Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila

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Cuttlefish see shape from shading,fine-tuning coloration in response to pictorial depth cues and directional illumination

Humans use shading as a cue to three-dimensional form by combining low-level information about light intensity with high-level knowledge about objects and the environment. Here, we examine how cuttlefish Sepia officinalis respond to light and shadow to shade the white square (WS) feature in their body pattern. Cuttlefish display the WS in the presence of pebble-like objects, and they can shade it to render the appearance of surface curvature to a human observer, which might benefit camouflage. Here we test how they colour the WS on visual backgrounds containing two-dimensional circular stimuli, some of which were shaded to suggest surface curvature, whereas others were uniformly coloured or divided into dark and light semicircles. WS shading, measured by lateral asymmetry, was greatest when the animal rested on a background of shaded circles and three-dimensional hemispheres, and less on plain white circles or black/white semicircles. In addition, shading was enhanced when light fell from the lighter side of the shaded stimulus, as expected for real convex surfaces. Thus, the cuttlefish acts as if it perceives surface curvature from shading, and takes account of the direction of illumination. However, the direction of WS shading is insensitive to the directions of background shading and illumination; instead the cuttlefish tend to turn to face the light source.     

Spatiotopic perceptual maps in humans: evidence from motion adaptation

How our perceptual experience of the world remains stable and continuous despite the frequent repositioning eye movements remains very much a mystery. One possibility is that our brain actively constructs a spatiotopic representation of the world, which is anchored in external--or at least head-centred--coordinates. In this study, we show that the positional motion aftereffect (the change in apparent position after adaptation to motion) is spatially selective in external rather than retinal coordinates, whereas the classic motion aftereffect (the illusion of motion after prolonged inspection of a moving source) is selective in retinotopic coordinates. The results provide clear evidence for a spatiotopic map in humans: one which can be influenced by image motion.     

The visual ecology of a deep-sea fish,the escolar Lepidocybium flavobrunneum (Smith, 1843)

Escolar (Lepidocybium flavobrunneum, family Gempylidae) are large and darkly coloured deep-sea predatory fish found in the cold depths (more than 200 m) during the day and in warm surface waters at night. They have large eyes and an overall low density of retinal ganglion cells that endow them with a very high optical sensitivity. Escolar have banked retinae comprising six to eight layers of rods to increase the optical path length for maximal absorption of the incoming light. Their retinae possess two main areae of higher ganglion cell density, one in the ventral retina viewing the dorsal world above (with a moderate acuity of 4.6 cycles deg⁻¹), and the second in the temporal retina viewing the frontal world ahead. Electrophysiological recordings of the flicker fusion frequency (FFF) in isolated retinas indicate that escolar have slow vision, with maximal FFF at the highest light levels and temperatures (around 9 Hz at 23°C) which fall to 1–2 Hz in dim light or cooler temperatures. Our results suggest that escolar are slowly moving sit-and-wait predators. In dim, warm surface waters at night, their slow vision, moderate dorsal resolution and highly sensitive eyes may allow them to surprise prey from below that are silhouetted in the downwelling light.     

Filtering and polychromatic vision in mantis shrimps: themes in visible and ultraviolet vision

Stomatopod crustaceans have the most complex and diverse assortment of retinal photoreceptors of any animals, with 16 functional classes. The receptor classes are subdivided into sets responsible for ultraviolet vision, spatial vision, colour vision and polarization vision. Many of these receptor classes are spectrally tuned by filtering pigments located in photoreceptors or overlying optical elements. At visible wavelengths, carotenoproteins or similar substances are packed into vesicles used either as serial, intrarhabdomal filters or lateral filters. A single retina may contain a diversity of these filtering pigments paired with specific photoreceptors, and the pigments used vary between and within species both taxonomically and ecologically. Ultraviolet-filtering pigments in the crystalline cones serve to tune ultraviolet vision in these animals as well, and some ultraviolet receptors themselves act as birefringent filters to enable circular polarization vision. Stomatopods have reached an evolutionary extreme in their use of filter mechanisms to tune photoreception to habitat and behaviour, allowing them to extend the spectral range of their vision both deeper into the ultraviolet and further into the red.     

