. In no species of fresh-water origin did we find significant opsin-based spectral shifts specific to the Baltic populations, only spectral differences due to varying A1/A2 chromophore ratio in some. For most species, rod lambda(max) fell within a wavelength range consistent with high signal-to-noise ratio of vision in the spectral conditions prevailing at depths where light becomes scarce in the respective waters. Exceptions were sandeels in the Baltic Sea, which are active only in bright light, and all species in a "brown" lake, where rod lambda(max) lay far below the theoretically optimal range.

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.

Visual pigment absorbance and spectral sensitivity of the Mysis relicta species group (Crustacea, Mysida) in different light environments.

Visual-pigment absorbance spectra and eye spectral sensitivities were examined in eight populations of opossum shrimp from different light environments. Four Finnish populations, two from the Baltic Sea and two from freshwater lakes, represent Mysis relicta, sensu stricto. The sibling species M. salemaai and M. diluviana are represented by, respectively, two Baltic Sea populations and two populations from freshwater lakes in Idaho, USA. In M. relicta, the visual pigments of the two lake populations were similar (lambda(max)=554.3+/-0.8 nm and 556.4+/-0.4 nm), but significantly red-shifted compared with the sea populations (at 529 and 535 nm) and with M. salemaai (at 521 and 525 nm). All these pigments had only A2 chromophore and the lake/sea difference indicates adaptive evolution of the opsin. In M. diluviana, lambda(max) varied in the range 505-529 nm and the shapes of spectra suggested varying A1/A2 chromophore proportions, with pure A1 in the 505 nm animals. Eye sensitivity spectra were flatter and peaked at longer wavelengths than the relevant visual-pigment templates, but declined with the same slope beyond ca. 700 nm. The deviations from visual-pigment spectra can be explained by ocular light filters based on three types of identified screening pigments.

The photoactivation energy of the visual pigment in two spectrally different populations of Mysis relicta (Crustacea, Mysida).

We report the first study of the relation between the wavelength of maximum absorbance (lambdamax) and the photoactivation energy (Ea) in invertebrate visual pigments. Two populations of the opossum shrimp Mysis relicta were compared. The two have been separated for 9,000 years and have adapted to different spectral environments ("Sea" and "Lake") with porphyropsins peaking at lambdamax=529 nm and 554 nm, respectively. The estimation of Ea was based on measurement of temperature effects on the spectral sensitivity of the eye. In accordance with theory (Stiles in Transactions of the optical convention of the worshipful company of spectacle makers. Spectacle Makers' Co., London, 1948), relative sensitivity to long wavelengths increased with rising temperature. The estimates calculated from this effect are Ea,529=47.8+/-1.8 kcal/mol and Ea,554=41.5+/-0.7 kcal/mol (different at P<0.01). Thus the red-shift of lambdamax in the "Lake" population, correlating with the long-wavelength dominated light environment, is achieved by changes in the opsin that decrease the energy gap between the ground state and the first excited state of the chromophore. We propose that this will carry a cost in terms of increased thermal noise, and that evolutionary adaptation of the visual pigment to the light environment is directed towards maximizing the signal-to-noise ratio rather than the quantum catch.