Hanne H. Thoen

A Different Form of Color Vision in Mantis Shrimp

One of the most complex eyes in the animal kingdom can be found in species of stomatopod crustaceans (mantis shrimp), some of which have 12 different photoreceptor types, each sampling a narrow set of wavelengths ranging from deep ultraviolet to far red (300 to 720 nanometers) (1–3). Functionally, this chromatic complexity has presented a mystery (3–5). Why use 12 color channels when three or four are sufficient for fine color discrimination? Behavioral wavelength discrimination tests (Δλ functions) in stomatopods revealed a surprisingly poor performance, ruling out color vision that makes use of the conventional color-opponent coding system (6–8). Instead, our experiments suggest that stomatopods use a previously unknown color vision system based on temporal signaling combined with scanning eye movements, enabling a type of color recognition rather than discrimination. Stomatopods use multiple photoreceptors to allow rapid color recognition rather than color discrimination. [Also see Perspective by Land and Osorio] Living Technicolor Color vision is generally carried out through the number of photoreceptor types found in the retina. The mantis shrimps (stomatopods) can have up to 12 photoreceptors, far more than needed for even extreme color acuity. Thoen et al. (p. 411; see the Perspective by Land and Osorio) conducted paired color discrimination tests with stomatopods and found that their ability to discriminate among colors was surprisingly low. Instead, stomatopods appear to use a color identification approach that results from a temporal scan of an object across the 12 photoreceptor sensitivities. This entirely unique form of vision would allow for extremely rapid color recognition without the need to discriminate between wavelengths within a spectrum.

In vitro bioassay for reactive toxicity towards proteins implemented for water quality monitoring

Reactive organic chemicals comprise a large number of compounds with a variety of reactive moieties. While most assays for reactive toxicity focus on DNA damage, reactivity towards proteins can also lead to irreparable damage, but reactivity towards proteins is typically not included in any test battery for water quality assessment. Glutathione (GSH) is a small tripeptide whose cysteine moiety can serve as a model for nucleophilic sites on proteins. GSH is also an important indicator of detoxification processes and the redox status of cells and due to its protective role, depletion of GSH ultimately leads to adverse effects. A bioassay based on genetically modified Escherichia coli strains was used to quantify the specific reactivity towards the protein-like biological nucelophile GSH. The significance of GSH for detoxification was assessed by comparing the growth inhibition induced by reference chemicals or water samples in a GSH-deficient strain to its fully functional parent strain. The GSH deficient strain showed the same sensitivity as the GSH proficient strain to non-reactive and DNA damaging chemicals, but was more sensitive to chemicals that attack cysteine in proteins. The difference in effect concentrations for 50% inhibition of growth assessed as biomass increase (EC(50)) between the two strains indicates the relevance of GSH conjugation as a detoxification step as well as direct reactivity with cysteine-containing proteins. Seven reference compounds serving as positive and negative controls were investigated. The E. coli strain that lacks GSH was four times more sensitive towards the positive control Sea-Nine, while negative controls benzo[a]pyrene, 2-aminoanthracene, phenol, t-butylhydroquinone, methyl methane sulfonate and 4-nitroquinoline oxide showed equal effect concentrations in both strains. Water samples collected across an indirect potable reuse scheme representing the complete water cycle from sewage to drinking water in South East Queensland, Australia were used to evaluate the applicability of the E. coli assay for reactive toxicity in water samples. While the EC(50) values of the GSH+ strain showed similar trends as in other biological endpoints over the various treatment chains, the specific response indicative of protein damage was only observed in samples that had undergone chlorination as a disinfection process. High natural organic matter or other matrix components disturbed the bioassay so much that we recommend it for future routine testing only in tertiary treated water or drinking water.

Evolution of Neural Computations: Mantis Shrimp and Human Color Decoding

Mantis shrimp and primates both possess good color vision, but the neural implementation in the two species is very different, a reflection of the largely unrelated evolutionary lineages of these creatures. Mantis shrimp have scanning compound eyes with 12 classes of photoreceptors, and have evolved a system to decode color information at the front-end of the sensory stream. Primates have image-focusing eyes with three classes of cones, and decode color further along the visual-processing hierarchy. Despite these differences, we report a fascinating parallel between the computational strategies at the color-decoding stage in the brains of stomatopods and primates. Both species appear to use narrowly tuned cells that support interval decoding color identification.

Insect-Like Organization of the Stomatopod Central Complex: Functional and Phylogenetic Implications

One approach to investigating functional attributes of the central complex is to relate its various elaborations to pancrustacean phylogeny, to taxon-specific behavioral repertoires and ecological settings. Here we review morphological similarities between the central complex of stomatopod crustaceans and the central complex of dicondylic insects. We discuss whether their central complexes possess comparable functional properties, despite the phyletic distance separating these taxa, with mantis shrimp (Stomatopoda) belonging to the basal branch of Eumalacostraca. Stomatopods possess the most elaborate visual receptor system in nature and display a fascinating behavioral repertoire, including refined appendicular dexterity such as independently moving eyestalks. They are also unparalleled in their ability to maneuver during both swimming and substrate locomotion. Like other pancrustaceans, stomatopods possess a set of midline neuropils, called the central complex, which in dicondylic insects have been shown to mediate the selection of motor actions for a range of behaviors. As in dicondylic insects, the stomatopod central complex comprises a modular protocerebral bridge (PB) supplying decussating axons to a scalloped fan-shaped body (FB) and its accompanying ellipsoid body (EB), which is linked to a set of paired noduli and other recognized satellite regions. We consider the functional implications of these attributes in the context of stomatopod behaviors, particularly of their eyestalks that can move independently or conjointly depending on the visual scene.