The normalized segment classification model: A new tool to compare spectral reflectance curves

1. Color patterns are complex traits under selective pressures from conspecifics, mutualists, and antagonists. To evaluate the salience of a pattern or the similarity between colors, several visual models are available. Color discrimination models estimate the perceptual difference between any two colors. Their application to a diversity of taxonomic groups has become common in the literature to answer behavioral, ecological, and evolutionary questions. To use these models, we need information about the visual system of our beholder species. However, many color patterns are simultaneously subject to selective pressures from different species, often from different taxonomic groups, with different visual systems. Furthermore, we lack information about the visual system of many species, leading ecologists to use surrogate values or theoretical estimates for model parameters.
2. Here, we present a modification of the segment classification method proposed by Endler (Biological Journal of the Linnean Society, 1990 41, 315–352): the normalized segment classification model (NSC). We explain its logic and use, exploring how NSC differs from other visual models. We also compare its predictions with available experimental data.
3. Even though the NSC model includes no information about the visual system of the receiver species, it performed better than traditional color discrimination models when predicting the output of some behavioral tasks. Although vision scientists define color as independent of stimulus brightness, a likely explanation for the goodness of fit of the NSC model is that its distance measure depends on brightness differences, and achromatic information can influence the decision‐making process of animals when chromatic information is missing.
4. Species‐specific models may be insufficient for the study of color patterns in a community context. The NSC model offers a species‐independent solution for color analyses, allowing us to calculate color differences when we ignore the intended viewer of a signal or when different species impose selective pressures on the signal.

     

The evolution of eyes and visually guided behaviour

The morphology and molecular mechanisms of animal photoreceptor cells and eyes reveal a complex pattern of duplications and co-option of genetic modules, leading to a number of different light-sensitive systems that share many components, in which clear-cut homologies are rare. On the basis of molecular and morphological findings, I discuss the functional requirements for vision and how these have constrained the evolution of eyes. The fact that natural selection on eyes acts through the consequences of visually guided behaviour leads to a concept of task-punctuated evolution, where sensory systems evolve by a sequential acquisition of sensory tasks. I identify four key innovations that, one after the other, paved the way for the evolution of efficient eyes. These innovations are (i) efficient photopigments, (ii) directionality through screening pigment, (iii) photoreceptor membrane folding, and (iv) focusing optics. A corresponding evolutionary sequence is suggested, starting at non-directional monitoring of ambient luminance and leading to comparisons of luminances within a scene, first by a scanning mode and later by parallel spatial channels in imaging eyes.     

Wide-field motion-sensitive neurons tuned to horizontal movement in the honeybee,Apis mellifera

This paper describes the morphology and response characteristics of two types of paired descending neurons (DNs) (classified as DNVII₁ and DNIV₁) and two lobula neurons (HR1 and HP1) in the honeybee, Apis mellifera.

Neurobiological constraints and fly systematics: how different types of neural characters can contribute to a higher level dipteran phylogeny

Much uncertainty still exists regarding higher level phylogenetic relationships in the insect order Diptera, and the need for independent analyses is apparent. In this paper, I present a parsimony analysis that is based on details of the nervous system of flies. Because neural characters have received little attention in modern phylogenetic analyses and the stability of neural traits has been debated, special emphasis is given to testing the robustness of the analysis itself and to evaluating how neurobiological constraints (such as levels of neural processing) influence the phylogenetic information content. The phylogenetic study is based on 14 species in three nematoceran and nine brachyceran families. All characters used in the analysis are based on anatomical details of the neural organization of the fly visual system. For the most part they relate to uniquely identifiable neurons, which are cells or cell types that can be confidently recognized as homologues among different species and thus compared. Parsimony analysis results in a phylogenetic hypothesis that favors specific previously suggested phylogenetic relationships and suggests alternatives regarding other placements. For example, several heterodactylan families (Bombyliidae, Asilidae, and Dolichopodidae) are supported in their placement as suggested by Sinclair et al. (1993), but Tipulidae and Syrphidae are placed differently. Tipulidae are placed at a derived rather than ancestral position within the Nematocera, and Syrphidae are placed within the Schizophora. The analysis suggests that neural characters generally maintain phylogenetic information well. However, by "forcing" neural characters onto conventional phylogenetic analyses it becomes apparent that not all neural centers maintain such information equally well. For example, neurons of the second-order visual neuropil, the medulla, contain stronger phylogenetic "signal" than do characters of the deeper visual center, the lobula plate. These differences may relate to different functional constraints in the two neuropils.     

