Structure and function of the optic lamina in stomatopods

Abstract

Throughout tropical coral reefs, one can find inquisitive eyes poking out of small holes belonging to often camouflaged but sometimes colourful crustaceans, the stomatopods, commonly known as mantis shrimp. Stomatopods have the most complex retinas in the world, with up to twelve colour, six polarization, and one or two luminance receptors. The apposition compound eye of stomatopods is separated into three parts: two hemispheres divided by a specialized mid-band. Behavioural tests have shown that the spectral discrimination abilities of stomatopods are surprisingly poor when compared to other animals and certainly relative to their retinal complexity. This suggests that they might not use the classical colour-opponent mechanism other colour vision systems rely on. This thesis aims to shed light on the way stomatopods process colour information, using neuroanatomy, electrophysiology, and behaviour.The first optic neuropil below the retina, the lamina, is relatively well-conserved among crustaceans and insects and this, perhaps surprisingly, includes stomatopods. The different types of neurons in the lamina of stomatopods have been partially described and are of the same type and number as in other crustaceans, but how they are connected is still unknown. I set out to describe the photoreceptor terminal morphology in the lamina and how the terminals are positioned in relation to one another, as well as relative to interneurons. Photoreceptor terminals of different spectral sensitivities appear to be in close proximity, suggesting that some sort of opponency may be taking place. Some interneurons cross lamina cartridge boundaries and communicate with other units, sometimes in different midband rows, presumably for luminance detection and calibration.Extracellular recordings of the lamina are similar to those of other insects and crustaceans. The lamina monopolar cells magnify and invert photoreceptor information, as is typical of the neuropil.To further understand colour processing in stomatopods, I investigated their ability to distinguish colour of different saturation types from grey. Previous work suggested that stomatopods may interpret colour as a pattern of photoreceptor activation, rather than compare individual signals. If this is true, they may have trouble distinguishing low saturation colours from grey because of similar activation patterns. Instead, Haptosquilla trispinosa was able to easily distinguish all colours of both high and low saturation from greys. The animals did show a decrease in performance over time in an artificial environment, which may have affected previous results.The overarching theme of this thesis was to examine at neuroanatomical, neurophysiological, and behavioural levels whether stomatopods use opponent processing, an overall pattern of photoreceptor activation, or another method to interpret visual information. A summary of new findings from the work of this thesis is as follows:• A full and corrected description of the projection of photoreceptor axons from the retina to the lamina show a more complex and reversed pattern than previously observed.• Photoreceptor R1-7 terminals in the lamina follow the pattern: R2/3/6/7 terminate in the distal lamina (epl1), with R2 and R7 terminals slightly above R3 and R6, respectively, and R1/4/5 terminate in the proximal lamina (epl2).• Reconstruction of a hemisphere lamina cartridge in two major superfamilies shows LMC1-3 as integral monopolar interneurons in both species, as well as inter-cartridge connections made by other neurons.• Partial reconstruction of lamina cartridges of midband rows 1-3 in H. trispinosa show connections between midband rows.• Initial investigation into extracellular recording from the lamina of stomatopods shows typical monopolar cell function as a summation and amplification of photoreceptor signals.• Behavioural examination of the hypothesis of colour processing as a pattern of photoreceptor activation does not account for the spectral discrimination ability of stomatopods. These results are at odds with previous findings and differences may be due to species used or as follows:• Stomatopod colour vision capabilities decrease over time spent in the artificial environment of a lab.• The species Haptosquilla trispinosa used in behavioural testing shows some colour-specific behaviours that also complicate interpretation of results.