An insect-like mushroom body in a crustacean brain

Mushroom bodies are the iconic learning and memory centers of insects. No previously described crustacean possesses a mushroom body as defined by strict morphological criteria although crustacean centers called hemiellipsoid bodies, which serve functions in sensory integration, have been viewed as evolutionarily convergent with mushroom bodies. Here, using key identifiers to characterize neural arrangements, we demonstrate insect-like mushroom bodies in stomatopod crustaceans (mantis shrimps). More than any other crustacean taxon, mantis shrimps display sophisticated behaviors relating to predation, spatial memory, and visual recognition comparable to those of insects. However, neuroanatomy-based cladistics suggesting close phylogenetic proximity of insects and stomatopod crustaceans conflicts with genomic evidence showing hexapods closely related to simple crustaceans called remipedes. We discuss whether corresponding anatomical phenotypes described here reflect the cerebral morphology of a common ancestor of Pancrustacea or an extraordinary example of convergent evolution.

Neural organization of afferent pathways from the stomatopod compound eye

Crustaceans and insects share many similarities of brain organization suggesting that their common ancestor possessed some components of those shared features. Stomatopods (mantis shrimps) are basal eumalacostracan crustaceans famous for their elaborate visual system, the most complex of which possesses 12 types of color photoreceptors and the ability to detect both linearly and circularly polarized light. Here, using a palette of histological methods we describe neurons and their neuropils most immediately associated with the stomatopod retina. We first provide a general overview of the major neuropil structures in the eyestalks lateral protocerebrum, with respect to the optical pathways originating from the six rows of specialized ommatidia in the stomatopods eye, termed the midband. We then focus on the structure and neuronal types of the lamina, the first optic neuropil in the stomatopod visual system. Using Golgi impregnations to resolve single neurons we identify cells in different parts of the lamina corresponding to the three different regions of the stomatopod eye (midband and the upper and lower eye halves). While the optic cartridges relating to the spectral and polarization sensitive midband ommatidia show some specializations not found in the lamina serving the upper and lower eye halves, the general morphology of the midband lamina reflects cell types elsewhere in the lamina and cell types described for other species of Eumalacostraca.

Intracellular recordings of spectral sensitivities in stomatopods: a comparison across species

Stomatopods (mantis shrimps) possess one of the most complex eyes in the world with photoreceptors detecting up to 12 different colors. It is not yet understood why stomatopods have almost four times the number of spectral photoreceptors compared with most other animals. It has, however, been suggested that these seemingly redundant photoreceptors could encode color through a new mechanism. Here we compare the spectral sensitivities across five species of stomatopods within the superfamily Gonodactyloidea using intracellular electrophysiological recordings. The results show that the spectral sensitivities across species of stomatopods are remarkably similar apart from some variation in the long-wavelength receptors. We relate these results to spectral sensitivity estimates previously obtained using microspectrophotometry and discuss the variation in the spectral sensitivity maxima (λmax) of the long-wavelength receptors in regard to the previous findings that stomatopods are able to tune their spectral sensitivities according to their respective light environment. We further discuss the similarities of the spectral sensitivities across species of stomatopods in regard to how color information might be processed by their visual systems.

Representation of the stomatopod's retinal midband in the optic lobes: Putative neural substrates for integrating chromatic, achromatic and polarization information

Stomatopods have an elaborate visual system served by a retina that is unique to this class of pancrustaceans. Its upper and lower eye hemispheres encode luminance and linear polarization while an equatorial band of photoreceptors termed the midband detects color, circularly polarized light and linear polarization in the ultraviolet. In common with many malacostracan crustaceans, stomatopods have stalked eyes, but they can move these independently within three degrees of rotational freedom. Both eyes separately use saccadic and scanning movements but they can also move in a coordinated fashion to track selected targets or maintain a forward eyestalk posture during swimming. Visual information is initially processed in the first two optic neuropils, the lamina and the medulla, where the eyes midband is represented by enlarged regions within each neuropil that contain populations of neurons, the axons of which are segregated from the neuropil regions subtending the hemispheres. Neuronal channels representing the midband extend from the medulla to the lobula where populations of putative inhibitory glutamic acid decarboxylase‐positive neurons and tyrosine hydroxylase‐positive neurons intrinsic to the lobula have specific associations with the midband. Here we investigate the organization of the midband representation in the medulla and the lobula in the context of their overall architecture. We discuss the implications of observed arrangements, in which midband inputs to the lobula send out collaterals that extend across the retinotopic mosaic pertaining to the hemispheres. This organization suggests an integrative design that diverges from the eumalacostracan ground pattern and, for the stomatopod, enables color and polarization information to be integrated with luminance information that presumably encodes shape and motion.