The case for primate V3

The visual system in primates is represented by a remarkably large expanse of the cerebral cortex. While more precise investigative studies that can be performed in non-human primates contribute towards understanding the organization of the human brain, there are several issues of visual cortex organization in monkey species that remain unresolved. In all, more than 20 areas comprise the primate visual cortex, yet there is little agreement as to the exact number, size and visual field representation of all but three. A case in point is the third visual area, V3. It is found relatively early in the visual system hierarchy, yet over the last 40 years its organization and even its very existence have been a matter of debate among prominent neuroscientists. In this review, we discuss a large body of recent work that provides straightforward evidence for the existence of V3. In light of this, we then re-examine results from several seminal reports and provide parsimonious re-interpretations in favour of V3. We conclude with analysis of human and monkey functional magnetic resonance imaging literature to make the case that a complete V3 is an organizational feature of all primate species and may play a greater role in the dorsal stream of visual processing.     

Initial findings on visual acuity thresholds in an African elephant (Loxodonta africana)

There are only a few published examinations of elephant visual acuity. All involved Asian elephants (Elephas maximus) and found visual acuity to be between 8′ and 11′ of arc for a stimulus near the tip of the trunk, equivalent to a 0.50 cm gap, at a distance of about 2 m from the eyes. We predicted that African elephants (Loxodonta africana) would have similarly high visual acuity, necessary to facilitate eye‐trunk coordination for feeding, drinking and social interactions. When tested on a discrimination task using Landolt‐C stimuli, one African elephant cow demonstrated a visual acuity of 48′ of arc. This represents the ability to discriminate a gap as small as 2.75 cm in a stimulus 196 cm from the eye. This single‐subject study provides a preliminary estimate of the visual acuity of African elephants. Zoo Biol 29:30–35, 2010. © 2009 Wiley‐Liss, Inc.     

Early duplication and functional diversification of the opsin gene family in insects

Recent analysis of the complete mosquito Anopheles gambiae genome has revealed a far higher number of opsin genes than for either the Drosophila melanogaster genome or any other known insect. In particular, the analysis revealed an extraordinary opsin gene content expansion, whereby half are long wavelength-sensitive (LW) opsin gene duplicates. We analyzed this genomic data in relationship to other known insect opsins to estimate the relative timing of the LW opsin gene duplications and to identify "missing" paralogs in extant species. The inferred branching patterns of the LW opsin gene family phylogeny indicate at least one early gene duplication within insects before the emergence of the orders Orthoptera, Mantodea, Hymenoptera, Lepidoptera, and Diptera. These data predict the existence of one more LW opsin gene than is currently known from most insects. We tested this prediction by using a degenerate PCR strategy to screen the hymenopteran genome for novel LW opsin genes. We isolated two LW opsin gene sequences from each of five bee species, Bombus impatiens, B. terrestris, Diadasia afflicta, D. rinconis, and Osmia rufa, including 1.1 to 1.2 kb from a known (LW Rh1) and 1 kb from a new opsin gene (LW Rh2). Phylogenetic analysis suggests that the novel hymenopteran gene is orthologous to A. gambiae GPRop7, a gene that is apparently missing from D. melanogaster. Relative rate tests show that LW Rh2 is evolving at a slower rate than LW Rh1 and, therefore, may be a useful marker for higher-level hymenopteran systematics. Site-specific rate tests indicate the presence of several amino acid sites between LW Rh1 and LW Rh2 that have undergone shifts in selective constraints after duplication. These sites and others are discussed in relationship to putative structural and functional differences between the two genes.     

Photopigment spectral absorbance of Lake Malaŵi cichlids

To predict spectral sensitivity, microspectrophotometry (MSP) was used to measure absorbance of photoreceptor cells from 15 species of Lake Malaŵi cichlids. Each fish had one rod and at least three cone pigments. UV‐sensitive pigments were common, but spectral sensitivity did not clearly correlate with feeding mode or habitat.     

Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments

The peak sensitivities (λ(max)) of the short-wavelength-sensitive-1 (SWS1) pigments in mammals range from the ultraviolet (UV) (360-400 nm) to the violet (400-450 nm) regions of the spectrum. In most cases, a UV or violet peak is determined by the residue present at site 86, with Phe conferring UV sensitivity (UVS) and either Ser, Tyr or Val causing a shift to violet wavelengths. In primates, however, the tuning mechanism of violet-sensitive (VS) pigments would appear to differ. In this study, we examine the tuning mechanisms of prosimian SWS1 pigments. One species, the aye-aye, possesses a pigment with Phe86 but in vitro spectral analysis reveals a VS rather than a UVS pigment. Other residues (Cys, Ser and Val) at site 86 in prosimians also gave VS pigments. Substitution at site 86 is not, therefore, the primary mechanism for the tuning of VS pigments in primates, and phylogenetic analysis indicates that substitutions at site 86 have occurred at least five times in primate evolution. The sole potential tuning site that is conserved in all primate VS pigments is Pro93, which when substituted by Thr (as found in mammalian UVS pigments) in the aye-aye pigment shifted the peak absorbance into the UV region with a λ(max) value at 371 nm. We, therefore, conclude that the tuning of VS pigments in primates depends on Pro93, not Tyr86 as in other mammals. However, it remains uncertain whether the initial event that gave rise to the VS pigment in the ancestral primate was achieved by a Thr93Pro or a Phe86Tyr substitution.     

Eye morphology and visual acuity in the pipevine swallowtail (Battus philenor) studied with a new method of measuring interommatidial angles

Because of the important role sensory systems play in the behaviour of animals, information on sensory capabilities is of great value to behavioural ecologists in the development of hypotheses to explain behaviour. In compound eyes, interommatidial angles are a key determinant of visual acuity but methods for measuring these angles are often demanding and limited to live animals with a pseudopupil. Here we present a new technique for measuring interommatidial angles that is less demanding in terms of technology than other techniques but still accurate. It allows measurements in eyes without a pseudopupil such as dark eyes or even museum specimens. We call this technique the radius of curvature estimation (RCE) method. We describe RCE and validate the method by comparing results from RCE with those from pseudopupil analysis for the butterfly Asterocampa leilia. As an application of RCE we measure the eyes of the butterfly Battus philenor, a species whose visually guided behaviour is well known but whose eye structure and visual acuity are unknown. We discuss the results of the eye morphology in B. philenor in relation to their behaviour and ecology. We contend that RCE fills a gap in the repertoire of techniques available to study peripheral determinants of spatial resolution in compound eyes, because it can be applied on species with dark eyes. RCE then opens up for sampling a larger number of specimens, which, in combination with being able to use museum specimens, makes it possible to quantitatively test ecologically and evolutionarily driven hypotheses about vision in animals in a new way.     

Modeling dichromatic and trichromatic sensitivity to the color properties of fruits eaten by squirrel monkeys (Saimiri sciureus)

Most platyrrhines have a visual polymorphism that is characterized by the presence of multiple alleles of the M/LWS gene on the X chromosome. This polymorphism is probably maintained by selection. There are two possible mechanisms by which this can be explained: First, heterozygous females may have perceptual advantages over dichromats, such that trichromacy would be favored via the existence of different visual pigments. This is known as selection by heterosis. Second, dichromacy may be advantageous in some situations, with polymorphism being maintained by frequency-dependent selection. In this study the reflectance spectra of fruits and flowers eaten by a troop of squirrel monkeys (Saimiri sciureus) in Eastern Amazon were measured using a spectrophotometer. S. sciureus have an SWS cone with a spectral tuning of approximately 430 nm, and three M/LWS alleles with spectral tunings of 535 nm, 550 nm, and 562 nm. Based on the spectral tunings of the different phenotypes and the spectral data obtained from the food items, the responses of the different visual systems to the measured objects were modeled and then compared. The model predicted that trichromatic phenotypes would have an advantage over dichromats in detecting fruits and flowers from background foliage, which suggests that heterosis is the mechanism for maintaining polymorphism in S. sciureus. On the other hand, a large proportion of fruits could not be detected by any of the phenotypes. Additional studies are necessary to determine whether other important aspects of the primates' visual world, such as prey, predator, and conspecific detection, favor tri- or dichromacy.